Time series models of decadal trends in the harmful algal species Karlodinium veneficum in Chesapeake Bay Harmful Algae (IF 3.087) Pub Date : 2018-02-24 Chih-Hsien (Michelle) Lin, Vyacheslav Lyubchich, Patricia M. Glibert
The harmful dinoflagellate, Karlodnium veneficum, has been implicated in fish-kill and other toxic, harmful algal bloom (HAB) events in waters worldwide. Blooms of K. veneficum are known to be related to coastal nutrient enrichment but the relationship is complex because this HAB taxon relies not only on dissolved nutrients but also particulate prey, both of which have also changed over time. Here, applying cross-correlations of climate-related physical factors, nutrients and prey, with abundance of K. veneficum over a 10-year (2002–2011) period, a synthesis of the interactive effects of multiple factors on this species was developed for Chesapeake Bay, where blooms of the HAB have been increasing. Significant upward trends in the time series of K. veneficum were observed in the mesohaline stations of the Bay, but not in oligohaline tributary stations. For the mesohaline regions, riverine sources of nutrients with seasonal lags, together with particulate prey with zero lag, explained 15%–46% of the variation in the K. veneficum time series. For the oligohaline regions, nutrients and particulate prey generally showed significant decreasing trends with time, likely a reflection of nutrient reduction efforts. A conceptual model of mid-Bay blooms is presented, in which K. veneficum, derived from the oceanic end member of the Bay, may experience enhanced growth if it encounters prey originating from the tributaries with different patterns of nutrient loading and which are enriched in nitrogen. For all correlation models developed herein, prey abundance was a primary factor in predicting K. veneficum abundance.
Thermal acclimation affects growth and lipophilic toxin production in a strain of cosmopolitan harmful alga Dinophysis acuminata Harmful Algae (IF 3.087) Pub Date : 2018-02-24 Leila Basti, Toshiyuki Suzuki, Hajime Uchida, Takashi Kamiyama, Satoshi Nagai
Species of the harmful algal bloom (HAB) genera Dinophysis are causative of one of the most widespread and expanding HAB events associated with the human intoxication, diarrheic shellfish poisoning (DSP). The effects of warming temperature on the physiology and toxinology of these mixotrophic species remain intractable due to their low biomass in nature and difficulties in establishing and maintaining them in culture. Hence, the present study investigated the influence of warming temperature, encompassing present and predicted climate scenarios, on growth and toxin production in a strain of the most cosmopolitan DSP-causative species, Dinophysis acuminata. The strain was isolated from western Japan, acclimated, and cultured over extended time spans. The specific growth and toxin production rates were highest at 20–26 °C and 17–29 °C, respectively, and had significant linear relationships during exponential phase. The cellular toxin production of okadaic acid and pectenotoxin-2 were highest during early exponential growth phase at temperatures ≤17 °C but highest during late stationary phase at temperatures ≥20 °C. The cellular toxin production of Dinophysistoxin-1, however, increased from early exponential to late stationary growth phase independently from temperature. The net toxin productions were not affected by acclimation temperature but significantly affected by growth and were highest during early exponential growth phase. Warming water temperatures increase growth and promote toxin production of D. acuminata, potentially increasing incidence of diarrheic shellfish poisoning events and closures of shellfish production. It is likely that D. acuminata is more toxic at low cell densities during bloom initiation in winter, and at high cell densities during bloom termination in spring-autumn. The results of the present research are also of importance for the mass production of D. acuminata for subsequent studies of the toxicological and pharmacological bioactivities of DSTs and PTX2, and the fate of these toxins in the natural environment and the vectoring shellfish molluscs.
Feeding and grazing impact by the bloom-forming euglenophyte Eutreptiella eupharyngea on marine eubacteria and cyanobacteria Harmful Algae (IF 3.087) Pub Date : 2018-02-21 Yeong Du Yoo, Kyeong Ah Seong, Hyung Seop Kim, Hae Jin Jeong, Eun Young Yoon, Jaeyeon Park, Jong Im Kim, Woongghi Shin, Brian Palenik
The phototrophic euglenophyte Eutreptiella eupharyngea often causes blooms in the coastal waters of many countries, but its mode of nutrition has not been assessed. This species has previously been considered as exclusively auxotrophic. To explore whether E. eupharyngea is a mixotrophic species, the protoplasm of E. eupharyngea cells were examined using light, epifluorescence, and transmission electron microscopy after eubacteria, the cyanobacterium Synechococcus sp., and diverse algal species were provided as potential prey. Furthermore, the ingestion rates of E. eupharyngea KR on eubacteria or Synechococcus sp. as a function of prey concentration were measured. In addition, grazing by natural populations of euglenophytes on natural populations of eubacteria in Masan Bay was investigated. This study is the first to report that E. eupharyngea is a mixotrophic species. Among the potential prey organisms offered, E. eupharyngea fed only on eubacteria and Synechococcus sp., and the maximum ingestion rates of these two organisms measured in the laboratory were 5.7 and 0.7 cells predator−1 h−1, respectively. During the field experiments, the maximum ingestion rates and grazing impacts of euglenophytes, including E. eupharyngea, on natural populations of eubacteria were 11.8 cells predator−1 h−1 and 1.228 d−1, respectively. Therefore, euglenophytes could potentially have a considerable grazing impact on marine bacterial populations.
Revealing the distinct habitat ranges and hybrid zone of genetic sub-populations within Pseudo-nitzschia pungens (Bacillariophyceae) in the West Pacific area Harmful Algae (IF 3.087) Pub Date : 2018-02-05 Jin Ho Kim, Pengbin Wang, Bum Soo Park, Joo-Hwan Kim, Shailesh Kumar Patidar, Myung-Soo Han
Genetic sub-populations (clades) of cosmopolitan marine diatom Pseudo-nitzschia pungens might have distinct habitats, and their hybrid zone is suspected in higher latitude area of the West Pacific area, however, it is still unrevealed because of technical difficulties and lack of evidences in natural environments. The aim of this study is to investigate the habitat characteristics of each clade of P. pungens on geographical distribution with the habitat temperature ranges of each clade and to reveal their hybrid zone in the West Pacific area. We employed the 137 number of nucleotide sequences of P. pungens and its sampling data (spatial and temporal scale) originated from the West Pacific area, and used field application of qPCR assay for intra-specific level of P. pungens. Only two genotypes, clade I and III, were identified in the West Pacific area. Clade I was distributed from 39 to 32.3°N, and clade III were from 1.4 to 34.4°N. The estimated habitat temperature for the clade I and clade III ranges were 8.1–26.9 °C and 24.2–31.2 °C, respectively. The latitudinal distributions and temperature ranges of each clade were significantly different. The qPCR assay employed, and results suggested that the hybrid zone for clade I and III has been observed in the southern Korean coasts, and clade III might be introduced from the Southern Pacific area. The cell abundances of clade III were strongly related with the higher seawater temperature and warm current force. This study has defined distinct habitat characteristics of genetically different sub-populations of P. pungens, and revealed its hybrid zone in natural environment for the first time. We also provided strong evidences about dispersion of the population of clade III to higher latitude in the West Pacific area.
Comparison of loop-mediated isothermal amplification with hyperbranched rolling circle amplification as a simple detection method for Heterosigma akashiwo Harmful Algae (IF 3.087) Pub Date : 2018-02-02 Chunyun Zhang, Yuanyuan Wang, Changlu Guo, Guofu Chen, Guangfeng Kan, Panpan Cai, Jin Zhou
The fish-killing alga Heterosigma akashiwo is a globally distributed, toxic, and bloom-forming raphidophyte that has caused great losses to the fishing industry in many coastal countries. Therefore, rapid and sensitive detection methods should be developed to present timely warning of harmful algal blooms. In this study, hyperbranched rolling circle amplification (HRCA) was established for the detection of H. akashiwo and compared with loop-mediated isothermal amplification (LAMP) in terms of specificity and sensitivity. The partial D1–D2 sequence of the large subunit (LSU) of rDNA of H. akashiwo was used to design a specific padlock probe for HRCA and two pairs of specific primers for LAMP. The parameters for HRCA were optimized. Cross-reactivity tests showed that the specificity of the developed HRCA for H. akashiwo was greater than that of LAMP in this study. The sensitivities of HRCA and LAMP were comparable and were 10-fold higher than that of regular PCR. These methods also yielded a detection limit of 20 fg/μL for the recombinant plasmid containing the target LSU D1–D2 and 1 cell for target species. The test with the simulated field samples indicated that the developed HRCA obtained a detection limit of 5 cells mL−1, which was lower than the warning cell density (100 cells mL−1) of H. akashiwo. The visual detection of positive HRCA could be achieved via coloration reaction with the addition of fluorescent SYBR Green I dye to the amplification products. The developed HRCA was also efficient for field samples with target cell densities ranging from 10 cells mL−1 to 1000 cells mL−1. Therefore, the proposed HRCA detection protocols are possibly applicable to the field monitoring of H. akashiwo.
Differential toxin response of Pseudo-nitzschia multiseries as a function of nitrogen speciation in batch and continuous cultures, and during a natural assemblage experiment Harmful Algae (IF 3.087) Pub Date : 2018-02-04 Regina L. Radan, William P. Cochlan
The toxigenic diatom Pseudo-nitzschia multiseries Hasle, isolated from the U.S. Pacific Northwest, was examined in unialgal laboratory cultures and in natural assemblages during shipboard experiments, to examine cellular growth and domoic acid (DA) production as a function of nitrogen (N) substrate and availability expected during bloom development and decline. Laboratory experiments utilizing batch cultures conducted at saturating (120 μmol photons m−2 s−1) photosynthetic photon flux density (PPFD), demonstrated that P. multiseries (strain NWFSC-245) grows equally well on the three N substrates tested (nitrate [NO3−], ammonium [NH4+] and urea), and achieved an average specific growth rate of 0.83 d−1. Despite equivalent growth rates, cellular toxicity (particulate DA concentration normalized to cell abundance) varied as a function of N substrate, with urea-grown cells demonstrating 1.3- and 3.4-fold more toxicity than both NH4+- and NO3−-grown cells. Cellular toxicity of the N-limited chemostat cultures, grown at a dilution rate of 0.48 d−1, were less than the cellular toxicity measured for the N-replete batch cultures for all three N substrates, but again cellular toxicity varied as a function of N substrate and the urea-supported cells were 3.5- and 4.3-fold more toxic than the respective NH4+- and NO3−-supported cells. Starved cultures of P. multiseries showed no decline in cellular toxicity or change in the order of toxicity as a function of N substrate, and cells previously supported by urea were 13- and 5-fold more toxic than NH4+- and NO3−-supported cells. At all three levels of N-sufficiency, the urea-grown cells consistently produced the highest concentration of particulate DA per cell compared to cells grown on either NO3− or NH4+. Shipboard N enrichment experiments using natural phytoplankton assemblages were conducted off the west coast of Washington in an area characterized by elevated concentrations of macronutrients and iron. All N (NO3−, NH4+ and urea) treatments showed significant increases in biomass (as measured by total and size-fractionated chlorophyll a) and the abundance of Pseudo-nitzschia species over the 6-d experiment. As with the unialgal laboratory experiments, cellular toxicity varied as a function of the N source supporting growth, and the planktonic assemblages enriched with either NH4+ or urea demonstrated greater cellular toxicity than the assemblages supported solely by NO3−. These laboratory and field results demonstrate that N substrate can regulate the toxicity of Pseudo-nitzschia species, and that N source should be considered when evaluating the potential effects of cultural eutrophication on the growth of toxigenic diatoms.
Consortial brown tide − picocyanobacteria blooms in Guantánamo Bay, Cuba Harmful Algae (IF 3.087) Pub Date : 2018-02-04 Nathan S. Hall, R. Wayne Litaker, W. Judson Kenworthy, Mark W. Vandersea, William G. Sunda, James P. Reid, Daniel H. Slone, Susan Butler
Life histories of microalgal species causing harmful blooms: Haploids, diploids and the relevance of benthic stages Harmful Algae (IF 3.087) Pub Date : 2018-02-04 Rosa Isabel Figueroa, Marta Estrada, Esther Garcés
In coastal and offshore waters, Harmful Algal Blooms (HABs) currently threaten the well-being of coastal countries. These events, which can be localized or involve wide-ranging areas, pose risks to human health, marine ecosystems, and economic resources, such as tourism, fisheries, and aquaculture. Dynamics of HABs vary from one site to another, depending on the hydrographic and ecological conditions. The challenge in investigating HABs is that they are caused by organisms from multiple algal classes, each with its own unique features, including different life histories. The complete algal life cycle has been determined in <1% of the described species, although elucidation of the life cycles of bloom-forming species is essential in developing preventative measures. The knowledge obtained thus far has confirmed the complexity of the algal life cycle, which is composed of discrete life stages whose morphology, ecological niche (plankton/benthos), function, and lifespan vary. The factors that trigger transitions between the different stages in nature are mostly unknown, but it is clear that an understanding of this process provides the key to effectively forecasting bloom recurrence, maintenance, and decline. Planktonic stages constitute an ephemeral phase of the life cycle of most species whereas resistant, benthic stages enable a species to withstand adverse conditions for prolonged periods, thus providing dormant reservoirs for eventual blooms and facilitating organismal dispersal. Here we review current knowledge of the life cycle strategies of major groups of HAB producers in marine and brackish waters. Rather than providing a comprehensive discussion, the objective was to highlight several of the research milestones that have changed our understanding of the plasticity and frequency of the different life cycle stages as well as the transitions between them. We also discuss the relevance of benthic and planktonic forms and their implications for HAB dynamics.
Phylogeny and salt-tolerance of freshwater Nostocales strains: Contribution to their systematics and evolution Harmful Algae (IF 3.087) Pub Date : 2018-02-04 Charlotte Duval, Solène Thomazeau, Yannick Drelin, Claude Yéprémian, Marc Bouvy, Arnaud Couloux, Marc Troussellier, Florence Rousseau, Cécile Bernard
Phylogenetic relationships among heterocytous genera (the Nostocales order) have been profoundly modified since the use of polyphasic approaches that include molecular data. There is nonetheless still ample scope for improving phylogenetic delineations of genera with broad ecological distributions, particularly by integrating specimens from specific or up-to-now poorly sampled habitats. In this context, we studied 36 new isolates belonging to Chrysosporum, Dolichospermum, Anabaena, Anabaenopsis, and Cylindrospermopsis from freshwater ecosystems of Burkina-Faso, Senegal, and Mayotte Island. Studying strains from these habitats is of particular interest as we suspected different range of salt variations during underwent periods of drought in small ponds and lakes. Such salt variation may cause different adaptation to salinity. We then undertook a polyphasic approach, combining molecular phylogenies, morphological analyses, and physiological measurements of tolerance to salinity. Molecular phylogenies of 117 Nostocales sequences showed that the 36 studied strains were distributed in seven lineages: Dolichospermum, Chrysosporum, Cylindrospermopsis/Raphidiopsis, Anabaenopsis, Anabaena sphaerica var tenuis/Sphaerospermopsis, and two independent Anabaena sphaerica lineages. Physiological data were congruent with molecular results supporting the separation into seven lineages. In an evolutionary context, salinity tolerance can be used as an integrative marker to reinforce the delineation of some cyanobacterial lineages. The history of this physiological trait contributes to a better understanding of processes leading to the divergence of cyanobacteria. In this study, most of the cyanobacterial strains isolated from freshwater environments were salt-tolerant, thus suggesting this trait constituted an ancestral trait of the heterocytous cyanobacteria and that it was probably lost two times secondarily and independently in the ancestor of Dolichospermum and of Cylindrospermopsis.
Akinete germination chamber: An experimental device for cyanobacterial akinete germination and plankton emergence Harmful Algae (IF 3.087) Pub Date : 2018-02-03 Chae-Hong Park, Myung-Hwan Park, Keun Hee Kim, Jung-Hwan Park, Dae-Ryul Kwon, Nan Young Kim, Byung-Jin Lim, Soon-Jin Hwang
Niche separation of Baltic Sea cyanobacteria during bloom events by species interactions and autecological preferences Harmful Algae (IF 3.087) Pub Date : 2018-01-13 Falk Eigemann, Marc Schwartke, Heide Schulz-Vogt
Effects of modified clay used for the control of harmful algal blooms on Alexandrium pacificum cysts Harmful Algae (IF 3.087) Pub Date : Yue Zhang, Zhiming Yu, Xiuxian Song, Yongquan Yuan, Xihua Cao
Cyst formation plays an important role in the resistance of dinoflagellates to adverse environments, and cyst germination is considered one of the causes of harmful algal blooms (HABs). Among the methods for mitigating HABs, modified clay (MC) is considered a promising strategy because of its high efficiency and low environmental impacts. The typical HAB species Alexandrium pacificum was focused on in this study to clarify the effects of MC on cyst formation and germination. The results showed that more than 90% of the vegetative cells were removed under the 0.6 g/L MC treatment. The vegetative cell density was monitored over 90 d and increased slightly to the peak at 10 d after the cell removal experiment, but persistent growth was not observed. The amount of cysts was maximal at 20 d after removal, however, most of the cysts were temporary cysts that subsequently disappeared. After 80 d, all the remaining cysts were resting ones. The total density of resting cysts was higher under MC concentrations of 0.2 and 0.4 g/L and lower under concentrations of 0.6, 0.8 and 1.0 g/L compared with that in the control. The total formation rate of resting cysts was 29.6% in the control group, and the lowest formation rate in the experimental groups was 15.5% at 0.6 g/L MC. The total germination rate of resting cyst decreased as the MC concentration increased, and approximately 68.0% of the resting cysts in the control group germinated successfully, whereas the addition of MC reduced the germination rate to as low as 12.4%. Our results indicated that the application of appropriate MC concentrations may provide an effective mitigation strategy for A. pacificum blooms because it does not leave more residual cysts, which can act as “seeds” for the initiation of HABs.
Molecular detection of harmful cyanobacteria and expression of their toxin genes in Dutch lakes using multi-probe RNA chips Harmful Algae (IF 3.087) Pub Date : 2018-01-06 Dedmer B. Van de Waal, Delphine Guillebault, Amparo Alfonso, Inés Rodríguez, Luis M. Botana, Ronald Bijkerk, Linda K. Medlin
Harmful cyanobacterial blooms are a major threat to water quality and human health. Adequate risk assessment is thus required, which relies strongly on comprehensive monitoring. Here, we tested novel multi-probe RNA chips developed in the European project, μAqua, to determine the abundance of harmful cyanobacterial species and expression of selected toxin genes in six Dutch lakes. All of the targeted cyanobacterial genera, except for Planktothrix, were detected using the microarray, with predominance of Dolichospermum and Microcystis signals, of which the former was found across all sites and detected by the probes for Anabaena where it was formerly placed. These were confirmed by microscopic cell counts at three sites, whereas at the other sites, microscopic cell counts were lower. Probe signals of Microcystis showed larger variation across sites but also matched microscopic counts for three sites. At the other sites, microscopic counts were distinctly higher. We detected anatoxin-a in the water at all sites, but unfortunately no genes for this toxin were on this generation of the toxin array. For microcystins, we found none or low concentrations in the water, despite high population densities of putative microcystin producers (i.e. Microcystis, Dolichospermum). The described method requires further testing with a wider range of cyanobacterial communities and toxin concentrations before implementation into routine cyanobacterial risk assessment. Yet, our results demonstrate a great potential for applying multi-probe RNA chips for species as well as toxins to eutrophic waters with high cyanobacterial densities as a routine monitoring tool and as a predictive tool for toxin potential.
Brevetoxin (PbTx-2) influences the redox status and NPQ of Karenia brevis by way of thioredoxin reductase Harmful Algae (IF 3.087) Pub Date : 2018-01-03 Wei Chen, Ricardo Colon, J.William Louda, Freddy Rodriguez del Rey, Michaella Durham, Kathleen S. Rein
Advection of Karenia brevis blooms from the Florida Panhandle towards Mississippi coastal waters Harmful Algae (IF 3.087) Pub Date : 2018-01-02 Inia M. Soto, Mustafa Kemal Cambazoglu, Adam D. Boyette, Kristina Broussard, Drew Sheehan, Stephan D. Howden, Alan M. Shiller, Brian Dzwonkowski, Laura Hode, Patrick J. Fitzpatrick, Robert A. Arnone, Paul F. Mickle, Kimberly Cressman
Harmful Algal Blooms (HABs) of Karenia brevis have been documented along coastal waters of every state bordering the Gulf of Mexico (GoM). Some Gulf Coast locations, such as Florida and Texas, suffer from recurrent intense and spatially large blooms, while others such as Mississippi seem to rarely observe them. The main objective of this work is to understand the dynamics that led to the K. brevis bloom in Mississippi coastal waters in fall 2015. Blooms of K. brevis from the Florida Panhandle region are often advected westward towards the Mississippi-Alabama coast; however there is interannual variability in their presence and intensity in Mississippi coastal waters. The 2015 K. brevis bloom was compared to the 2007 Florida Panhandle K. brevis bloom, which showed a westward advection pattern, but did not intensify along the Mississippi coast. Cell counts and flow cytometry were obtained from the Mississippi Department of Marine Resources, Alabama Department of Public Health, Florida Fish and Wildlife Conservation Commission and The University of Southern Mississippi. Ocean color satellite imagery from the Moderate Resolution Imaging Spectroradiometer onboard the Aqua satellite was used to detect and delineate the blooms in 2007 and 2015. Two different regional applications of NCOM-Navy Coastal Ocean Model (1-km resolution NCOM-GoM/Gulf of Mexico and 6-km resolution NCOM-IASNFS/Intra Americas Sea Nowcast Forecast System) were used to understand the circulation and transport pathways. A Lagrangian particle tracking software was used to track the passive movement of particles released at different locations for both bloom events. Ancillary data (e.g., nutrients, wind, salinity, river discharge) from local buoys, monitoring stations and coincident oceanographic cruises were also included in the analysis. The blooms of K. brevis reached the Mississippi coast both years; however, the bloom in 2007 lasted only a few days and there is no evidence that it entered the Mississippi Sound. Two major differences were observed between both years. First, circulation patterns in 2015 resulting from an intense westward-northwestward that persisted until December allowed for continuous advection, whereas this pattern was not evident in 2007. Second, local river discharge was elevated throughout late fall 2015 while 2007 was below the average. Thus, elevated discharge may have provided sufficient nutrients for bloom intensification. These results illustrate the complex, but important interactions in coastal zones. Further, they emphasize the importance in establishing comprehensive HAB monitoring programs, which facilitate our understanding of nutrient and phytoplankton dynamics, and stress the importance for multi-agency cooperation across state boundaries.
Realized niche analysis of phytoplankton communities involving HAB: Phaeocystis spp. as a case study Harmful Algae (IF 3.087) Pub Date : 2017-12-27 Stéphane Karasiewicz, Elsa Breton, Alain Lefebvre, Tania Hernández Fariñas, Sébastien Lefebvre
The link between harmful algal blooms, phytoplankton community dynamics and global environmental change is not well understood. To tackle this challenging question, a new method was used to reveal how phytoplankton communities responded to environmental change with the occurrence of an harmful algae, using the coastal waters of the eastern English Channel as a case study. The great interannual variability in the magnitude and intensity of Phaeocystis spp. blooms, along with diatoms, compared to the ongoing gradual decrease in anthropogenic nutrient concentration and rebalancing of nutrient ratios; suggests that other factors, such as competition for resources, may also play an important role. A realized niche approach was used with the Outlying Mean Index analysis and the dynamics of the species’ realized subniches were estimated using the Within Outlying Mean Indexes calculations under low (L) and high (H) contrasting Phaeocystis spp. abundance. The Within Outlying Mean Indexes allows the decomposition of the realized niche into realized subniches, found within the subset of habitat conditions and constrained by a subset of a biotic factor. The two contrasting scenarios were characterized by significantly different subsets of environmental conditions and diatom species (BV-step analysis), and different seasonality in salinity, turbidity, and nutrients. The subset L environmental conditions were potentially favorable for Phaeocystis spp. but it suffered from competitive exclusion by key diatom species such as Skeletonema spp., Thalassiosira gravida, Thalassionema nitzschioides and the Pseudo-nitzchia seriata complex. Accordingly, these diatoms species occupied 81% of Phaeocystis spp.'s existing fundamental subniche. In contrast, the greater number of diatoms, correlated with the community trend, within subset H exerted a weaker biological constraint and favored Phaeocystis spp. realized subniche expansion. In conclusion, the results strongly suggest that both abiotic and biotic interactions should be considered to understand Phaeocystis spp. blooms with greater consideration of the preceeding diatoms. HABs needs must therefore be studied as part of the total phytoplankton community.
Colony formation in two Microcystis morphotypes: Effects of temperature and nutrient availability Harmful Algae (IF 3.087) Pub Date : 2017-12-26 Zhipeng Duan, Xiao Tan, Keshab Parajuli, Sanjina Upadhyay, Danfeng Zhang, Xiaoqian Shu, Qianqian Liu
The ability of Microcystis to form large colonies is a key trait that contributes to competition ability over other phytoplankton and facilitates the formation of surface scums in many freshwater systems. The effect of temperature and nutrients on this trait, however, is far from clear and needs further investigation, especially under a warmer climate and nutrient overloading in aquatic systems globally. In this study, two colonial strains of Microcystis (M. wesenbergii and M. ichthyoblabe) originally isolated from Lake Taihu in China, were used to investigate cyanobacterial aggregation under a range of temperatures (15–30 °C), phosphorus availability (0.004–8 mg P L−1), and nitrogen availability (0.04–40 mg N L−1). The mechanism of colony formation in Microcystis was determined based on growth rates and extracellular polysaccharide (EPS) contents. The colony size of both strains increased significantly when the temperature rose from 15 to 25 °C. A further increase in temperature from 25 to 30 °C, however, reduced the colony size of M. ichthyoblabe significantly, and, in contrast, increased the colony size of M. wesenbergii. Higher phosphorus availability promoted the formation of larger colonies in both strains. In comparison, nitrogen had no significant effect on the colony size. Furthermore, although EPS was a significant contributor to the formation of large colonies in colonial Microcystis, growth rate was a dominant driving factor in this process. The findings of this study highlight that warmer temperatures and phosphorus enrichment might enhance surface Microcystis scums directly through increasing the colony size. This study also provides new insights into the mechanism of colony formation in Microcystis.
Intraspecific bloom succession in the harmful dinoflagellate Cochlodinium polykrikoides (Dinophyceae) extended the blooming period in Korean coastal waters in 2009 Harmful Algae (IF 3.087) Pub Date : 2017-12-18 Bum Soo Park, Jin Ho Kim, Joo-Hwan Kim, Seung Ho Baek, Myung-Soo Han
Although there have been extensive studies on dinoflagellate blooms in recent decades, the mechanism that allows the maintenance of blooms over long periods remains uncertain, and studies on genetically differentiated subpopulations may provide insights into this mechanism. In this study, the influence of two genetically distinct subpopulations of the dinoflagellate Cochlodinium polykrikoides, referred to as Group I and IV, on bloom duration in Korean coastal waters (KCW) was examined using a quantitative PCR (qPCR) assay. In this study, a C. polykrikoides bloom occurred over a longer period in 2009 (49 days), whereas the bloom period was shorter in 2010 (35 days). The qPCR results indicate that intraspecific bloom succession between Groups I and IV occurred in 2009, whereas only a single subpopulation (Group I) was responsible for the bloom in 2010. Based on the statistical analysis, the Group I and Group IV blooms occurred under significantly different environmental conditions (p ≤ 0.05) in terms of water temperature, pH, and phosphate concentration, and these subpopulations exhibited significantly different relationships with environmental factors, particularly water temperature (p < 0.01). This variability may allow blooms to continue through intraspecific bloom succession even after environmental conditions change. Southern KCW are affected by outer regions via the Tsushima Warm Current (TWC) every summer. Group IV (≤1108 ± 69 cells L−1) was primarily observed along the route of the TWC in summer 2009, when the bloom of this subpopulation occurred in southern KCW. These results suggest that Group IV transported via the TWC may have influenced the bloom dynamics of this subpopulation in summer 2009.
Variable allelopathy among phytoplankton reflected in red tide metabolome Harmful Algae (IF 3.087) Pub Date : 2017-12-15 Remington X. Poulin, Kelsey L. Poulson-Ellestad, Jessie S. Roy, Julia Kubanek
Harmful algae are known to utilize allelopathy, the release of compounds that inhibit competitors, as a form of interference competition. Competitor responses to allelopathy are species-specific and allelopathic potency of producing algae is variable. In the current study, the biological variability in allelopathic potency was mapped to the underlying chemical variation in the exuded metabolomes of five genetic strains of the red tide dinoflagellate Karenia brevis using 1H nuclear magnetic resonance (NMR) spectroscopy. The impacts of K. brevis allelopathy on growth of a model competitor, Asterionellopsis glacialis, ranged from strongly inhibitory to negligible to strongly stimulatory. Unique metabolomes of K. brevis were visualized as chemical fingerprints, suggesting three distinct metabolic modalities – allelopathic, non-allelopathic, and stimulatory – with each modality distinguished from the others by different concentrations of several metabolites. Allelopathic K. brevis was characterized by enhanced concentrations of fatty acid-derived lipids and aromatic or other polyunsaturated compounds, relative to less allelopathic K. brevis. These findings point to a previously untapped source of information in the study of allelopathy: the chemical variability of phytoplankton, which has been underutilized in the study of bloom dynamics and plankton chemical ecology.
Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum Harmful Algae (IF 3.087) Pub Date : 2017-12-16 Kenneth Neil Mertens, M. Consuelo Carbonell-Moore, Vera Pospelova, Martin J. Head, Andrea Highfield, Declan Schroeder, Haifeng Gu, Karl B. Andree, Margarita Fernandez, Aika Yamaguchi, Yoshihito Takano, Kazumi Matsuoka, Elisabeth Nézan, Gwenael Bilien, Yuri Okolodkov, Kazuhiko Koike, Mona Hoppenrath, Maya Pfaff, Grant Pitcher, Abdulrahman Al-Muftah, André Rochon, Po Teen Lim, Chui Pin Leaw, Zhen Fei Lim, Marianne Ellegaard
Strains of a dinoflagellate from the Salton Sea, previously identified as Protoceratium reticulatum and yessotoxin producing, have been reexamined morphologically and genetically and Pentaplacodinium saltonense n. gen. et sp. is erected to accommodate this species. Pentaplacodinium saltonense differs from Protoceratium reticulatum (Claparède et Lachmann 1859) Bütschli 1885 in the number of precingular plates (five vs. six), cingular displacement (two widths vs. one), and distinct cyst morphology. Incubation experiments (excystment and encystment) show that the resting cyst of Pentaplacodinium saltonense is morphologically most similar to the cyst-defined species Operculodinium israelianum (Rossignol, 1962) Wall (1967) and O. psilatum Wall (1967). Collections of comparative material from around the globe (including Protoceratium reticulatum and the genus Ceratocorys) and single cell PCR were used to clarify molecular phylogenies. Variable regions in the LSU (three new sequences), SSU (12 new sequences) and intergenic ITS 1–2 (14 new sequences) were obtained. These show that Pentaplacodinium saltonense and Protoceratium reticulatum form two distinct clades. Pentaplacodinium saltonense forms a monophyletic clade with several unidentified strains from Malaysia. LSU and SSU rDNA sequences of three species of Ceratocorys (C. armata, C. gourreti, C. horrida) from the Mediterranean and several other unidentified strains from Malaysia form a well-supported sister clade. The unique phylogenetic position of an unidentified strain from Hawaii is also documented and requires further examination. In addition, based on the V9 SSU topology (bootstrap values >80%), specimens from Elands Bay (South Africa), originally described as Gonyaulax grindleyi by Reinecke (1967), cluster with Protoceratium reticulatum. The known range of Pentaplacodinium saltonense is tropical to subtropical, and its cyst is recorded as a fossil in upper Cenozoic sediments. Protoceratium reticulatum and Pentaplacodinium saltonense seem to inhabit different niches: motile stages of these dinoflagellates have not been found in the same plankton sample.
Growth-suppressing and algicidal properties of an extract from Arundo donax, an invasive riparian plant, against Prymnesium parvum, an invasive harmful alga Harmful Algae (IF 3.087) Pub Date : 2017-11-23 Reynaldo Patiño, Rakib H. Rashel, Amede Rubio, Scott Longing
This study examined the ability of acidic and neutral/alkaline fractions of a methanolic extract from giant reed (Arundo donax) and of two of its constituents, gramine and skatole, to inhibit growth of the ichthyotoxic golden alga (Prymnesium parvum) in batch culture. For this study, growth suppression was defined as inhibition of maximum cell density, algicidal activity as early occurrence of negative growth, and algistatic activity as lack of net growth. The acidic fraction did not affect algal growth. The neutral/alkaline fraction showed growth-suppressing and algicidal activities but no signs of algistatic activity – namely, cells in cultures surviving a partial-algicidal exposure concentration (causing transient negative growth) were later able to initiate positive growth but at higher concentrations, algicidal activity was full and irreversible. Gramine suppressed growth more effectively than skatole and at the highest concentration tested, gramine also showed partial-algicidal and algistatic activity. While the partial-algicidal activities of the neutral/alkaline fraction and of gramine were short-lived (≤6 days) and thus may share similar mechanisms, algistatic activity was unique to gramine and persisted for >3 weeks. Given gramine’s reported concentration in the neutral/alkaline fraction, its corresponding level of algicidal activity is much lower than the fraction’s suggesting the latter contains additional potent algicides. Inhibition of maximum cell density by all test compounds was associated with reductions in exponential growth rate, and in the case of the neutral/alkaline fraction and gramine also reductions in early (pre-exponential) growth. These results indicate that giant reed is a potential source of natural products to control golden alga blooms. Giant reed is an invasive species in North America, thus also providing incentive for research into strategies to couple management efforts for both species.
Effects of increased zooplankton biomass on phytoplankton and cyanotoxins: A tropical mesocosm study Harmful Algae (IF 3.087) Pub Date : 2017-11-23 Juliana dos Santos Severiano, Viviane Lúcia dos Santos Almeida-Melo, Maria do Carmo Bittencourt-Oliveira, Mathias Ahii Chia, Ariadne do Nascimento Moura
Zooplankton are important biocontrol agents for algal blooms in temperate lakes, while their potential in tropical and subtropical environments is not well understood. The aim of the present study was to evaluate the influence of increased zooplankton biomass on phytoplankton community and cyanotoxins (microcystins and saxitoxin) content of a tropical reservoir (Ipojuca reservoir, Brazil) using in situ mesocosms. Mesocosms consisted of 50 L transparent polyethylene bags suspended in the reservoir for twelve days. Phytoplankton populations were exposed to treatments having 1 (control), 2, 3 and 4 times the biomass of zooplankton found in the reservoir at the beginning of the experiment. Filamentous cyanobacteria such as Planktothrix agardhii and Cylindrospermopsis raciborskii were not negatively influenced by increasing zooplankton biomass. In contrast, the treatments with 3 and 4 times zooplankton biomass negatively affected the cyanobacteria Aphanocapsa sp., Chroococcus sp., Dolichospermum sp., Merismopedia tenuissima, Microcystis aeruginosa and Pseudanabaena sp.; the diatom Cyclotella meneghiniana; and the cryptophyte Cryptomonas sp. Total microcystin concentration both increased and decreased at different times depending on zooplankton treatment, while saxitoxin level was not significantly different between the treatments and control. The results of the present study suggest that zooplankton biomass can be manipulated to control the excessive proliferation of non-filamentous bloom forming cyanobacteria (e.g. M. aeruginosa) and their associated cyanotoxins.
Seasonal dynamics of microcystin-degrading bacteria and toxic cyanobacterial blooms: Interaction and influence of abiotic factors Harmful Algae (IF 3.087) Pub Date : 2017-12-06 María Ángeles Lezcano, Antonio Quesada, Rehab El-Shehawy
Massive proliferations of cyanobacteria coexist and have different interactions with other microorganisms, including microcystin (MC)-degrading bacteria. Despite their relevance in the environment for the removal of MCs, this bacterial community has been scarcely studied. The influence of physicochemical factors and the seasonal dynamics of toxic cyanobacteria on the relative abundance and seasonal dynamics of the MC-degrading bacterial community with mlr genes (mlr+) were investigated during a two-year study at a water reservoir in central Spain. The capacity of the total bacterial community on the degradation of MCs during the whole period of study was also evaluated. The results showed that the relative abundance of mlr+ bacteria started to increase after the increase in the relative abundance of toxic cyanobacteria and MC concentrations in the water, indicating a related seasonal dynamic and an important interaction between the two communities. The correspondence of several peaks of mlr+ bacteria with decreases in the relative abundance of toxic cyanobacteria and vice versa may also suggest a possible antagonistic relationship that deserves an in-depth study. The lack of a significant relationship between the physicochemical factors and the temporal shifts of both MC producers and degraders also supports the notion that the interaction of the two communities is an important driver of their seasonal dynamics in nature. Regarding the capacity of the total bacterial community for the degradation of MCs, this capacity was only observed during the toxic cyanobacterial bloom episodes, highlighting the importance of the pre-exposure to MCs in the reservoir for triggering the MC biodegradation process.
Application of solid phase adsorption toxin tracking (SPATT) devices for the field detection of Gambierdiscus toxins Harmful Algae (IF 3.087) Pub Date : 2017-12-08 Mélanie Roué, Hélène Taiana Darius, Jérôme Viallon, André Ung, Clémence Gatti, D. Tim Harwood, Mireille Chinain
Septic systems contribute to nutrient pollution and harmful algal blooms in the St. Lucie Estuary, Southeast Florida, USA Harmful Algae (IF 3.087) Pub Date : 2017-10-26 Brian E. Lapointe, Laura W. Herren, Armelle L. Paule
Nutrient enrichment is a significant global-scale driver of change in coastal waters, contributing to an array of problems in coastal ecosystems. The St. Lucie Estuary (SLE) in southeast Florida has received national attention as a result of its poor water quality (elevated nutrient concentrations and fecal bacteria counts), recurring toxic Microcystis aeruginosa blooms, and its proximity to the northern boundary of tropical coral species in the United States. The SLE has an artificially large watershed comprised of a network of drainage canals, one of which (C-44) is used to lower the water level in Lake Okeechobee. Public attention has primarily been directed at nutrient inputs originating from the lake, but recent concern over the importance of local watershed impacts prompted a one-year watershed study designed to investigate the interactions between on-site sewage treatment and disposal systems (OSTDS or septic systems), groundwaters, and surface waters in the SLE and nearshore reefs. Results provided multiple lines of evidence of OSTDS contamination of the SLE and its watershed: 1) dissolved nutrients in groundwaters and surface waters were most concentrated adjacent to two older (pre-1978) residential communities and the primary canals, and 2) sucralose was present in groundwater at residential sites (up to 32.0 μg/L) and adjacent surface waters (up to 5.5 μg/L), and 3) δ15N values in surface water (+7.5 o/oo), macroalgae (+4.4 o/oo) and phytoplankton (+5.0 o/oo) were within the published range (>+3 o/oo) for sewage N and similar to values in OSTDS-contaminated groundwaters. Measured δ15N values in M. aeruginosa became increasingly enriched during transport from the C-44 canal (∼5.8 o/oo) into the mid-estuary (∼8.0 o/oo), indicating uptake and growth on sewage N sources within the urbanized estuary. Consequently, there is a need to reduce N and P loading, as well as fecal loading, from the SLE watershed via septic-to-sewer conversion projects and to minimize the frequency and intensity of the releases from Lake Okeechobee to the SLE via additional water storage north of the lake. These enhancements would improve water quality in both the SLE and Lake Okeechobee, reduce the occurrence of toxic harmful algal blooms in the linked systems, and improve overall ecosystem health in the SLE and downstream reefs.
A multilevel trait-based approach to the ecological performance of Microcystis aeruginosa complex from headwaters to the ocean Harmful Algae (IF 3.087) Pub Date : 2017-11-01 Carla Kruk, Angel M. Segura, Lucía Nogueira, Ignacio Alcántara, Danilo Calliari, Gabriela Martínez de la Escalera, Carmela Carballo, Carolina Cabrera, Florencia Sarthou, Paola Scavone, Claudia Piccini
The Microcystis aeruginosa complex (MAC) clusters cosmopolitan and conspicuous harmful bloom-forming cyanobacteria able to produce cyanotoxins. It is hypothesized that low temperatures and brackish salinities are the main barriers to MAC proliferation. Here, patterns at multiple levels of organization irrespective of taxonomic identity (i.e. a trait-based approach) were analyzed. MAC responses from the intracellular (e.g. respiratory activity) to the ecosystem level (e.g. blooms) were evaluated in wide environmental gradients. Experimental results on buoyancy and respiratory activity in response to increased salinity (0–35) and a literature review of maximum growth rates under different temperatures and salinities were combined with field sampling from headwaters (800 km upstream) to the marine end of the Rio de la Plata estuary (Uruguay-South America). Salinity and temperature were the major variables affecting MAC responses. Experimentally, freshwater MAC cells remained active for 24 h in brackish waters (salinity = 15) while colonies increased their flotation velocity. At the population level, maximum growth rate decreased with salinity and presented a unimodal exponential response with temperature, showing an optimum at 27.5 °C and a rapid decrease thereafter. At the community and ecosystem levels, MAC occurred from fresh to marine waters (salinity 30) with a sustained relative increase of large mucilaginous colonies biovolume with respect to individual cells. Similarly, total biomass and, specific and morphological richness decreased with salinity while blooms were only detected in freshwater both at high (33 °C) and low (11 °C) temperatures. In brackish waters, large mucilaginous colonies presented advantages under osmotic restrictive conditions. These traits values have also been associated with higher toxicity potential. This suggest salinity or low temperatures would not represent effective barriers for the survival and transport of potentially toxic MAC under likely near future scenarios of increasing human impacts (i.e. eutrophication, dam construction and climate change).
Sandwich hybridization probes for the detection of Pseudo-nitzschia (Bacillariophyceae) species: An update to existing probes and a description of new probes Harmful Algae (IF 3.087) Pub Date : 2017-11-01 Holly A. Bowers, Roman Marin, James M. Birch, Christopher A. Scholin
New sandwich hybridization assay (SHA) probes for detecting Pseudo-nitzschia species (P. arenysensis, P. fraudulenta, P. hasleana, P. pungens) are presented, along with updated cross-reactivity information on historical probes (SHA and FISH; fluorescence in situ hybridization) targeting P. australis and P. multiseries. Pseudo-nitzschia species are a cosmopolitan group of diatoms that produce varying levels of domoic acid (DA), a neurotoxin that can accumulate in finfish and shellfish and transfer throughout the food web. Consumption of infected food sources can lead to illness in humans (amnesic shellfish poisoning; ASP) and marine wildlife (domoic acid poisoning; DAP). The threat of human illness, along with economic loss from fishery closures has resulted in the implementation of monitoring protocols and intensive ecological studies. SHA probes have been instrumental in some of these efforts, as the technique performs well in complex heterogeneous sample matrices and has been adapted to benchtop and deployable (Environmental Sample Processor) platforms. The expanded probe set will enhance future efforts towards understanding spatial, temporal and successional patterns in species during bloom and non-bloom periods.
Life-history stages of natural bloom populations and the bloom dynamics of a tropical Asian ribotype of Alexandrium minutum Harmful Algae (IF 3.087) Pub Date : 2017-11-09 Winnie Lik Sing Lau, Ing Kuo Law, Guat Ru Liow, Kieng Soon Hii, Gires Usup, Po Teen Lim, Chui Pin Leaw
In 2015, a remarkably high density bloom of Alexandrium minutum occurred in Sungai Geting, a semi-enclosed lagoon situated in the northeast of Peninsular Malaysia, causing severe discoloration and contaminated the benthic clams (Polymesoda). Plankton and water samples were collected to investigate the mechanisms of bloom development of this toxic species. Analysis of bloom samples using flow cytometry indicated that the bloom was initiated by the process of active excystment, as planomycetes (>4C cells) were observed in the early stage of the bloom. Increase in planozygotes (2C cells) was evident during the middle stage of the bloom, coinciding with an abrupt decrease in salinity and increase of temperature. The bloom was sustained through the combination of binary division of vegetative cells, division of planozygotes, and cyst germination through continuous excystment. Nutrient depletion followed by precipitation subsequently caused the bloom to terminate. This study provides the first continuous record of in situ life-cycle stages of a natural bloom population of A. minutum through a complete bloom cycle. The event has provided a fundamental understanding of the pelagic life-cycle stages of this tropical dinoflagellate, and demonstrated a unique bloom development characteristic shared among toxic Alexandrium species in coastal embayments.
Effects of modified clay on the physiological and photosynthetic activities of Amphidinium carterae Hulburt Harmful Algae (IF 3.087) Pub Date : 2017-11-09 Shuya Liu, Zhiming Yu, Xiuxian Song, Xihua Cao
Among the strategies for treating harmful algal blooms, flocculation using modified clay (MC) has been widely applied in the field. This paper studied the mitigation of MC on Amphidinium carterae Hulburt, finding that MC could not only effectively remove A. carterae, but also affect the physiological activities of the residual algae and inhibit their normal growth. The superoxide dismutase (SOD) activity, catalase (CAT) activity and malondialdehyde (MDA) content of the residual algae significantly increased compared with the control, indicating that MC stimulated the accumulation of reactive oxygen species (ROS) in algal cells. In addition, the cell density was significantly correlated with the SOD activity, CAT activity and MDA content in the experiment groups, suggesting that intracellular ROS might be the main internal factor inhibiting cell growth. To reveal the mechanism of ROS generation, this paper further evaluated the effect of MC on photosynthesis in the residual microalgae, and found that compared with the control the absorption flux per photosystem II (PSII) reaction center (ABS/RC), the trapping flux per RC (TR0/RC) and the electron transport flux per RC (ET0/RC) increased, while the TR0/ABS and ET0/ABS decreased after adding 0.10 g/L and 0.25 g/L MC. These findings indicate that the MC led to an imbalance between photosynthetic light absorption and energy utilization and that the partial RCs became non-primary quinone electron acceptor (QA)-RCs, further inducing the over-excitation of the active RCs. And MC caused the suppression of the electron transport chain (ETC): the ETC from the QA to the secondary quinone electron acceptor (QB) was blocked and the size of plastoquinone pool decreased, which could induce the over-reduction of PSII. The over-excitation of PSII and the damaged ETC likely induce the generation of ROS during photosynthesis. Thus, MC likely induced the accumulation of intracellular ROS due to photosynthesis inhibition, consequently hindering the growth of the residual algae.
Morphology and phylogeny of Prorocentrum caipirignum sp. nov. (Dinophyceae), a new tropical toxic benthic dinoflagellate Harmful Algae (IF 3.087) Pub Date : 2017-11-10 Silvia M. Nascimento, M. Cristina Q. Mendes, Mariângela Menezes, Francisco Rodríguez, Catharina Alves-de-Souza, Suema Branco, Pilar Riobó, José Franco, José Marcos C. Nunes, Mariusz Huk, Steven Morris, Santiago Fraga
A new species of toxic benthic dinoflagellate is described based on laboratory cultures isolated from two locations from Brazil, Rio de Janeiro and Bahia. The morphology was studied with SEM and LM. Cells are elliptical in right thecal view and flat. They are 37–44 μm long and 29–36 μm wide. The right thecal plate has a V shaped indentation where six platelets can be identified. The thecal surface of both thecal plates is smooth and has round or kidney shaped and uniformly distributed pores except in the central area of the cell, and a line of marginal pores. Some cells present an elongated depression on the central area of the apical part of the right thecal plate. Prorocentrum caipirignum is similar to Prorocentrum lima in its morphology, but can be differentiated by the general cell shape, being elliptical while P. lima is ovoid. In the phylogenetic trees based on ITS and LSU rDNA sequences, the P. caipirignum clade appears close to the clades of P. lima and Prorocentrum hoffmannianum. The Brazilian strains of P. caipirignum formed a clade with strains from Cuba, Hainan Island and Malaysia and it is therefore likely that this new species has a broad tropical distribution. Prorocentrum caipirignum is a toxic species that produces okadaic acid and the fast acting toxin prorocentrolide.
Differences in the photoacclimation and photoprotection exhibited by two species of the ciguatera causing dinoflagellate genus, Gambierdiscus Harmful Algae (IF 3.087) Pub Date : 2017-11-13 Alexander K. Leynse, Michael L. Parsons, Serge E. Thomas
In culture, Gambierdiscus spp. have been shown to prefer irradiances that are relatively low (≤250 μmol photons m−2 s−1) versus those to which they are frequently exposed to in their natural environment (>500 μmol photons m−2 s−1). Although several behavioral strategies for coping with such irradiances have been suggested, it is unclear as to how these dinoflagellates do so on a physiological level. More specifically, how do long term exposures (30 days) affect cell size and cellular chlorophyll content, and what is the photosynthetic response to short term, high irradiance exposures (up to 1464 μmol photons m−2 s−1)? The results of this study reveal that cell size and chlorophyll content exhibited by G. carolinianus increased with acclimation to increasing photon flux density. Additionally, both G. carolinianus and G. silvae exhibited reduced photosynthetic efficiency when acclimated to increased photon flux density. Photosynthetic yield exhibited by G. silvae was greater than that for G. carolinianus across all acclimation irradiances. Although such differences were evident, both G. carolinianus and G. silvae appear to have adequate biochemical mechanisms to withstand exposure to irradiances exceeding 250 μmol photons m−2 s−1 for at least short periods of time following acclimation to irradiances of up to 150 μmol photons m−2 s−1.
Environmental control of harmful dinoflagellates and diatoms in a fjordic system Harmful Algae (IF 3.087) Pub Date : 2017-09-23 Ruth F. Paterson, Sharon McNeill, Elaine Mitchell, Thomas Adams, Sarah C. Swan, Dave Clarke, Peter I. Miller, Eileen Bresnan, Keith Davidson
Fjordic coastlines provide an ideal protected environment for both finfish and shellfish aquaculture operations. This study reports the results of a cruise to the Scottish Clyde Sea, and associated fjordic sea lochs, that coincided with blooms of the diarrhetic shellfish toxin producing dinoflagellate Dinophysis acuta and the diatom genus Chaetoceros, that can generate finfish mortalities. Unusually, D. acuta reached one order of magnitude higher cell abundance in the water column (2840 cells L−1) than the more common Dinophysis acuminata (200 cells L−1) and was linked with elevated shellfish toxicity (maximum 601 ± 237 μg OA eq/kg shellfish flesh) which caused shellfish harvesting closures in the region. Significant correlations between D. acuta abundance and that of Mesodinium rubrum were also observed across the cruise transect potentially supporting bloom formation of the mixotrophic D. acuta. Significant spatial variability in phytoplankton that was related to physical characteristics of the water column was observed, with a temperature-driven frontal region at the mouth of Loch Fyne being important in the development of the D. acuta, but not the Chaetoceros bloom. The front also provided important protection to the aquaculture located within the loch, with neither of the blooms encroaching within it. Analysis based on a particle-tracking model confirms the importance of the front to cell transport and shows significant inter-annual differences in advection within the region, that are important to the harmful algal bloom risk therein.
Early warning of limit-exceeding concentrations of cyanobacteria and cyanotoxins in drinking water reservoirs by inferential modelling Harmful Algae (IF 3.087) Pub Date : 2017-10-10 Friedrich Recknagel, Philip T. Orr, Michael Bartkow, Annelie Swanepoel, Hongqing Cao
Geosmin production and polyphasic characterization of Oscillatoria limosa Agardh ex Gomont isolated from the open canal of a large drinking water system in Tianjin City, China Harmful Algae (IF 3.087) Pub Date : 2017-10-12 Fangfang Cai, Gongliang Yu, Kai Zhang, Youxin Chen, Qiang Li, Yiming Yang, Jinlin Xie, Yilang Wang, Renhui Li
Taste and odor (T & O) episodes always cause strong effects on drinking water supply system. Luanhe River diversion into Tianjin City in China is an important drinking water resource. Massive growth of a benthic filamentous cyanobacterium with geosmin production in the open canal caused a strong earthy odor episode in Tianjin. On the basis of the morphological and molecular identification of this cyanobacterium as Oscillatoria limosa Agardh ex Gomont, the genetic basis for geosmin biosynthesis and factors influencing growth and geosmin production of O. limosa CHAB 7000 were studied in this work. A 2268-bp open reading frame, encoding 755 amino acids, was amplified and characterized as the geosmin synthase gene (geo), followed by a cyclic nucleotide-binding protein gene (cnb). Phylogenetic analysis implied that the evolution of the geosmin genes in O. limosa CHAB 7000 might involve a horizontal gene transfer event. Examination on the growth and geosmin production of O. limosa CHAB 7000 at different light intensities showed that the maximum geosmin production was observed at 10 μmol photons m−2 s−1, while the optimum growth was at 60 μmol photons m−2 s−1. Under three temperature conditions (15 °C, 25 °C, and 35 °C), the maximum growth and geosmin production were observed at 25 °C. Most amounts of geosmin were retained in cells during the growth phase, but high temperature and low light intensity increased the release of geosmin into the medium, implying that O. limosa CHAB 7000 had a high potential harm for the release of geosmin from its cells at these adverse conditions.
Variation within and between cyanobacterial species and strains affects competition: Implications for phytoplankton modelling Harmful Algae (IF 3.087) Pub Date : 2017-10-13 Man Xiao, Matthew P. Adams, Anusuya Willis, Michele A. Burford, Katherine R. O’Brien
Cyanobacteria Microcystis aeruginosa and Cylindrospermopsis raciborskii are two harmful species which co-occur and successively dominate in freshwaters globally. Within-species strain variability affects cyanobacterial population responses to environmental conditions, and it is unclear which species/strain would dominate under different environmental conditions. This study applied a Monte Carlo approach to a phytoplankton dynamic growth model to identify how growth variability of multiple strains of these two species affects their competition. Pairwise competition between four M. aeruginosa and eight C. raciborskii strains was simulated using a deterministic model, parameterized with laboratory measurements of growth and light attenuation for all strains, and run at two temperatures and light intensities. 17 000 runs were simulated for each pair using a statistical distribution with Monte Carlo approach. The model results showed that cyanobacterial competition was highly variable, depending on strains present, light and temperature conditions. There was no absolute ‘winner’ under all conditions as there were always strains predicted to coexist with the dominant strains, which were M. aeruginosa strains at 20 °C and C. raciborskii strains at 28 °C. The uncertainty in prediction of species competition outcomes was due to the substantial variability of growth responses within and between strains. Overall, this study demonstrates that within-species strain variability has a potentially large effect on cyanobacterial population dynamics, and therefore this variability may substantially reduce confidence in predicting outcomes of phytoplankton competition in deterministic models, that are based on only one set of parameters for each species or strain.
Mitigation of harmful algal blooms using modified clays: Theory, mechanisms, and applications Harmful Algae (IF 3.087) Pub Date : 2017-10-14 Zhiming Yu, Xiuxian Song, Xihua Cao, Yang Liu
Clay dispersal is one of only a few mitigation methods for harmful algal blooms (HABs) ever applied in the field; however, low flocculation efficiency has always been the most significant drawback associated with natural unmodified clays. This review discusses key factors affecting the flocculation efficiency, based on results obtained in studies of the mechanisms underlying interactions between clay particles and HAB organisms. It further elaborates clay surface modification theory and methods for improving removal efficiency of HAB cells, followed by descriptions of various modified clays successfully prepared with removal efficiencies of HAB cells that are up to hundreds of times greater than natural clays and have lower dosing requirements of 4–10 t/km2. Presently, modified clays are the most widely used method for the mitigation of HAB in the field in China. This review also evaluates potential ecological effects of modified clay disposal on water quality, typical aquatic organisms, benthic environments, and ecosystems. Both laboratory and field results have demonstrated that modified clays markedly can actually improve water quality after treatment and pose no negative effects on aquatic ecosystems.
The influence of salinity in the domoic acid effect on estuarine phytoplankton communities Harmful Algae (IF 3.087) Pub Date : 2017-10-21 Elise Van Meerssche, James L. Pinckney
Toxic species of the diatom genus Pseudo-nitzschia, observed worldwide from coastal waters to the open ocean, produce the neurotoxin domoic acid (DA). DA is an important environmental and economic hazard due to shellfish contamination with subsequent effects on higher trophic levels. Previous research has demonstrated that, among other environmental factors, salinity influences the abundance and toxicity of Pseudo-nitzschia. In this study, the environmental factors driving the growth of Pseudo-nitzschia and the production of dissolved DA (dDA) in North Inlet estuary were examined. The effect of salinity on the growth inhibition of phytoplankton induced by the initial presence as well as by an addition of dDA was also assessed. Initially, the diatom abundance was negatively correlated with the abundance of Pseudo-nitzschia and with the concentration of dDA. With the addition of a concentrated solution of dDA, the percent inhibition of cryptophytes and diatoms was significantly correlated with salinity and suggested a higher sensitivity to dDA at extreme salinities. These results emphasize the importance of salinity in assessing the properties of DA and potentially of other phycotoxins on phytoplankton.
Bloom dynamics and chemical defenses of benthic cyanobacteria in the Indian River Lagoon, Florida Harmful Algae (IF 3.087) Pub Date : 2017-10-23 Jennifer M. Sneed, Theresa Meickle, Niclas Engene, Sherry Reed, Sarath Gunasekera, Valerie J. Paul
Cyanobacterial blooms are predicted to become more prominent in the future as a result of increasing seawater temperatures and the continued addition of nutrients to coastal waters. Many benthic marine cyanobacteria have potent chemical defenses that protect them from top down pressures and contribute to the persistence of blooms. Blooms of benthic cyanobacteria have been observed along the coast of Florida and within the Indian River Lagoon (IRL), a biodiverse estuary system that spans 250 km along Florida’s east coast. In this study, the cyanobacterial bloom progression at three sites within the central IRL was monitored over the course of two summers. The blooms consisted of four unique cyanobacterial species, including the recently described Okeania erythroflocculosa. The cyanobacteria produced a range of known bioactive compounds including malyngolide, lyngbyoic acid, microcolins A–B, and desacetylmicrocolin B. Ecologically-relevant assays showed that malyngolide inhibited the growth of marine fungi (Dendryphiella salina and Lindra thalassiae); microcolins A–B and desacetylmicrocolin B inhibited feeding by a generalist herbivore, the sea urchin Lytechinus variegatus; and lyngbyoic acid inhibited fungal growth and herbivore feeding. These chemical defenses likely contribute to the persistence of cyanobacterial blooms in the IRL during the summer growing period.
Insights into the harmful algal flora in northwestern Mediterranean coastal lagoons revealed by pyrosequencing metabarcodes of the 28S rRNA gene Harmful Algae (IF 3.087) Pub Date : 2017-07-24 Daniel Grzebyk, Stéphane Audic, Bernard Lasserre, Eric Abadie, Colomban de Vargas, Béatrice Bec
This study investigated the genetic diversity of phytoplankton communities in six shallow lagoons located on the French coast of the northwestern Mediterranean Sea that represented a trophic gradient ranging from oligotrophic to hypereutrophic. The phytoplankton communities were sampled once a month from spring (May) to the beginning of autumn (September/early October) in 2012 and fractionated by size. Metabarcodes were generated from cDNAs by targeting the D1-D2 region of the 28S rRNA gene and pyrosequenced using Roche 454 technology. Examination of the annotated barcodes revealed harmful algal species not previously documented in these lagoons. Three ichthyotoxic species belonging to Pfiesteriaceae were detected: Luciella masanensis was relatively widespread and abundant in many samples, whereas Pfiesteria piscicida and Stoeckeria changwonensis were found as single barcode sequences. Furthermore, a phylogenetic analysis of barcodes annotated as belonging to Pfiesteriaceae suggested the existence of two previously undescribed clades. The other toxic or potentially harmful dinoflagellates detected through rare barcodes were Dinophysis acuminata, Vulcanodinium rugosum, Alexandrium andersonii and A. ostenfeldii. The two most abundant dinoflagellate taxa were Gymnodinium litoralis and Akashiwo sanguinea with respect to sequence numbers. Four diatom species from the genus Pseudo-nitzschia that potentially produce domoic acid were identified (P. galaxiae, P. delicatissima, P. brasiliana and P. calliantha). These observations are discussed in terms of the literature and monitoring records related to the identified taxa in this Mediterranean area.
Identification of unique microbiomes associated with harmful algal blooms caused by Alexandrium fundyense and Dinophysis acuminata Harmful Algae (IF 3.087) Pub Date : 2017-07-24 Theresa K. Hattenrath-Lehmann, Christopher J. Gobler
Biotic interactions dominate plankton communities, yet the microbial consortia associated with harmful algal blooms (HABs) have not been well-described. Here, high-throughput amplicon sequencing of ribosomal genes was used to quantify the dynamics of bacterial (16S) and phytoplankton assemblages (18S) associated with blooms and cultures of two harmful algae, Alexandrium fundyense and Dinophysis acuminata. Experiments were performed to assess changes in natural bacterial and phytoplankton communities in response to the filtrate from cultures of these two harmful algae. Analysis of prokaryotic sequences from ecosystems, experiments, and cultures revealed statistically unique bacterial associations with each HAB. The dinoflagellate, Alexandrium, was strongly associated with multiple genera of Flavobacteria including Owenweeksia spp., Maribacter spp., and individuals within the NS5 marine group. While Flavobacteria also dominated Dinophysis-associated communities, the relative abundance of Alteromonadales bacteria strongly co-varied with Dinophysis abundances during blooms and Ulvibacter spp. (Flavobacteriales) and Arenicella spp. (Gammaproteobacteria) were associated with cells in culture. Eukaryotic sequencing facilitated the discovery of the endosymbiotic, parasitic dinoflagellate, Amoebophrya spp., that had not been regionally described but represented up to 17% of sequences during Alexandrium blooms. The presence of Alexandrium in field samples and in experiments significantly altered the relative abundances of bacterial and phytoplankton by both suppressing and promoting different taxa, while this effect was weaker in Dinophysis. Experiments specifically revealed a negative feedback loop during blooms whereby Alexandrium filtrate promoted the abundance of the parasite, Amoebophrya spp. Collectively, this study demonstrates that HABs formed by Alexandrium and Dinophysis harbor unique prokaryotic and eukaryotic microbiomes that are likely to, in turn, influence the dynamics of these HABs.
Which species, Alexandrium catenella (Group I) or A. pacificum (Group IV), is really responsible for past paralytic shellfish poisoning outbreaks in Jinhae-Masan Bay, Korea? Harmful Algae (IF 3.087) Pub Date : 2017-07-26 Hyeon Ho Shin, Zhun Li, Eun Song Kim, Jong-Woo Park, Weol Ae Lim
Paralytic shellfish poisoning (PSP) caused the deaths of four people in coastal area of Korea, mainly Jinhae-Masan Bay and adjacent areas, in April 1986 and in 1996. The PSP outbreaks were caused by the consumption of mussels, Mytilus edulis. The organism that caused PSP was identified, from morphological data only, as Alexandrium tamarense which is recently renamed as A. catenella, however recent studies have shown that the morphological diagnostic characteristics used to identify Alexandrium species have uncertainties and molecular tools and other criteria should be considered as well. The organism that caused past PSP outbreaks and incidents in Korea therefore need to be carefully reconsidered. The aim of this study was to re-evaluate the species really responsible for past outbreaks of PSP in Jinhae-Masan Bay, Korea. The temporal production and fluxes of the resting cysts of Alexandrium species were investigated for one year (from March 2011 to February 2012) using a sediment trap, and the morphology and phylogeny of vegetative cells germinated from the resting cysts were analysed. The production of Alexandrium species peaked in August and November, when temporal discrepancies were found in the water temperature (22.4 and 22.7 °C in August, 19.1 and 19.6 °C in November) and salinity (29.5 and 26.1 psu in August, 30.5 and 31.8 psu in November). The morphological data revealed that Alexandrium species germinated from resting cysts collected in August have a ventral pore on the 1′ plate, whereas the 1′ plate in Alexandrium species germinated from resting cysts collected in November lacks a ventral pore. Molecular phylogenetic data for the vegetative cells from the germination experiments allowed the August and November peaks to be assigned to Alexandrium catenella (Group I) and A. pacificum (Group IV), respectively. This indicates that the production of resting cysts of A. catenella can be enhanced by relatively high water temperature. This result is not consistent with those of previous studies that A. catenella responsible for PSP outbreaks was found at relatively low water temperature. In addition, large subunit ribosomal sequences data revealed that A. pacificum isolates from Korea were closely related to those from Australia, Japan and New Zealand where the PSP toxicity of shellfish and blooms occurred in the 1990s, indicating that the introduction of toxic dinoflagellates were related to ballast water from bulk-cargo shipping. Based on these results, we concluded that past PSP outbreaks in Jinhae-Masan Bay of Korea could have been caused by A. pacificum rather than by A. catenella.
Applicability of massively parallel sequencing on monitoring harmful algae at Varna Bay in the Black Sea Harmful Algae (IF 3.087) Pub Date : 2017-07-28 Nina Dzhembekova, Shingo Urusizaki, Snejana Moncheva, Petya Ivanova, Satoshi Nagai
In this study the plankton diversity in 13 environmental samples from Varna Bay (in the western Black Sea) was analyzed using massively parallel sequencing (MPS). This preliminary study was undertaken to assess the potential of this technology for future implementation in monitoring programs in the Black Sea. Amplicon sequences of the 18S rRNA gene (V4-5 regions) were obtained using the Illumina MiSeq 250PE platform. A total of 1137 operational taxonomic units (OTUs) were obtained among which 242 OTUs with >0.990 BLAST top hit similarity (21.3% of all detected OTUs) closely related to sequences belonging to −protists. A large portion (175 OTUs = 72.3%) was identified at the species levels, including species typical for the Bulgarian Black Sea plankton community, as well as many that haven’t been reported earlier in the Bulgarian Black Sea coast (124 OTUs = 51.2%). Dinoflagellates were represented by the highest species number (77 OTUs comprising 31.8% of protist species), with dominant genera Gyrodinium and Heterocapsa. The present survey revealed the presence of 12 species listed as harmful, some of which have been previously overlooked, such as Cochlodinium polykrikoides, Karenia bicuneiformis, and Karlodinium veneficum. Species identification was possible for 10.3–36.0% of the detected OTUs in the six major supergroups. The frequency in Rhizaria was significantly lower than that in other major groups (p < 0.05–0.01), implying difficulties in the classification from morphology-based observations. The metagenetic data had an insufficient resolution of the 18S rRNA gene for species identification in many genera. These issues may hamper the implementation of MPS-based surveys for plankton monitoring, especially for detecting harmful algal blooms (HAB). The sequencing technology is steadily improving and it is expected that sequence length and quality issues will be resolved in the near future. The ongoing efforts to register taxonomic information and quality controls in the international nucleotide sequence databases (INSDs) will be essential for improving taxonomic identification power.
Assessing the use of artificial substrates to monitor Gambierdiscus populations in the Florida Keys Harmful Algae (IF 3.087) Pub Date : 2017-07-29 Michael L. Parsons, Ashley L. Brandt, Amanda Ellsworth, Alex K. Leynse, Lacey K. Rains, Donald M. Anderson
Four distinct coastal locations were sampled on a monthly basis near Long Key (Florida Keys, USA) over a 13-month period to study Gambierdiscus population dynamics on different substrates, including four macrophyte species (Dictyota spp., Halimeda spp., Laurencia spp., and Thalassia testudinum) and three artificial substrates (polyvinyl chloride (PVC) tiles, burlap, and fiberglass window screen). Cell densities of Gambierdiscus were generally lower on Dictyota versus Halimeda and Laurencia. Cell densities of Gambierdiscus were significantly correlated among macrophyte hosts in 54% of the comparisons, and between macrophyte hosts and artificial substrates in 72% of the comparisons. Predictive slopes determined from regression analyses between cell densities on artificial substrates and macrophyte hosts indicated that, on an areal basis, fewer cells were present on macrophytes versus artificial substrates (cells cm−2) and that slope variation (error) among the different macrophytes and sites ranged from 5% to 200%, averaging 61% overall. As the data required log-transformation prior to analyses, this level of error translates into two-orders of magnitude in range of estimation of the overall average abundance of Gambierdiscus cells on macrophytes (135 cells g−1 wet weight); 20–2690 cells g−1 ww. The lack of consistent correlation among Gambierdiscus cell densities on macrophytes versus artificial substrates, coupled with the high level of error associated with the predictive slope estimations, indicates that extreme caution should be taken when interpreting the data garnered from artificial substrate deployments, and that such deployments should be thoroughly vetted prior to routine use for monitoring purposes.
The life history of the toxic marine dinoflagellate Protoceratium reticulatum (Gonyaulacales) in culture Harmful Algae (IF 3.087) Pub Date : 2017-08-01 Pablo Salgado, Rosa I. Figueroa, Isabel Ramilo, Isabel Bravo
Asexual and sexual life cycle events were studied in cultures of the toxic marine dinoflagellate Protoceratium reticulatum. Asexual division by desmoschisis was characterized morphologically and changes in DNA content were analyzed by flow cytometry. The results indicated that haploid cells with a C DNA content occurred only during the light period whereas a shift from a C to a 2C DNA content (indicative of S phase) took place only during darkness. The sexual life cycle was documented by examining the mating type as well as the morphology of the sexual stages and nuclei. Gamete fusion resulted in a planozygote with two longitudinal flagella, but longitudinally biflagellated cells arising from planozygote division were also observed, so one of the daughter cells retained two longitudinal flagella while the other daughter cell lacked them. Presumed planozygotes (identified by their longitudinally biflagellated form) followed two life-cycle routes: division and encystment (resting cyst formation). Both the division of longitudinally biflagellated cells and resting cyst formation are morphologically described herein. Resting cyst formation through sexual reproduction was observed in 6.1% of crosses and followed a complex heterothallic pattern. Clonal strains underwent sexuality (homothallism for planozygote formation and division) but without the production of resting cysts. Ornamental processes of resting cysts formed from the cyst wall under an outer balloon-shaped membrane and were fully developed in <1 h. Obligatory dormancy period was of ∼4 months. Excystment resulted in a large, rounded, pigmented, longitudinally biflagellated but motionless, thecate germling that divided by desmoschisis. Like the planozygote, the first division of the germling yielded one longitudinally biflagellated daughter cell and another without longitudinal flagella. The longitudinal biflagellation state of both sexual stages and of the first division products of these cells is discussed.
Spatial and temporal variability in macroalgal blooms in a eutrophied coastal estuary Harmful Algae (IF 3.087) Pub Date : 2017-09-26 Carol S. Thornber, Michele Guidone, Christopher Deacutis, Lindsay Green, Christine N. Ramsay, Melissa Palmisciano
All three macroalgal clades (Chlorophyta, Rhodophyta, and Phaeophyceae) contain bloom-forming species. Macroalgal blooms occur worldwide and have negative consequences for coastal habitats and economies. Narragansett Bay (NB), Rhode Island, USA, is a medium sized estuary that is heavily influenced by anthropogenic activities and has been plagued by macroalgal blooms for over a century. Over the past decade, significant investment has upgraded wastewater treatment from secondary treatment to water-quality based limits (i.e. tertiary treatment) in an effort to control coastal eutrophication in this system. The goal of this study was to improve the understanding of multi-year macroalgal bloom dynamics through intensive aerial and ground surveys conducted monthly to bi-monthly during low tides in May–October 2006–2013 in NB. Aerial surveys provided a rapid characterization of macroalgal densities across a large area, while ground surveys provided high resolution measurements of macroalgal identity, percent cover, and biomass. Macroalgal blooms in NB are dominated by Ulva and Gracilaria spp. regardless of year or month, although all three clades of macroalgae were documented. Chlorophyta cover and nutrient concentrations were highest in the middle and upper bay. Rhodophyta cover was highest in the middle and lower bay, while drifting Phaeophyceae cover was patchy. Macroalgal blooms of >1000 g fresh mass (gfm)/m2 (max = 3510 gfm/m2) in the intertidal zone and >3000 gfm/m3 (max = 8555 gfm/m3) in the subtidal zone were observed within a heavily impacted embayment (Greenwich Bay). Macroalgal percent cover (intertidal), biomass (subtidal), and diversity varied significantly between year, month-group, site, and even within sites, with the highest species diversity at sites outside of Greenwich Bay. Total intertidal macroalgal percent cover, as well as subtidal Ulva biomass, were positively correlated with temperature. Dissolved inorganic nitrogen concentrations were correlated with the total biomass of macroalgae and the subtidal biomass of Gracilaria spp. but not the biomass of Ulva spp. Despite seasonal reductions in the nutrient output of wastewater treatment facilities emptying into upper Narragansett Bay in recent years, macroalgal blooms still persist. Continued long-term monitoring of water quality, macroalgal blooms, and ecological indicators is essential to understand the changes in macroalgal bloom dynamics that occur after nutrient reductions from management efforts.
Management of harmful benthic dinoflagellates requires targeted sampling methods and alarm thresholds Harmful Algae (IF 3.087) Pub Date : 2017-08-11 Valentina Giussani, Valentina Asnaghi, Andrea Pedroncini, Mariachiara Chiantore
Concern regarding Benthic Harmful Algal Blooms (BHABs) is increasing since some harmful benthic species have been identified in new areas. In the Mediterranean basin, the most common harmful benthic microalgae are Ostreopsis cf. ovata and Prorocentrum lima, which produce palytoxin-like compounds and okadaic acid respectively, and the need to implement monitoring activities has increased. However, a general agreement on appropriate strategies (e.g. sampling season, definition of alarm thresholds, etc.) is still lagging behind, especially for P. lima, whose proliferation dynamics are still poorly known.
Mixotrophy in the marine red-tide cryptophyte Teleaulax amphioxeia and ingestion and grazing impact of cryptophytes on natural populations of bacteria in Korean coastal waters Harmful Algae (IF 3.087) Pub Date : 2017-08-11 Yeong Du Yoo, Kyeong Ah Seong, Hae Jin Jeong, Wonho Yih, Jung-Rae Rho, Seung Won Nam, Hyung Seop Kim
Cryptophytes are ubiquitous and one of the major phototrophic components in marine plankton communities. They often cause red tides in the waters of many countries. Understanding the bloom dynamics of cryptophytes is, therefore, of great importance. A critical step in this understanding is unveiling their trophic modes. Prior to this study, several freshwater cryptophyte species and marine Cryptomonas sp. and Geminifera cryophila were revealed to be mixotrophic. The trophic mode of the common marine cryptophyte species, Teleaulax amphioxeia has not been investigated yet. Thus, to explore the mixotrophic ability of T. amphioxeia by assessing the types of prey species that this species is able to feed on, the protoplasms of T. amphioxeia cells were carefully examined under an epifluorescence microscope and a transmission electron microscope after adding each of the diverse prey species. Furthermore, T. amphioxeia ingestion rates heterotrophic bacteria and the cyanobacterium Synechococcus sp. were measured as a function of prey concentration. Moreover, the feeding of natural populations of cryptophytes on natural populations of heterotrophic bacteria was assessed in Masan Bay in April 2006. This study reported for the first time, to our knowledge, that T. amphioxeia is a mixotrophic species. Among the prey organisms offered, T. amphioxeia fed only on heterotrophic bacteria and Synechococcus sp. The ingestion rates of T. amphioxeia on heterotrophic bacteria or Synechococcus sp. rapidly increased with increasing prey concentrations up to 8.6 × 106 cells ml−1, but slowly at higher prey concentrations. The maximum ingestion rates of T. amphioxeia on heterotrophic bacteria and Synechococcus sp. reached 0.7 and 0.3 cells predator−1 h−1, respectively. During the field experiments, the ingestion rates and grazing coefficients of cryptophytes on natural populations of heterotrophic bacteria were 0.3–8.3 cells predator−1 h−1 and 0.012–0.033 d−1, respectively. Marine cryptophytes, including T. amphioxeia, are known to be favorite prey species for many mixotrophic and heterotrophic dinoflagellates and ciliates. Cryptophytes, therefore, likely play important roles in marine food webs and may exert a considerable potential grazing impact on the populations of marine bacteria.
The dinoflagellate Akashiwo sanguinea will benefit from future climate change: The interactive effects of ocean acidification, warming and high irradiance on photophysiology and hemolytic activity Harmful Algae (IF 3.087) Pub Date : 2017-08-11 Guanyong Ou, Hong Wang, Ranran Si, Wanchun Guan
Due to global climate change, marine phytoplankton will likely experience low pH (ocean acidification), high temperatures and high irradiance in the future. Here, this work report the results of a batch culture experiment conducted to study the interactive effects of elevated CO2, increased temperature and high irradiance on the harmful dinoflagellate Akashiwo sanguinea, isolated at Dongtou Island, Eastern China Sea. The A. sanguinea cells were acclimated in high CO2 condition for about three months before testing the responses of cells to a full factorial matrix experimentation during a 7-day period. This study measured the variation in physiological parameters and hemolytic activity in 8 treatments, representing full factorial combinations of 2 levels each of exposure to CO2 (400 and 1000 μatm), temperature (20 and 28 °C) and irradiance (50 and 200 μmol photons m−2 s−1). Sustained growth of A. sanguinea occurred in all treatments, but high CO2 (HC) stimulated faster growth than low CO2 (LC). The pigments (chlorophyll a and carotenoid) decreased in all HC treatments. The quantum yield (Fv/Fm) declined slightly in all high-temperature (HT) treatments. High irradiance (HL) induced the accumulation of ultraviolet-absorbing compounds (UVabc) irrespective of temperature and CO2. The hemolytic activity in the LC treatments, however, declined when exposed to HT and HL, but HC alleviated the adverse effects of HT and HL on hemolytic activity. All HC and HL conditions and the combinations of high temperature*high light (HTHL) and high CO2*high temperature*high light (HCHTHL) positively affected the growth in comparison to the low CO2*low temperature*low light (LCLTLL) treatment. High temperature (HT), high light (HL) and a combination of HT*HL, however, negatively impacted hemolytic activity. CO2 was the main factor that affected the growth and hemolytic activity. There were no significant interactive effects of CO2*temperature*irradiance on growth, pigment, Fv/Fm or hemolytic activity, but there were effects on Pm, α, and Ek. If these results are extrapolated to the natural environment, it can be hypothesized that A. sanguinea cells will benefit from the combination of ocean acidification, warming, and high irradiance that are likely to occur under future climate change. It is assumed that faster growth and higher hemolytic activity and UVabc of this species will occur under future conditions compared with those the current CO2 (400 μatm) and temperature (20 °C) conditions.
An evaluation of the genus Amphidinium (Dinophyceae) combining evidence from morphology, phylogenetics, and toxin production, with the introduction of six novel species Harmful Algae (IF 3.087) Pub Date : 2017-08-29 Sarah Karafas, Sing Tung Teng, Chui Pin Leaw, Catharina Alves-de-Souza
The genus Amphidinium is an important group of athecated dinoflagellates because of its high abundance in marine habitats, its member’s ability to live in a variety of environmental conditions and ability to produce toxins. Furthermore, the genus is of particular interest in the biotechnology field for its potential in the pharmaceutical arena. Taxonomically the there is a history of complication and confusion over the proper identities and placements of Amphidinium species due to high genetic variability coupled with high morphological conservation. Thirteen years has passed since the most recent review of the group, and while many issues were resolved, some remain. The present study used microscopy, phylogenetics of the 28S region of rDNA, secondary structure of the ITS2 region of rDNA, compensatory base change data, and cytotoxicity data from Amphidinium strains collected world-wide to elucidate remaining confusion. This holistic approach using multiple lines of evidence resulted in a more comprehensive understanding of the morphological, ecological, and genetic characteristics that are attributed to organisms belonging to Amphidinium, including six novel species: A. fijiensis, A. magnum, A. paucianulatum, A. pseudomassartii, A. theodori, and A. tomasii.
Identification of Azadinium species and a new azaspiracid from Azadinium poporum in Puget Sound, Washington State, USA Harmful Algae (IF 3.087) Pub Date : 2017-09-18 Joo-Hwan Kim, Urban Tillmann, Nicolaus G. Adams, Bernd Krock, Whitney L. Stutts, Jonathan R. Deeds, Myung-Soo Han, Vera L. Trainer
The identification of a new suite of toxins, called azaspiracids (AZA), as the cause of human illnesses after the consumption of shellfish from the Irish west coast in 1995, resulted in interest in understanding the global distribution of these toxins and of species of the small dinoflagellate genus Azadinium, known to produce them. Clonal isolates of four species of Azadinium, A. poporum, A. cuneatum, A. obesum and A. dalianense were obtained from incubated sediment samples collected from Puget Sound, Washington State in 2016. These Azadinium species were identified using morphological characteristics confirmed by molecular phylogeny. Whereas AZA could not be detected in any strains of A. obesum, A. cuneatum and A. dalianense, all four strains of A. poporum produced a new azaspiracid toxin, based on LC–MS analysis, named AZA-59. The presence of AZA-59 was confirmed at low levels in situ using a solid phase resin deployed at several stations along the coastlines of Puget Sound. Using a combination of molecular methods for species detection and solid phase resin deployment to target shellfish monitoring of toxin at high-risk sites, the risk of azaspiracid shellfish poisoning can be minimized.
Response of bacterial communities to cyanobacterial harmful algal blooms in Lake Taihu, China Harmful Algae (IF 3.087) Pub Date : 2017-08-29 Xiaomei Su, Alan D. Steinman, Xiangming Tang, Qingju Xue, Yanyan Zhao, Liqiang Xie
Cyanobacterial harmful algal blooms are prevalent around the world, influencing aquatic organisms and altering the physico-chemical properties in freshwater systems. However, the response of bacterial communities to toxic cyanobacterial blooms and associated microcystins (MC) remain poorly understood even though global concentrations of MC have increased dramatically in the past few decades. To address this issue, the dynamics of bacterial community composition (BCC) in the water column and how BCC is influenced by both harmful cyanobacterial blooms and environmental factors were investigated on a monthly basis from August 2013 to July 2014 in Lake Taihu, China. Non-metric multidimensional scaling (NMDS) revealed that seasonal variation in BCC was significant, and that the succession of BCC greatly depends on changes in environmental conditions. Redundancy analysis (RDA) results showed that the overall variation of BCC was explained mainly by dissolved oxygen (DO), nitrate nitrogen (NO3−-N), and Microcystis. The alpha biodiversity of the bacterial community was different among months with the highest diversity in February and the lowest diversity in October. Furthermore, significant negative relationships were found between alpha biodiversity indices and Microcystis abundance as well as with intracellular MC concentrations, indicating that Microcystis and associated MC may influence the bacterial community structure by reducing its biodiversity. This study shows that potential associations exist between toxic cyanobacterial blooms and bacterial communities but more investigations are needed to obtain a mechanistic understanding of their complex relationships.
Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists Harmful Algae (IF 3.087) Pub Date : 2017-08-29 Jin Hee Ok, Hae Jin Jeong, An Suk Lim, Kyung Ha Lee
The phototrophic dinoflagellate Takayama helix that is known to be harmful to abalone larvae has recently been revealed to be mixotrophic. Although mixotrophy elevates the growth rate of T. helix by 79%–185%, its absolute growth rate is still as low as 0.3 d−1. Thus, if the mortality rate of T. helix due to predation is high, this dinoflagellate may not easily prevail. To investigate potential effective protistan grazers on T. helix, feeding by diverse heterotrophic dinoflagellates such as engulfment-feeding Oxyrrhis marina, Gyrodinium dominans, Gyrodinium moestrupii, Polykrikos kofoidii, and Noctiluca scintillans, peduncle-feeding Aduncodinium glandula, Gyrodiniellum shiwhaense, Luciella masanensis, and Pfiesteria piscicida, pallium-feeding Oblea rotunda and Protoperidinium pellucidum, and the naked ciliates Pelagostrobilidium sp. (ca. 40 μm in cell length) and Strombidinopsis sp. (ca. 150 μm in cell length) on T. helix was explored. Among the tested heterotrophic protists, O. marina, G. dominans, G. moestrupii, A. glandula, L. masanensis, P. kofoidii, P. piscicida, and Strombidinopsis sp. were able to feed on T. helix. The growth rates of all these predators except Strombidinopsis sp. with T. helix prey were lower than those without the prey. The growth rate of Strombidinopsis sp. on T. helix was almost zero although the growth rate of Strombidinopsis sp. with T. helix prey was higher than those without the prey. Moreover, T. helix fed on O. marina and P. pellucidum and lysed the cells of P. kofoidii and G. shiwhaense. With increasing the concentrations of T. helix, the growth rates of O. marina and P. kofoidii decreased, but those of G. dominans and L. masanensis largely did not change. Therefore, reciprocal predation, lysis, no feeding, and the low ingestion rates of the common protists preying on T. helix may result in a low mortality rate due to predation, thereby compensating for this species’ low growth rate.
Nutrient ratios influence variability in Pseudo-nitzschia species diversity and particulate domoic acid production in the Bay of Seine (France) Harmful Algae (IF 3.087) Pub Date : 2017-09-01 Maxine Thorel, Pascal Claquin, Mathilde Schapira, Romain Le Gendre, Philippe Riou, Didier Goux, Bertrand Le Roy, Virginie Raimbault, Anne-Flore Deton-Cabanillas, Pauline Bazin, Valérie Kientz-Bouchart, Juliette Fauchot
The population dynamics of different Pseudo-nitzschia species, along with particulate domoic acid (pDA) concentrations, were studied from May 2012 to December 2013 in the Bay of Seine (English Channel, Normandy). While Pseudo-nitzschia spp. blooms occurred during the two years of study, Pseudo-nitzschia species diversity and particulate domoic acid concentrations varied greatly. In 2012, three different species were identified during the spring bloom (P. australis, P. pungens and P. fraudulenta) with high pDA concentrations (∼1400 ng l−1) resulting in shellfish harvesting closures. In contrast, the 2013 spring was characterised by a P. delicatissima bloom without any toxic event. Above all, the results show that high pDA concentrations coincided with the presence of P. australis and with potential silicate limitation (Si:N < 1), while nitrate concentrations were still replete. The contrasting environmental conditions between 2012 and 2013 highlight different environmental controls that might favour the development of either P. delicatissima or P. australis. This study points to the key role of Pseudo-nitzschia diversity and cellular toxicity in the control of particulate domoic acid variations and highlights the fact that diversity and toxicity are influenced by nutrients, especially nutrient ratios.
The prevalence of benthic dinoflagellates associated with ciguatera fish poisoning in the central Red Sea Harmful Algae (IF 3.087) Pub Date : 2017-09-09 Daniela Catania, Mindy L. Richlen, Yim Ling Mak, Steve L. Morton, Elizabeth H. Laban, Yixiao Xu, Donald M. Anderson, Leo Lai Chan, Michael L. Berumen
This study confirms the presence of the toxigenic benthic dinoflagellates Gambierdiscus belizeanus and Ostreopsis spp. in the central Red Sea. To our knowledge, this is also the first report of these taxa in coastal waters of Saudi Arabia, indicating the potential occurrence of ciguatera fish poisoning (CFP) in that region. During field investigations carried out in 2012 and 2013, a total of 100 Turbinaria and Halimeda macroalgae samples were collected from coral reefs off the Saudi Arabian coast and examined for the presence of Gambierdiscus and Ostreopsis, two toxigenic dinoflagellate genera commonly observed in coral reef communities around the world. Both Gambierdiscus and Ostreopsis spp. were observed at low densities (<200 cells g−1 wet weight algae). Cell densities of Ostreopsis spp. were significantly higher than Gambierdiscus spp. at most of the sampling sites, and abundances of both genera were negatively correlated with seawater salinity. To assess the potential for ciguatoxicity in this region, several Gambierdiscus isolates were established in culture and examined for species identity and toxicity. All isolates were morphologically and molecularly identified as Gambierdiscus belizeanus. Toxicity analysis of two isolates using the mouse neuroblastoma cell-based assay for ciguatoxins (CTX) confirmed G. belizeanus as a CTX producer, with a maximum toxin content of 6.50 ± 1.14 × 10−5 pg P-CTX-1 eq. cell−1. Compared to Gambierdiscus isolates from other locations, these were low toxicity strains. The low Gambierdiscus densities observed along with their comparatively low toxin contents may explain why CFP is unidentified and unreported in this region. Nevertheless, the presence of these potentially toxigenic dinoflagellate species at multiple sites in the central Red Sea warrants future study on their possible effects on marine food webs and human health in this region.
Potential human health risk assessment of cylindrospermopsin accumulation and depuration in lettuce and arugula Harmful Algae (IF 3.087) Pub Date : 2017-09-09 Micheline Kézia Cordeiro-Araújo, Mathias Ahii Chia, Maria do Carmo Bittencourt-Oliveira
Newly discovered role of the heterotrophic nanoflagellate Katablepharis japonica, a predator of toxic or harmful dinoflagellates and raphidophytes Harmful Algae (IF 3.087) Pub Date : 2017-09-11 Ji Eun Kwon, Hae Jin Jeong, So Jin Kim, Se Hyeon Jang, Kyung Ha Lee, Kyeong Ah Seong
Heterotrophic nanoflagellates are ubiquitous and known to be major predators of bacteria. The feeding of free-living heterotrophic nanoflagellates on phytoplankton is poorly understood, although these two components usually co-exist. To investigate the feeding and ecological roles of major heterotrophic nanoflagellates Katablepharis spp., the feeding ability of Katablepharis japonica on bacteria and phytoplankton species and the type of the prey that K. japonica can feed on were explored. Furthermore, the growth and ingestion rates of K. japonica on the dinoflagellate Akashiwo sanguinea—a suitable algal prey item—heterotrophic bacteria, and the cyanobacteria Synechococcus sp., as a function of prey concentration were determined. Among the prey tested, K. japonica ingested heterotrophic bacteria, Synechococcus sp., the prasinophyte Pyramimonas sp., the cryptophytes Rhodomonas salina and Teleaulax sp., the raphidophytes Heterosigma akashiwo and Chattonella ovata, the dinoflagellates Heterocapsa rotundata, Amphidinium carterae, Prorocentrum donghaiense, Alexandrium minutum, Cochlodinium polykrikoides, Gymnodinium catenatum, A. sanguinea, Coolia malayensis, and the ciliate Mesodinium rubrum, however, it did not feed on the dinoflagellates Alexandrium catenella, Gambierdiscus caribaeus, Heterocapsa triquetra, Lingulodinium polyedra, Prorocentrum cordatum, P. micans, and Scrippsiella acuminata and the diatom Skeletonema costatum. Many K. japonica cells attacked and ingested a prey cell together after pecking and rupturing the surface of the prey cell and then uptaking the materials that emerged from the ruptured cell surface. Cells of A. sanguinea supported positive growth of K. japonica, but neither heterotrophic bacteria nor Synechococcus sp. supported growth. The maximum specific growth rate of K. japonica on A. sanguinea was 1.01 d−1. In addition, the maximum ingestion rate of K. japonica for A. sanguinea was 0.13 ng C predator−1d−1 (0.06 cells predator−1d−1). The maximum ingestion rate of K. japonica for heterotrophic bacteria was 0.019 ng C predator−1d−1 (266 bacteria predator−1d−1), and the highest ingestion rate of K. japonica for Synechococcus sp. at the given prey concentrations of up to ca. 107 cells ml−1 was 0.01 ng C predator−1d−1 (48 Synechococcus predator−1d−1). The maximum daily carbon acquisition from A. sanguinea, heterotrophic bacteria, and Synechococcus sp. were 307, 43, and 22%, respectively, of the body carbon of the predator. Thus, low ingestion rates of K. japonica on heterotrophic bacteria and Synechococcus sp. may be responsible for the lack of growth. The results of the present study clearly show that K. japonica is a predator of diverse phytoplankton, including toxic or harmful algae, and may also affect the dynamics of red tides caused by these prey species.
Effect of CO2 on growth and toxicity of Alexandrium tamarense from the East China Sea, a major producer of paralytic shellfish toxins Harmful Algae (IF 3.087) Pub Date : 2017-09-14 Min Pang, Jintao Xu, Pei Qu, Xuewei Mao, Zhenxing Wu, Ming Xin, Ping Sun, Zongxing Wang, Xuelei Zhang, Hongju Chen
In recent decades, the frequency and intensity of harmful algal blooms (HABs), as well as a profusion of toxic phytoplankton species, have significantly increased in coastal regions of China. Researchers attribute this to environmental changes such as rising atmospheric CO2 levels. Such addition of carbon into the ocean ecosystem can lead to increased growth, enhanced metabolism, and altered toxicity of toxic phytoplankton communities resulting in serious human health concerns. In this study, the effects of elevated partial pressure of CO2 (pCO2) on the growth and toxicity of a strain of Alexandrium tamarense (ATDH) widespread in the East and South China Seas were investigated. Results of these studies showed a higher specific growth rate (0.31 ± 0.05 day−1) when exposed to 1000 μatm CO2, (experimental), with a corresponding density of (2.02 ± 0.19) × 107 cells L−1, that was significantly larger than cells under 395 μatm CO2(control). These data also revealed that elevated pCO2 primarily affected the photosynthetic properties of cells in the exponential growth phase. Interestingly, measurement of the total toxin content per cell was reduced by half under elevated CO2 conditions. The following individual toxins were measured in this study: C1, C2, GTX1, GTX2, GTX3, GTX4, GTX5, STX, dcGTX2, dcGTX3, and dcSTX. Cells grown in 1000 μatm CO2 showed an overall decrease in the cellular concentrations of C1, C2, GTX2, GTX3, GTX5, STX, dcGTX2, dcGTX3, and dcSTX, but an increase in GTX1 and GTX4. Total cellular toxicity per cell was measured revealing an increase of nearly 60% toxicity in the presence of elevated CO2 compared to controls. This unusual result was attributed to a significant increase in the cellular concentrations of the more toxic derivatives, GTX1 and GTX4.Taken together; these findings indicate that the A. tamarense strain ATDH isolated from the East China Sea significantly increased in growth and cellular toxicity under elevated pCO2 levels. These data may provide vital information regarding future HABs and the corresponding harmful effects as a result of increasing atmospheric CO2.
Domoic acid in a marine pelagic food web: Exposure of southern right whales Eubalaena australis to domoic acid on the Península Valdés calving ground, Argentina Harmful Algae (IF 3.087) Pub Date : 2017-09-14 Valeria C. D’Agostino, Mariana Degrati, Viviana Sastre, Norma Santinelli, Bernd Krock, Torben Krohn, Silvana L. Dans, Mónica S. Hoffmeyer
The gulfs that surround Península Valdés (PV), Golfo Nuevo and Golfo San José in Argentina, are important calving grounds for the southern right whale Eubalaena australis. However, high calf mortality events in recent years could be associated with phycotoxin exposure. The present study evaluated the transfer of domoic acid (DA) from Pseudo-nitzschia spp., potential producers of DA, to living and dead right whales via zooplanktonic vectors, while the whales are on their calving ground at PV. Phytoplankton and mesozooplankton (primary prey of the right whales at PV and potential grazers of Pseudo-nitzschia cells) were collected during the 2015 whale season and analyzed for species composition and abundance. DA was measured in plankton and fecal whale samples (collected during whale seasons 2013, 2014 and 2015) using liquid chromatography coupled to tandem mass spectrometry (LC–MS/MS). The genus Pseudo-nitzschia was present in both gulfs with abundances ranging from 4.4 × 102 and 4.56 × 105 cell l−1. Pseudo-nitzschia australis had the highest abundance with up to 4.56 × 105 cell l−1. DA in phytoplankton was generally low, with the exception of samples collected during a P. australis bloom. No clear correlation was found between DA in phytoplankton and mesozooplankton samples. The predominance of copepods in mesozooplankton samples indicates that they were the primary vector for the transfer of DA from Pseudo-nitzschia spp. to higher trophic levels. High levels of DA were detected in four whale fecal samples (ranging from 0.30 to 710 μg g−1 dry weight of fecal sample or from 0.05 and 113.6 μg g−1 wet weight assuming a mean water content of 84%). The maximum level of DA detected in fecal samples (710 μg DA g−1 dry weight of fecal sample) is the highest reported in southern right whales to date. The current findings demonstrate for the first time that southern right whales, E. australis, are exposed to DA via copepods as vectors during their calving season in the gulfs of PV.
Transcriptional response of the harmful raphidophyte Heterosigma akashiwo to nitrate and phosphate stress Harmful Algae (IF 3.087) Pub Date : 2017-09-06 Sheean T. Haley, Harriet Alexander, Andrew R. Juhl, Sonya T. Dyhrman
The marine eukaryotic alga Heterosigma akashiwo (Raphidophyceae) is known for forming ichthyotoxic harmful algal blooms (HABs). In the past 50 years, H. akashiwo blooms have increased, occurring globally in highly eutrophic coastal and estuarine systems. These systems often incur dramatic physicochemical changes, including macronutrient (nitrogen and phosphorus) enrichment and depletion, on short timescales. Here, H. akashiwo cultures grown under nutrient replete, low N and low P growth conditions were examined for changes in biochemical and physiological characteristics in concert with transcriptome sequencing to provide a mechanistic perspective on the metabolic processes involved in responding to N and P stress. There was a marked difference in the overall transcriptional pattern between low N and low P transcriptomes. Both nutrient stresses led to significant changes in the abundance of thousands of contigs related to a wide diversity of metabolic pathways, with limited overlap between the transcriptomic responses to low N and low P. Enriched contigs under low N included many related to nitrogen metabolism, acquisition, and transport. In addition, metabolic modules like photosynthesis and carbohydrate metabolism changed significantly under low N, coincident with treatment-specific changes in photosynthetic efficiency and particulate carbohydrate content. P-specific contigs responsible for P transport and organic P use were more enriched in the low P treatment than in the replete control and low N treatment. These results provide new insight into the genetic mechanisms that distinguish how this HAB species responds to these two common nutrient stresses, and the results can inform future field studies, linking transcriptional patterns to the physiological ecology of H. akashiwo in situ.
Biogeography of bloom-forming microcystin producing and non-toxigenic populations of Dolichospermum lemmermannii (Cyanobacteria) Harmful Algae (IF 3.087) Pub Date : 2017-06-03 Camilla Capelli, Andreas Ballot, Leonardo Cerasino, Alessio Papini, Nico Salmaso
In the last decades, the cyanobacterium Dolichospermum lemmermannii showed an increasing spread to Southern Europe, raising serious concerns due to its ability to produce cyanotoxins. The widening of its geographic distribution and the observation of strains showing high optimum temperature underline its ecological heterogeneity, suggesting the existence of different ecotypes. To investigate its biogeography, new isolates from different European water bodies, together with strains maintained by the Norwegian Institute for Water Research Culture Collection of Algae, were genetically characterised for the 16S rRNA gene and compared with strains obtained from public repositories. Geographic distance highly influenced the differentiation of genotypes, further suggesting the concurrent role of geographic isolation, physical barriers and environmental factors in promoting the establishment of phylogenetic lineages adapted to specific habitats. Differences among populations were also examined by morphological analysis and evaluating the toxic potential of single strains, which revealed the exclusive ability of North European strains to produce microcystins, whereas the populations in Southern Europe tested negative for a wide range of cyanotoxins. The high dispersion ability and the existence of toxic genotypes indicate the possible spread of harmful blooms in other temperate regions.
Some contents have been Reproduced by permission of The Royal Society of Chemistry.
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