Effect of ciliate strain, size, and nutritional content on the growth and toxicity of mixotrophic Dinophysis acuminata Harmful Algae (IF 4.138) Pub Date : 2018-08-18 Juliette L. Smith, Mengmeng Tong, David Kulis, Donald M. Anderson
Previous studies indicate differences in bloom magnitude and toxicity between regional populations, and more recently, between geographical isolates of Dinophysis acuminata; however, the factors driving differences in toxicity/toxigenicity between regions/strains have not yet been fully elucidated. Here, the roles of prey strains (i.e., geographical isolates) and their associated attributes (i.e., biovolume and nutritional content) were investigated in the context of growth and production of toxins as a possible explanation for regional variation in toxicity of D. acuminata. The mixotrophic dinoflagellate, D. acuminata, isolated from NE North America (MA, U.S.) was offered a matrix of prey lines in a full factorial design, 1 × 2 × 3; one dinoflagellate strain was fed one of two ciliates, Mesodinium rubrum, isolated from coastal regions of Japan or Spain, which were grown on one of three cryptophytes (Teleaulax/Geminigera clade) isolated from Japan, Spain, or the northeastern USA. Additionally, predator: prey ratios were manipulated to explore effects of the prey’s total biovolume on Dinophysis growth or toxin production. These studies revealed that the biovolume and nutritional status of the two ciliates, and less so the cryptophytes, impacted the growth, ingestion rate, and maximum biomass of D. acuminata. The predator’s consumption of the larger, more nutritious prey resulted in an elevated growth rate, greater biomass, and increased toxin quotas and total toxin per mL of culture. Grazing on the smaller, less nutritious prey, led to fewer cells in the culture but relatively more toxin exuded from the cells on per cell basis. Once the predator: prey ratios were altered so that an equal biovolume of each ciliate was delivered, the effect of ciliate size was lost, suggesting the predator can compensate for reduced nutrition in the smaller prey item by increasing grazing. While significant ciliate-induced effects were observed on growth and toxin metrics, no major shifts in toxin profile or intracellular toxin quotas were observed that could explain the large regional variations observed between geographical populations of this species.
Genetic evidence in tracking the origin of Ulva prolifera blooms in the Yellow Sea, China Harmful Algae (IF 4.138) Pub Date : 2018-08-15 Qing-Chun Zhang, Ren-Cheng Yu, Zhen-Fan Chen, Li-Mei Qiu, Yun-Feng Wang, Fan-Zhou Kong, Hui-Xia Geng, Yue Zhao, Peng Jiang, Tian Yan, Ming-Jiang Zhou
Recurrent green tides have been recorded in the Yellow Sea for 11 consecutive years. The origin of floating green algae in the Yellow Sea, however, remains a subject of debate. Previous studies suggest that the major bloom-forming green alga Ulva prolifera represent a unique ecotype different from other attached populations of U. prolifera in China. In this study, 97 green algal samples collected during the 2012 green-tide event and from other locations along the coastline of China were analyzed. Based on the sequences of nuclear ribosomal RNA gene (rDNA) internal transcribed spacer (ITS) region and 5S rDNA spacer region, the green alga U. prolifera in the samples were identified. The intraspecific genetic diversity within U. prolifera was then examined using sequences of 5S rDNA spacer and a marker of sequence characterized amplified region (SCAR) highly specific for bloom-forming U. prolifera in the Yellow Sea. The screening results for SCAR marker demonstrated that U. prolifera attached to aquaculture rafts in Subei Shoal belong to the same ecotype of the bloom-forming U. prolifera in the Yellow Sea. These findings offer genetic evidence that aquaculture rafts in Subei Shoal are a major source of floating green algae in the Yellow Sea.
Sympatric occurrence of two Azadinium poporum ribotypes in the Eastern Mediterranean Sea Harmful Algae (IF 4.138) Pub Date : 2018-08-14 Zhaohe Luo, Bernd Krock, Antonia Giannakourou, Amalia Venetsanopoulou, Kalliopi Pagou, Urban Tillmann, Haifeng Gu
The marine dinoflagellate Azadinium poporum produce azaspiracids (AZA) and has been recorded widely in the world. However, information on its biogeography is still limited, especially in view of the fact that A. poporum comprises several genetically differentiated groups. A total of 18 strains of A. poporum were obtained from the Eastern Mediterranean area by incubating surface sediment collected from Ionian Sea of Greece. The morphology of these strains was examined with light microscopy and scanning electron microscopy. Small subunit ribosomal DNA (SSU rDNA), large subunit ribosomal DNA (LSU rDNA) and internal transcribed spacer (ITS) sequences were obtained from all cultured strains. Molecular phylogeny based on concatenated SSU, LSU and ITS sequences confirmed three ribotypes within A. poporum and revealed two subclades within ribotypes A and C. Greek strains of A. poporum ribotype A were nested within ribotype A2 together with strains from Western Mediterranean Sea and French Atlantic, and Greek strains of A. poporum ribotype C were nested within ribotype C2 together with a strain from the Gulf of Mexico. Growth experiments on four selected strains revealed that ribotypes A and C from Greece differed in their growth at higher temperatures, indicating that they are physiologically differentiated. Azaspiracid profiles were analyzed for 15 cultured A. poporum strains using LCMS/MS and demonstrate that the A. poporum ribotype A from Greece produce low level or no AZA and A. poporum ribotype C from Greece produces predominantly AZA-40 (9.6–30.2 fg cell−1) followed by AZA-2 (2.1–2.6 fg cell−1). The first record of AZA-40 producing A. poporum from the Mediterranean suggests that this species is a potential source for azaspiracid contaminations in shellfish from the Eastern Mediterranean Sea.
Insights into cyanophage-mediated dynamics of nodularin and other non-ribosomal peptides in Nodularia spumigena Harmful Algae (IF 4.138) Pub Date : 2018-08-14 Sigitas Šulčius, Hanna Mazur-Marzec, Irma Vitonytė, Kotryna Kvederavičiūtė, Jolita Kuznecova, Eugenijus Šimoliūnas, Karin Holmfeldt
The effect of cyanophage infection and lysis on the dynamics of the hepatotoxin nodularin (NOD) and other non-ribosomal peptides (NRPs) produced by cyanobacteria is poorly understood. In this study, changes in concentration of NOD and other NRPs during cyanophage infection of the filamentous cyanobacteria Nodularia spumigena were assessed using incubation experiments. Viral infection and lysis were associated with a significant reduction (93% at the 96 h post infection) of N. spumigena cell density. While no correlation between N. spumigena abundance and total concentration of NOD (ng mL−1) within the infected cells was observed, cellular NOD quota (ng cell−1) gradually increased in the remaining cyanophage resistant N. spumigena subpopulation. Lysis of N. spumigena cells resulted in a substantial increase (>57 times) of dissolved NOD concentration in the culture medium. The relative concentration of other cyclic (anabaenopeptins) and linear (aeruginosins, spumigins) NRPs produced by N. spumigena also increased in response to cyanophage addition. This study highlights the importance of cyanophage infection on the population toxicity of filamentous cyanobacteria and demonstrates a significant contribution of virus-mediated cell lysis on the conversion of NOD from the particulate to dissolved phase.
Habitat complexity affects benthic harmful dinoflagellate assemblages in the fringing reef of Rawa Island, Malaysia Harmful Algae (IF 4.138) Pub Date : 2018-08-10 Hwa Lin Yong, Nurin Izzati Mustapa, Li Keat Lee, Zhen Fei Lim, Toh Hii Tan, Gires Usup, Haifeng Gu, R. Wayne Litaker, Patricia A. Tester, Po Teen Lim, Chui Pin Leaw
Few studies have investigated the effect of fine-scale habitat differences on the dynamics of benthic harmful dinoflagellate assemblages. To determine how these microhabitat differences affect the distribution and abundance of the major benthic harmful dinoflagellate genera in a tropical coral reef ecosystem, a field study was undertaken between April–September 2015 and January 2016 on the shallow reef flat of the fringing reef of Rawa Island, Terengganu, Malaysia. Sampling of benthic dinoflagellates was carried out using an artificial substrate sampling method (fiberglass screens). Benthic microhabitats surrounding the sampling screens were characterized simultaneously from photographs of a 0.25-m2 quadrat based on categories of bottom substrate types. Five taxonomic groups of benthic dinoflagellates, Ostreopsis, Gambierdiscus, Prorocentrum, Amphidinium, and Coolia were identified, and cells were enumerated using a light microscope. The results showed Gambierdiscus was less abundant than other genera throughout the study period, with maximum abundance of 1.2 × 103 cells 100 cm−2. While most taxa were present on reefs with high coral cover, higher cell abundances were observed in reefs with high turf algal cover and coral rubble, with the exception of Ostreopsis, where the abundance reached a maximum of 3.4 × 104 cells 100 cm−2 in habitats with high coral cover. Microhabitat heterogeneity was identified as a key factor governing the benthic harmful dinoflagellate assemblages and may account for much of the observed variability in dominant taxa. This finding has significant implications for the role of variability in the benthic harmful algal bloom (BHAB) outbreaks and the potential in identifying BHAB-related toxin transfer pathways and the key vectors in the food webs.
Microcystin interferes with defense against high oxidative stress in harmful cyanobacteria Harmful Algae (IF 4.138) Pub Date : 2018-08-10 J. Merijn Schuurmans, Bregje W. Brinkmann, A. Katharina Makower, Elke Dittmann, Jef Huisman, Hans C.P. Matthijs
Harmful cyanobacteria producing toxic microcystins are a major concern in water quality management. In recent years, hydrogen peroxide (H2O2) has been successfully applied to suppress cyanobacterial blooms in lakes. Physiological studies, however, indicate that microcystin protects cyanobacteria against oxidative stress, suggesting that H2O2 addition might provide a selective advantage for microcystin-producing (toxic) strains. This study compares the response of a toxic Microcystis strain, its non-toxic mutant, and a naturally non-toxic Microcystis strain to H2O2 addition representative of lake treatments. All three strains initially ceased growth upon H2O2 addition. Contrary to expectation, the non-toxic strain and non-toxic mutant rapidly degraded the added H2O2 and subsequently recovered, whereas the toxic strain did not degrade H2O2 and did not recover. Experimental catalase addition enabled recovery of the toxic strain, demonstrating that rapid H2O2 degradation is indeed essential for cyanobacterial survival. Interestingly, prior to H2O2 addition, gene expression of a thioredoxin and peroxiredoxin was much lower in the toxic strain than in its non-toxic mutant. Thioredoxin and peroxiredoxin are both involved in H2O2 degradation, and microcystin may potentially suppress their activity. These results show that microcystin-producing strains are less prepared for high levels of oxidative stress, and are therefore hit harder by H2O2 addition than non-toxic strains.
A decade and a half of Pseudo-nitzschia spp. and domoic acid along the coast of southern California Harmful Algae (IF 4.138) Pub Date : 2018-08-10 Jayme Smith, Paige Connell, Richard H. Evans, Alyssa G. Gellene, Meredith D.A. Howard, Burton H. Jones, Susan Kaveggia, Lauren Palmer, Astrid Schnetzer, Bridget N. Seegers, Erica L. Seubert, Avery O. Tatters, David A. Caron
Blooms of the marine diatom genus Pseudo-nitzschia that produce the neurotoxin domoic acid have been documented with regularity along the coast of southern California since 2003, with the occurrence of the toxin in shellfish tissue predating information on domoic acid in the particulate fraction in this region. Domoic acid concentrations in the phytoplankton inhabiting waters off southern California during 2003, 2006, 2007, 2011 and 2017 were comparable to some of the highest values that have been recorded in the literature. Blooms of Pseudo-nitzschia have exhibited strong seasonality, with toxin appearing predominantly in the spring. Year-to-year variability of particulate toxin has been considerable, and observations during 2003, 2006, 2007, 2011 and again in 2017 linked domoic acid in the diets of marine mammals and seabirds to mass mortality events among these animals. This work reviews information collected during the past 15 years documenting the phenology and magnitude of Pseudo-nitzschia abundances and domoic acid within the Southern California Bight. The general oceanographic factors leading to blooms of Pseudo-nitzschia and outbreaks of domoic acid in this region are clear, but subtle factors controlling spatial and interannual variability in bloom magnitude and toxin production remain elusive.
The impact of short-term depositions of macroalgal blooms on widgeon-grass meadows in a river-dominated estuary Harmful Algae (IF 4.138) Pub Date : 2018-07-27 Marianna Lanari, Margareth S. Copertino, Leonir A. Colling, Fábio C. Bom
Macroalgal blooms can trigger adverse biogeochemical conditions at the sediment-water interface of shallow coastal areas, hence threatening critical habitats such as seagrasses meadows. The direction and magnitude of macroalgal blooms impacts on the aquatic ecosystem can be context-dependent, varying according to the local hydrodynamic conditions. Thus, studies investigating the impacts of stagnant algal depositions on the benthos may fail to address realistic situations and interactions which are common in well-flushed systems. This is especially true for the South America coast, where no study has investigated the effects of macroalgal blooms on seagrasses meadows. To fully understand the impacts of macroalgal blooms on sediment biogeochemistry and seagrass habitats across distinct environmental conditions and biogeographical regions, two independent, complementary field experiments replicated the natural temporal patterns of drift macroalgal mats depositions on unvegetated and vegetated (Ruppia maritima meadows) shoals of the Patos Lagoon estuary (PLE), a subtropical, high hydrodynamic system in southern Brazil. Transitory depositions of algal mats alleviated deleterious biogeochemical conditions in the sediment-water interface of unvegetated bottoms. Nevertheless, these unstable algal depositions promoted significant reductions in R. maritima biomass, by reducing their shoot height and density, and rhizome length. That plant biomass reductions were followed by a decrease in the abundance of the dominant infaunal tanaidacean Monokalliapseudes schubarti, indicating that algal impacts on seagrasses were transferred to higher trophic levels. Our results suggest that, although unstable deposition of drift algal mats can attenuate potential adverse impacts at the sediment-water interface, the physical stress during mats advection can still trigger small seagrass losses. This process may diminish the resilience of R. maritima meadows in the PLE, with impacts on estuarine nutrient cycling and secondary production. We conclude that, although harmful drift macroalgal blooms area global phenomenon, the mechanisms through which macroalgae impair seagrass habitats may vary according to the environmental context. Therefore, further studies are necessary to identify the underlying mechanisms of drift macroalgae-seagrass-macrofauna interactions in high hydrodynamic systems and their generality across distinct biogeographical areas.
Seawater nitrogen concentration and light independently alter performance, growth, and resource allocation in the bloom-forming seaweeds Ulva lactuca and Ulvaria obscura (Chlorophyta) Harmful Algae (IF 4.138) Pub Date : 2018-07-24 Kathryn L. Van Alstyne
Ulva lactuca and Ulvaria obscura are seaweeds that form green tides on Salish Sea shores. They have similar macroscopic morphologies but differ in their biochemistries and physiological responses. To understand how they are affected by changes in environmental conditions, a factorial experiment was conducted in which algae were grown in artificial seawater with either low (10 μM) or high (160 μM) nitrate (NO3−) concentrations at high (29 mol photons·m−2.day−1) and low (4 mol photons·m−2.day−1) light levels. Light and NO3− affected algal responses, but always independently. After two weeks, U. lactuca grown in high light were larger, had lower maximum quantum yields (MQYs), and lower nitrogen (N), carbon (C), pigment, and dimethylsulfoniopropionate (DMSP) concentrations, respectively, relative to algae in low light. In contrast, U. obscura growth was unaffected by light. Like U. lactuca, U. obscura grown in high light had lower MQYs, and N, pigment, and DMSP concentrations. In high light, U. obscura also had 89% higher dopamine concentrations and a tendency to fragment. Both U. lactuca and U. obscura grown in 160 μM NO3− were larger, had higher MQYs, and higher N, pigment, and DMSP concentrations, respectively, than algae in 10 μM NO3−. Also, when U. obscura was grown in the 160 μM NO3− medium, it significantly increased its surface area/mass ratio. Although both species grew faster in high NO3−, high light only promoted the growth of Ulva, which may explain the dominance of Ulva in summer months. High light was physiologically stressful to both species and caused increases in photoprotective mechanisms, such as the production of dopamine, a melanin precursor, in Ulvaria, and DMSP lysis in Ulva to generate antioxidants. Growing in 10 μM NO3- produced responses that were consistent with nitrogen limitation and had greater impacts on Ulvaria than Ulva, suggesting that Ulvaria responds more strongly to eutrophication.
Overvalued allelopathy and overlooked effects of humic acid-like substances on Microcystis aeruginosa and Scenedesmus obliquus competition Harmful Algae (IF 4.138) Pub Date : 2018-07-21 Miaomiao Zhao, Xinyi Chen, Ning Ma, Qiuyue Zhang, Dong Qu, Ming Li
To form Microcystis blooms, Microcystis must be competitively dominant to other phytoplankton species to produce enough biomass. The aim of this study was to determine the competition mechanisms between Microcystis aeruginosa and Scenedesmus obliquus. M. aeruginosa and S. obliquus were separately cultured in the filtrate of mono and mixed cultures of M. aeruginosa and S. obliquus with varying treatments concerning N, P and iron availability. The inhibition rate for M. aeruginosa was 20–31% when cultured in mono and mixed culture filtrates enriched with N and P, but this rate was reduced to −15 to 19% when cultured in filtrates enriched with N, P and iron. The inhibition rate for M. aeruginosa decreased from 80 to 100% to 11–39% in dialytic filtrates. However, there were no differences in inhibition rate for S. obliquus, regardless of filtrate or dialytic filtrate treatments. The potential allelochemical, 2-butyl-octanol (0.144 mg L−1), was found to have little inhibitory effect to M. aeruginosa or S. obliquus. Thus, previously reported allelopathy to Microcystis would be overestimated. We also report a new mechanism in phytoplankton competition in this study. The phytoplankton secreted humic acid-like substances that can reduce the bioavailability of iron, resulting in the inhibition of other phytoplankton.
Effects of salinity variation on growth and yessotoxin composition in the marine dinoflagellate Lingulodinium polyedra from a Skagerrak fjord system (western Sweden) Harmful Algae (IF 4.138) Pub Date : 2018-07-17 Carolin Peter, Bernd Krock, Allan Cembella
The marine dinoflagellate Lingulodinium polyedra is a toxigenic species capable of forming high magnitude and occasionally harmful algal blooms (HABs), particularly in temperate coastal waters throughout the world. Three cultured isolates of L. polyedra from a fjord system on the Skagerrak coast of Sweden were analyzed for their growth characteristics and to determine the effects of a strong salinity gradient on toxin cell quotas and composition. The cell quota of yessotoxin (YTX) analogs, as determined by liquid chromatography coupled with tandem mass spectrometry (LC–MS/MS), ranged widely among strains. For two strains, the total toxin content remained constant over time in culture, but for the third strain, the YTX cell quota significantly decreased (by 32%) during stationary growth phase. The toxin profiles of the three strains differed markedly and none produced YTX. The analog 41a-homo-YTX (m/z 1155), its putative methylated derivative 9-Me-41a-homo-YTX (m/z 1169) and an unspecified keto-YTX (m/z 1047) were detected in strain LP29-10H, whereas strain LP30-7B contained nor-YTX (m/z 1101), and two unspecified YTX analogs at m/z 1159 and m/z 1061. The toxin profile of strain LP30-8D comprised two unspecified YTX analogs at m/z 1061 and m/z 991 and carboxy-YTX (m/z 1173). Strain LP30-7B cultured at multiple salinities (10, 16, 22, 28 and 34) did not tolerate the lowest salinity (10), but there was a statistically significant decrease (by 21%) in toxin cell quota between growth at the highest versus lower permissible salinities. The toxin profile for strain LP30-7B remained constant over time for a given salinity. At lower salinities, however, the proportion of the unspecified YTX analog (m/z 1061) was significantly higher, especially with respect to nor-YTX (m/z 1101). This study shows high intra-specific variability in yessotoxin composition among strains from the same geographical region and inconsistency in toxin cell quota under different environmental regimes and growth stages in culture. This variation has important implications for the kinetics of YTX production and food web transfer in natural bloom populations from diverse geographical regions.
The toxic benthic dinoflagellate Prorocentrum maculosum Faust is a synonym of Prorocentrum hoffmannianum Faust Harmful Algae (IF 4.138) Pub Date : 2018-07-11 Francisco Rodríguez, Pilar Riobó, Guillermo D. Crespín, Antonio H. Daranas, Caterina R. de Vera, Manuel Norte, José Javier Fernández, Santiago Fraga
Three strains of the toxic benthic dinoflagellate Prorocentrum hoffmannianum were isolated in the Canary Islands (north-east Atlantic Ocean, Spain). The identity of the strains was determined by phylogenetic analyses of partial LSU rDNA (D1-D2 regions) but their morphology based on SEM images corresponded to P. maculosum. Their toxin profiles were analyzed by liquid chromatography and high resolution mass spectrometry analysis (LC–HRMS) on cell extracts and culture media. Okadaic acid and three analogs were detected in all strains. Rather, in culture media the detected compounds were variable among strains, two of them being okadaic acid analogs not found on cell extracts. As a result, the taxonomy of the species was revised and P. maculosum is proposed as a junior synonym of P. hoffmannianum whose description is emended.
Domoic acid in California sea lion fetal fluids indicates continuous exposure to a neuroteratogen poses risks to mammals Harmful Algae (IF 4.138) Pub Date : 2018-07-07 Kathi A. Lefebvre, Alicia Hendrix, Barbie Halaska, Padraig Duignan, Sara Shum, Nina Isoherranen, David J. Marcinek, Frances M.D. Gulland
Domoic acid (DA) is a neuroexcitotoxic amino acid that is naturally produced by some species of marine diatoms during harmful algal blooms (HABs). The toxin is transferred through the food web from plantivorous fish and shellfish to marine mammals resulting in significant morbidity and mortality. Due to the timing and location of DA producing HABs, it is well documented that pregnant female California sea lions (CSL) are regularly exposed to DA through their diet thereby posing exposure risks to a neuroteratogen in developing fetuses. In the present study, fluids from 36 fetuses sampled from naturally exposed pregnant CSLs were examined for DA. Domoic acid was detected in 79% of amniotic fluid (n = 24), 67% of allantoic fluid (n = 9), 75% of urine (n = 4), 41% of meconium (n = 17) and 29% of stomach content (n = 21) samples opportunistically collected from CSL fetuses. The distribution of DA in fetal samples indicates an increased prenatal exposure risk due to recirculation of DA in fetal fluids and continuous exposure to the developing brain.
The polychaete, Paraprionospio pinnata, is a likely vector of domoic acid to the benthic food web in the northern Gulf of Mexico Harmful Algae (IF 4.138) Pub Date : 2018-07-04 Melissa M. Baustian, Sibel Bargu, Wendy Morrison, Chelsea Sexton, Nancy N. Rabalais
A somewhat disparate, yet temporally cohesive, set of phytoplankton abundance, microphytobenthos, including the diatom Pseudo-nitzschia, benthic infauna, and sediment toxin data were used to develop a theory for the transfer of domoic acid (DA) from the toxic diatom to the benthos in the highly productive waters of the northern Gulf of Mexico near the Mississippi River plume. Archived samples and new data were used to test the theory that DA is likely to be incorporated into benthic consumers. High spring abundances of potentially toxic Pseudo-nitzschia diatoms were simultaneously present in the surface waters, bottom waters and on the seafloor. Examination of the gut contents of a typical deposit-feeding and suspension-feeding polychaete, Paraprionospio pinnata, during similar periods of high Pseudo-nitzschia abundance in surface water indicated consumption of the diatoms. Demersal fishes, particularly Atlantic croaker, are known to consume these polychaetes, with a potential for transfer of DA to even higher trophic levels. These findings warrant a theory to be tested with further studies about the trophic linkage of a phytoplankton toxin into the benthic food web.
Induction of domoic acid production in diatoms—Types of grazers and diatoms are important Harmful Algae (IF 4.138) Pub Date : 2018-07-02 Nina Lundholm, Bernd Krock, Uwe John, Jette Skov, Jinfeng Cheng, Marina Pančić, Sylke Wohlrab, Kristie Rigby, Torkel Gissel Nielsen, Erik Selander, Sara Harðardóttir
Grazers can induce toxin (domoic acid, DA) production in diatoms. The toxic response has been observed in two species of Pseudo-nitzschia and was induced by Calanus copepods. In this study, interactions between diatoms and copepods were further explored using different species of diatoms and copepods. All herbivorous copepods induced toxin production, whereas exposure to carnivorous copepods did not. In line with this, increasing the number of herbivorous copepods resulted in even higher toxin production. The induced response is thus only elicited by copepods that pose a real threat to the responding cells, which supports that the induced toxin production in diatoms evolved as an inducible defense. The cellular toxin content in Pseudo-nitzschia was positively correlated to the concentration of a group of specific polar lipids called copepodamides that are excreted by the copepods. This suggests that copepodamides are the chemical cues responsible for triggering the toxin production. Carnivorous copepods were found to produce less or no copepodamides. Among the diatoms exposed to grazing herbivorous copepods, only two of six species of Pseudo-nitzschia and none of the Nitzschia or Fragilariopsis strains responded by producing DA, indicating that not all Pseudo-nitzschia species/strains are able to produce DA, and that different diatom species might have different strategies for coping with grazing pressure. Growth rate was negatively correlated to cellular domoic acid content indicating an allocation cost associated with toxin production. Long-term grazing experiments showed higher mortality rates of grazers fed toxic diatoms, supporting the hypothesis that DA production is an induced defense mechanism.
The Yellow Sea green tide: A risk of macroalgae invasion Harmful Algae (IF 4.138) Pub Date : 2018-06-02 Jin Zhao, Peng Jiang, Ri Qiu, Yingying Ma, Chunhui Wu, Huihui Fu, Huaxin Chen, Fuchao Li
Large scale green tides have bloomed successively in the Yellow Sea since 2007. The floating ecotype of Ulva prolifera, which is responsible for the environmental disaster, drifted a long distance during the blooming time and was exotic to the coastal area. The Yellow Sea green tide can be a potential source to incur bio-invasion. In this study, the distribution pattern and propagule pressure of the floating ecotype was investigated along the Qingdao coastline, which was seriously impacted by the green tide. Two out of 661 attached Ulva specimens collected in different seasons were identified as the floating ecotype by molecular markers, indicating that a few individuals of the floating ecotype had settled down, and their attached population could have spontaneously established. In seawater and sediments, the proportion of the floating ecotype in Ulva propagules reached up to 32% and 69% respectively when the floating algae was accumulating on seashore, which was a great propagule pressure to the local ecosystem. Results of the field test indicated that the available resources and the competition between the floating ecotype and the local Ulva species might be the main restrictions for settlement. Though the current scale of the established population is still small, the risk of biological invasion by the floating ecotype exists and it deserves more attention.
Variability and profiles of lipophilic toxins in bivalves from Great Britain during five and a half years of monitoring: Okadaic acid, dinophysis toxins and pectenotoxins Harmful Algae (IF 4.138) Pub Date : 2018-06-19 Monika Dhanji-Rapkova, Alison O’Neill, Benjamin H. Maskrey, Lewis Coates, Mickael Teixeira Alves, Rebecca J. Kelly, Robert G. Hatfield, Stephanie J. Rowland-Pilgrim, Adam M. Lewis, Myriam Algoet, Andrew D. Turner
Official control biotoxin testing of bivalve molluscs from Great Britain has been conducted by Cefas for over a decade. Reflecting the changes in legislation, bioassays were gradually replaced by analytical methods, firstly for analysis of Paralytic shellfish toxins, followed by introduction of liquid chromatography tandem mass spectrometric (LCMS/MS) method for lipophilic toxins (LTs) in 2011. Twelve compounds, representing three main groups of regulated lipophilic toxins, as well as two non-regulated cyclic imines were examined in over 20,500 samples collected between July 2011 and December 2016. The toxins belonging to Okadaic acid (OA) group toxins were the most prevalent and were quantified in 23% of samples, predominantly from Scotland. The temporal pattern of OA group occurrences remained similar each year, peaking in summer months and tailing off during autumn and winter, however their abundance and magnitude varied between years significantly, with concentrations reaching up to 4993 μg OA eq./kg. Three toxin profiles were identified, reflecting the relative contribution of the two main toxins, OA and dinophysis toxin-2 (DTX2). Dinophysis toxin-1 (DTX1) was less common and was never detected in samples with high proportions of DTX2. Inter-annual changes in profiles were observed within certain regions, with the most notable being an increase of DTX2 occurrences in north-west Scotland and England in the last three years of monitoring. In addition, seasonal changes of profiles were identified when OA, the dominant toxin in early summer, was replaced by higher proportions of DTX2 in late summer and autumn. The profile distribution possibly reflected the availability of individual Dinophysis species as a food source for shellfish, however persistence of DTX2 during autumn and winter in mussels might have also been attributed to their physiology. Mussels were the only species with higher average proportions of non-esterified toxins, while Pacific oysters, cockles, surf clams, razors and queen scallops contained almost exclusively ester forms. In addition, a temporal change in proportion of OA and DTX2 free form was observed in mussels. Pectenotoxin-2 (PTX2) was quantified only on rare occasions.
Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum Harmful Algae (IF 4.138) Pub Date : 2018-06-18 Houshuo Jiang, David M. Kulis, Michael L. Brosnahan, Donald M. Anderson
Predator-prey interactions of planktonic protists are fundamental to plankton dynamics and include prey selection, detection, and capture as well as predator detection and avoidance. Propulsive, morphology-specific behaviors modulate these interactions and therefore bloom dynamics. Here, interactions between the mixotrophic, harmful algal bloom (HAB) dinoflagellate Dinophysis acuminata and its ciliate prey Mesodinium rubrum were investigated through quantitative microvideography using a high-speed microscale imaging system (HSMIS). The dinoflagellate D. acuminata is shown to detect its M. rubrum prey via chemoreception while M. rubrum is alerted to D. acuminata via mechanoreception at much shorter distances (89 ± 39 μm versus 41 ± 32 μm). On detection, D. acuminata approaches M. rubrum with reduced speed. The ciliate M. rubrum responds through escape jumps that are long enough to detach its chemical trail from its surface, thereby disorienting the predator. To prevail, D. acuminata uses capture filaments and/or releases mucus to slow and eventually immobilize M. rubrum cells for easier capture. Mechanistically, results support the notion that the desmokont flagellar arrangement of D. acuminata lends itself to phagotrophy. In particular, the longitudinal flagellum plays a dominant role in generating thrust for the cell to swim forward, while at other times, it beats to supply a tethering or anchoring force to aid the generation of a posteriorly-directed, cone-shaped scanning current by the transverse flagellum. The latter is strategically positioned to generate flow for enhanced chemoreception and hydrodynamic camouflage, such that D. acuminata can detect and stealthily approach resting M. rubrum cells in the water column.
Screening of cyclic imine and paralytic shellfish toxins in isolates of the genus Alexandrium (Dinophyceae) from Atlantic Canada Harmful Algae (IF 4.138) Pub Date : 2018-07-06 Jiangbing Qiu, Cheryl Rafuse, Nancy I. Lewis, Aifeng Li, Fanping Meng, Daniel G. Beach, Pearse McCarron
The dinoflagellate genus Alexandrium Halim has frequently been associated with harmful algal blooms. Although a number of species from this genus are known to produce paralytic shellfish toxins (PST) and/or cyclic imines (CI), studies on comprehensive toxin profiling using techniques capable of detecting the full range of PST and CI analogues are limited. Isolates of Alexandrium spp. from Atlantic Canada were analyzed by targeted and untargeted liquid chromatography-tandem mass spectrometry (LC–MS). Results showed a number of distinct profiles and wide ranging cell quotas of PST and spirolides (SPX) in both A. catenella (Whedon & Kofoid) Balech and A. ostenfedii (Paulsen) Balech & Tangen. The concentration of PST in A. catenella ranged from 0.0029 to 54 fmol cell−1 with the major components being C2 and GTX4. In addition, putative PST metabolites were confirmed for the first time in A. catenella by high resolution MS/MS. By comparison, A. ostenfeldii isolates showed much lower concentrations of PST (
Recruitment-promoting of dormant Microcystis aeruginosa by three benthic bacterial species Harmful Algae (IF 4.138) Pub Date : 2018-06-05 Wansheng Zou, Zhi Wang, Qisheng Song, Shaoxian Tang, Yuande Peng
Quantifying harmful algal bloom thresholds for farmed salmon in southern Chile Harmful Algae (IF 4.138) Pub Date : 2018-06-18 Rodrigo M. Montes, Ximena Rojas, Paulina Artacho, Alfredo Tello, Renato A. Quiñones
Harmful algal blooms (HABs) have affected salmon farms in Chile since the early 1970′s, causing massive losses in fish. Two large HABs occurred in 2002 and 2009, during which Alexandrium catenella blooms killed tons of salmon over an extended geographic area in southern Chile. At the beginning of 2016, high and persistent densities of Pseudochattonella cf. verruculosa and A. catenella were detected in the estuarine and marine ecosystems of southern Chile. Mortality for this latter event reached 27 million salmon and trout (i.e. 39,000 tons). Unfortunately, the threshold concentrations of algae that could be harmful to the health of farmed salmon in southern Chile have not yet been quantified. Here, to protect fish farms from HABs, critical concentration levels, i.e. thresholds at which the behavior of farmed Salmo salar is affected by harmful algae were quantified using generalized linear mixed models (GLMM). An extensive database from southern Chile covering the period from 1989 to 2016 was analyzed. The database included salmon behavior, cell abundance of microalgae and oceanographic factors. For both species analyzed, the higher the cell abundance, the greater the probability of detecting anomalous behavior. A threshold of 397 cells/mL was estimated for A. catenella, although it can increase up to ca. >975 cells/mL at a Secchi depth >6 m and up to 874 cells/mL during flood tide. A threshold value <1 cell/mL for Pseudochattonella cf. verruculosa was found to be associated with anomalous salmon behavior, which significantly increased at a water temperature of 11 °C. Evidence for a relationship between fish behavior and mortality is provided.
Mycosporine-like amino acids (MAAs)—producing Microcystis in Lake Erie: Development of a qPCR assay and insight into its ecology Harmful Algae (IF 4.138) Pub Date : 2018-06-01 Chenlin Hu, Stuart A. Ludsin, Jay F. Martin, Elke Dittmann, Jiyoung Lee
Environmental factors influencing the distribution and abundance of Alexandrium catenella in Kachemak bay and lower cook inlet, Alaska Harmful Algae (IF 4.138) Pub Date : 2018-06-28 Mark W. Vandersea, Steven R. Kibler, Patricia A. Tester, Kristine Holderied, Dominic E. Hondolero, Kim Powell, Steve Baird, Angela Doroff, Darcy Dugan, R. Wayne Litaker
Despite the long history of paralytic shellfish poisoning (PSP) events in Alaska, little is known about the seasonal distribution and abundance of the causative organism, Alexandrium, or the environmental factors that govern toxic bloom development. To address this issue, a five year study (2012–2017) was undertaken in Kachemak Bay and lower Cook Inlet Alaska to determine how the occurrence of Alexandrium catenella, the dominant PSP-causing Alexandrium species, was influenced by temperature, salinity, nutrient concentrations, and other environmental factors. Cell concentrations from 572 surface water samples were estimated using quantitative PCR. Monthly sampling revealed a seasonal pattern of A. catenella bloom development that was positively correlated with water temperature. Prevailing salinity conditions did not significantly affect abundance, nor was nutrient limitation a direct factor. Elevated cell concentrations were detected in 35 samples from Kachemak Bay (100-3050 cell eq. L−1) while a maximum abundance of 67 cell eq. L−1 was detected in samples from lower Cook Inlet sites. Monitoring data showed average water temperatures in Kachemak Bay increased by ∼2 °C over the course of the study and were accompanied by an increase in Alexandrium abundance. Based on these findings, 7–8 °C appears to represent a temperature threshold for significant bloom development in Kachemak Bay, with the greatest risk of shellfish toxicity occurring when temperatures exceed 10–12 °C. The role of temperature is further supported by time series data from the Alaska Coastal Current (station GAK1), which showed that summertime shellfish toxicity events in Kachemak Bay generally followed periods of anomalously high winter water temperatures. These data indicate monitoring changes in water temperatures may be used as an early warning signal for subsequent development of shellfish toxicity in Kachemak Bay.
A closely-related clade of globally distributed bloom-forming cyanobacteria within the Nostocales Harmful Algae (IF 4.138) Pub Date : 2018-06-29 Connor B. Driscoll, Kevin A. Meyer, Sigitas Šulčius, Nathan M. Brown, Gregory J. Dick, Huansheng Cao, Giedrius Gasiūnas, Albertas Timinskas, Yanbin Yin, Zachary C. Landry, Timothy G. Otten, Timothy W. Davis, Susan B. Watson, Theo W. Dreher
Harmful epiphytic dinoflagellate assemblages on macrophytes in the Gulf of Tunis Harmful Algae (IF 4.138) Pub Date : 2018-06-15 Mohamed Amine Hachani, Amel Dhib, Afef Fathalli, Boutheina Ziadi, Souad Turki, Lotfi Aleya
The spatio-temporal distribution of epiphytic and planktonic microalgae coupled with environmental factors was investigated for a one-year period in the Gulf of Tunis (northeastern Tunisia). Harmful microalgae assemblages were dominated by three toxic epiphytic dinoflagellates: Ostreopsis sp., Prorocentrum lima and Coolia monotis. They were observed, both on macrophytes (1.03 × 105 cells g−1 FW ; 1.3 × 104 cells g−1 FW and 865 cells g−1 FW, respectively) and in the water column (2.35 × 104 cells L−1; 3.72 × 103 cells L−1; 1.04 × 103 cells L−1, respectively). Species abundances decreased with depth and maximum concentrations were found in shallow waters (0.5–1 m). The highest species abundance was registered both on macroalgae and seagrass with no special preference observed for either of these substrates. Redundancy analyses (RDA) show significant changes in these species abundances according to sites and seasons. The proliferation of Ostreopsis sp. is widespread in summer, when water temperature is warm, and especially in bay zones. The occurrence of P. lima and C. monotis blooms was mainly correlated to nutrients. In this study, macrophyte beds in the Gulf of Tunis were a reservoir of potentially toxic species that could pose a real threat, both to ecosystems and to public health.
Optimization of extraction methods for quantification of microcystin-LR and microcystin-RR in fish, vegetable, and soil matrices using UPLC–MS/MS Harmful Algae (IF 4.138) Pub Date : 2018-05-16 Manjunath Manubolu, Jiyoung Lee, Kenneth M. Riedl, Zi Xun Kua, Lindsay P. Collart, Stuart A. Ludsin
Human-driven environmental change has increased the occurrence of harmful cyanobacteria blooms in aquatic ecosystems. Concomitantly, exposure to microcystin (MC), a cyanobacterial toxin that can accumulate in animals, edible plants, and agricultural soils, has become a growing public health concern. For accurate estimation of health risks and timely monitoring, availability of reliable detection methods is imperative. Nonetheless, quantitative analysis of MCs in many types of biological and environmental samples has proven challenging because matrix interferences can hinder sample preparation and extraction procedures, leading to poor MC recovery. Herein, controlled experiments were conducted to enhance the use of ultra-performance liquid-chromatography tandem-mass spectrometry (UPLC–MS/MS) to recover MC-LR and MC-RR at a range of concentrations in seafood (fish), vegetables (lettuce), and environmental (soil) matrices. Although these experiments offer insight into detailed technical aspects of the MC homogenization and extraction process (i.e., sonication duration and centrifugation speed during homogenization; elution solvent to use during the final extraction), they centered on identifying the best (1) solvent system to use during homogenization (2–3 tested per matrix) and (2) single-phase extraction (SPE) column type (3 tested) to use for the final extraction. The best procedure consisted of the following, regardless of sample type: centrifugation speed = 4200 × g; elution volume = 8 mL; elution solvent = 80% methanol; and SPE column type = hydrophilic–lipophilic balance (HLB), with carbon also being satisfactory for fish. For sonication, 2 min, 5 min, and 10 min were optimal for fish, lettuce, and soil matrices, respectively. Using the recommended HLB column, the solvent systems that led to the highest recovery of MCs were methanol:water:butanol for fish, methanol:water for lettuce, and EDTA-Na4P2O7 for soils. Given that the recommended procedures resulted in average MC-LR and MC-RR recoveries that ranged 93 to 98%, their adoption for the preparation of samples with complex matrices before UPLC–MS/MS analysis is encouraged.
Evaluating the portability of satellite derived chlorophyll-a algorithms for temperate inland lakes using airborne hyperspectral imagery and dense surface observations Harmful Algae (IF 4.138) Pub Date : 2018-05-15 Richard Johansen, Richard Beck, Jakub Nowosad, Christopher Nietch, Min Xu, Song Shu, Bo Yang, Hongxing Liu, Erich Emery, Molly Reif, Joseph Harwood, Jade Young, Dana Macke, Mark Martin, Garrett Stillings, Richard Stumpf, Haibin Su
This study evaluated the performances of twenty-nine algorithms that use satellite-based spectral imager data to derive estimates of chlorophyll-a concentrations that, in turn, can be used as an indicator of the general status of algal cell densities and the potential for a harmful algal bloom (HAB). The performance assessment was based on making relative comparisons between two temperate inland lakes: Harsha Lake (7.99 km2) in Southwest Ohio and Taylorsville Lake (11.88 km2) in central Kentucky. Of interest was identifying algorithm-imager combinations that had high correlation with coincident chlorophyll-a surface observations for both lakes, as this suggests portability for regional HAB monitoring. The spectral data utilized to estimate surface water chlorophyll-a concentrations were derived from the airborne Compact Airborne Spectral Imager (CASI) 1500 hyperspectral imager, that was then used to derive synthetic versions of currently operational satellite-based imagers using spatial resampling and spectral binning. The synthetic data mimics the configurations of spectral imagers on current satellites in earth’s orbit including, WorldView-2/3, Sentinel-2, Landsat-8, Moderate-resolution Imaging Spectroradiometer (MODIS), and Medium Resolution Imaging Spectrometer (MERIS). High correlations were found between the direct measurement and the imagery-estimated chlorophyll-a concentrations at both lakes. The results determined that eleven out of the twenty-nine algorithms were considered portable, with r2 values greater than 0.5 for both lakes. Even though the two lakes are different in terms of background water quality, size and shape, with Taylorsville being generally less impaired, larger, but much narrower throughout, the results support the portability of utilizing a suite of certain algorithms across multiple sensors to detect potential algal blooms through the use of chlorophyll-a as a proxy. Furthermore, the strong performance of the Sentinel-2 algorithms is exceptionally promising, due to the recent launch of the second satellite in the constellation, which will provide higher temporal resolution for temperate inland water bodies. Additionally, scripts were written for the open-source statistical software R that automate much of the spectral data processing steps. This allows for the simultaneous consideration of numerous algorithms across multiple imagers over an expedited time frame for the near real-time monitoring required for detecting algal blooms and mitigating their adverse impacts.
Detection of cyanotoxins (microcystins/nodularins) in livers from estuarine and coastal bottlenose dolphins (Tursiops truncatus) from Northeast Florida Harmful Algae (IF 4.138) Pub Date : 2018-06-07 Amber Brown, Amanda Foss, Melissa A. Miller, Quincy Gibson
Microcystins/Nodularins (MCs/NODs) are potent hepatotoxic cyanotoxins produced by harmful algal blooms (HABs) that occur frequently in the upper basin of the St. Johns River (SJR), Jacksonville, FL, USA. Areas downstream of bloom locations provide critical habitat for an estuarine population of bottlenose dolphins (Tursiops truncatus). Since 2010, approximately 30 of these dolphins have stranded and died within this impaired watershed; the cause of death was inconclusive for a majority of these individuals. For the current study, environmental exposure to MCs/NODs was investigated as a potential cause of dolphin mortality. Stranded dolphins from 2013 to 2017 were categorized into estuarine (n = 17) and coastal (n = 10) populations. Because estuarine dolphins inhabit areas with frequent or recurring cyanoblooms, they were considered as a comparatively high-risk group for cyanotoxin exposure in relation to coastal animals. All available liver samples from estuarine dolphins were tested regardless of stranding date, and samples from coastal individuals that stranded outside of the known cyanotoxin bloom season were assessed as controls. The MMPB (2-methyl-3-methoxy-4-phenylbutiric acid) technique was used to determine total (bound and free) concentrations of MCs/NODS in liver tissues. Free MCs/NODs extractions were conducted and analyzed using ELISA and LC–MS/MS on MMPB-positive samples to compare test results. MMPB testing resulted in low-level total MCs/NODs detection in some specimens. The Adda ELISA produced high test values that were not supported by concurrent LC–MS/MS analyses, indicative of false positives. Our results indicate that both estuarine and coastal dolphins are exposed to MCs/NODs, with potential toxic and immune health impacts.
Cyanobacteria and cyanotoxins at the river-estuarine transition Harmful Algae (IF 4.138) Pub Date : 2018-06-07 Paul A. Bukaveckas, Rima Franklin, Spencer Tassone, Brendan Trache, Todd Egerton
We examined seasonal and longitudinal patterns in the occurrence of toxic cyanobacteria in the James River Estuary (Virginia). Highest chlorophyll and cyanobacteria levels were observed in the tidal freshwater segment, particularly during dry summers when freshwater replacement time was long. Cyanobacteria accounted for a small proportion of phytoplankton biomass (7–15%), and Microcystis comprised a small proportion of the cyanobacteria (<1%). Despite this, measureable levels of microcystin were commonly observed in water (>85% of samples in July, August and September), fish tissues (87% of planktivorous fishes) and shellfish (83% of individuals). Generic indicators of algal blooms (chlorophyll and algal biomass) had limited utility for predicting microcystin concentrations. However, chlorophyll was found to be a useful predictor for the probability of exceeding specific toxin thresholds. Tissue microcystin concentrations were highest in fish and shellfish collected from the tidal fresh segment, but were detectable in biota collected from the oligohaline at distances 50 km seaward.
Cyanobacteria breakthrough: Effects of Limnothrix redekei contamination in an artificial bank filtration on a regional water supply Harmful Algae (IF 4.138) Pub Date : 2018-06-07 Adam K. Rose, Larelle Fabbro, Susan Kinnear
Mitigation of cyanobacterial or “blue-green algal” blooms is a challenging task for water managers across Australia. In the present study, a regional drinking water source (located in Central Queensland) was studied to identify the potential risks posed by cyanobacteria. Data were collected from the drinking water source (a lagoon) as well as the drinking water supply infrastructure, at monthly intervals between September 2012 and December 2014. In March 2013 there was an extreme rainfall event where floodwaters infiltrated the water supply without passing through bank filtration. The floodwaters also compromised the bank filtration via erosion. The pump well and bank filtration system were subsequently upgraded/maintained in May 2013. Results showed that following the extreme event and infrastructure upgrade, two distinct Limnothrix redekei blooms microscopically identified, were detected in the drinking water supply chain. Further investigations indicated that the species was also present in the pump well infrastructure, a dark environment, growing on the surface of the newly installed pump well cement pipe. After observing the occurrence and habitat niche of this species during the present study, a suggestion was made to minimise cyanobacterial contamination and proliferation within the water supply chain infrastructure. The preliminary proposal is to use clean sand on the sub-surface layer of the bank filtration, complemented with biologically active sand as a surface cap. Furthermore, the culturing techniques reported in this study can potentially be used to optimize assessment for Limnothrix redekei populations surrounding water extraction points.
Seasonal distribution of Gambierdiscus spp. in Wakasa Bay, the Sea of Japan, and antagonistic relationships with epiphytic pennate diatoms Harmful Algae (IF 4.138) Pub Date : 2018-05-19 Mitsutaka Nakada, Yuki Hatayama, Akira Ishikawa, Tetsuro Ajisaka, Shigeki Sawayama, Ichiro Imai
The occurrence of the ciguatera fish poisoning (CFP) causative Gambierdiscus spp. was confirmed in the Sea of Japan for the first time in 2009. This paper reports seasonal distribution of Gambierdiscus spp. and epiphytic diatoms in the Sea of Japan. Monitoring results suggested an antagonistic interaction in abundances between epiphytic diatoms and the dinoflagellate Gambierdiscus spp. Allelopathic effects of diatoms were considered to be involved in the competitive phenomenon. Therefore it is hypothesized that cell densities of epiphytic pennate diatoms on macroalgae are a novel determinant affecting the abundance of Gambierdiscus spp. other than sea water temperature, salinity and nutrients. Monitorings of the abundance of epiphytic diatoms would lead us to predict the occurrences of Gambierdiscus spp. blooms in the CFP area, and thereby the CFP risk assessments would be developed. Phylogenetic analyses indicated that Gambierdiscus spp. in the Sea of Japan belonged to Gambierdiscus sp. type 2 which was reported to be non-toxic. Nevertheless, based on morphological characteristics, at least two types of Gambierdiscus spp. were found in the Sea of Japan. It is needed to test the toxicity of the both types of Gambierdiscus recognized in the present study for evaluation of the probability of CFP outbreak risks in the Sea of Japan in the future.
Morphological, molecular and toxigenic characteristics of Namibian Pseudo-nitzschia species – including Pseudo-nitzschia bucculenta sp. nov. Harmful Algae (IF 4.138) Pub Date : 2018-05-31 Frederik Frøsig Gai, Cecilie Kirketerp Hedemand, Deon C. Louw, Kolette Grobler, Bernd Krock, Øjvind Moestrup, Nina Lundholm
A field study was undertaken to investigate the occurrence and toxin production of species in the diatom genus Pseudo-nitzschia in Namibian waters, in the extremely productive Benguela upwelling system. From surveys conducted on the R/V Mirabilis and the R/V !Anichab, 52 strains were morphologically determined to species level, supported by nuclear ITS rDNA data. Seven species were identified; P. australis, P. decipiens, P. dolorosa, P. fraudulenta, P. plurisecta, P. pungens var. cingulata, and the new species P. bucculenta F. Gai, C. K. Hedemand, N. Lundholm & Ø. Moestrup sp. nov.Molecular and morphological diversity of the Namibian Pseudo-nitzschia species is discussed. Most importantly, P. bucculenta is both morphologically and phylogenetically most similar to P. dolorosa differing mainly in valve width and densities of striae, poroids and band striae as well as by four hemi-compensatory base changes in the ITS2. Morphological and molecular differences among the strains of P. decipiens suggest a temperate and a warm water subdivision. The geographical and toxigenic characteristics of the identified Pseudo-nitzschia species are described and compared to previous studies. Initial tests of toxin production in all seven species revealed production of domoic acid (DA) in two species: one strain of P. australis (0.074 pg DA cell−1) and two strains of P. plurisecta (0.338 pg DA cell−1 and 0.385 pg DA cell−1).
Chattonella subsalsa (Raphidophyceae) growth and hemolytic activity in response to agriculturally-derived estuarine contaminants Harmful Algae (IF 4.138) Pub Date : 2018-05-28 Stacie L. Flood, JoAnn M. Burkholder
The potential for toxic contaminants and nutrient pollution to alter natural cycles of estuarine phytoplankton blooms is well known, yet few studies have examined how these combined stressors affect harmful algal species. Here, a robust testing protocol was developed to enable an ecotoxicological assessment of responses to commonly co-occurring estuarine contaminants by harmful algal bloom species. The population growth and toxicity (as cell density and hemolytic activity, respectively) of a cultured strain of the toxigenic raphidiophycean, Chattonella subsalsa, were assessed in two experiments (duration 10 days and 28 days) across a gradient of atrazine concentrations and N:P ratios simulating nutrient-rich versus nutrient-depleted regimes. The response of this large-celled, slowly growing alga to atrazine × nutrients depended on growth phase; atrazine was most inhibitory during early exponential population growth (day 10), whereas nutrient regime was a more important influence during later phases of growth (day 28). Without atrazine, toxicity toward fish was highest in low-P cultures. At atrazine levels >25 μg L−1, hemolytic activity was highest in low-N cultures, and increased with increasing atrazine concentration in all nutrient-limited cultures. Hemolytic activity varied inversely with atrazine concentration in N,P-replete conditions. Overall, atrazine inhibitory effects on population growth of this C. subsalsa strain depended on the growth phase and the nutrient regime; hemolytic activity was higher and further enhanced by atrazine in low N-P regimes; and atrazine inhibited hemolytic activity in nutrient-replete conditions. The data suggest that, depending on the growth phase and nutrient regime, atrazine can help promote toxic C. subsalsa blooms.
Significant activities of extracellular enzymes from a brown tide in the coastal waters of Qinhuangdao, China Harmful Algae (IF 4.138) Pub Date : 2018-03-19 Linjian Ou, Xiaohong Liu, Jingjing Li, Xianling Qin, Lei Cui, Songhui Lu
Brown tides of Aureococcus anophagefferens have occurred annually in the coastal waters of Qinhuangdao since 2009. High levels of dissolved organic matter (DOM) are always measured during bloom periods. Study focusing on the effect of DOM on the occurrences of brown tides in this area is scare by far. To analyze the efficiency of DOM hydrolysis by different groups of microorganisms and the possible influence of DOM on the formation of brown tides, extracellular enzymes such as α, β-glucosidases (α, β-GLUs), leucine aminopeptidase (LAP) and alkaline phosphatase (AP) as well as other environmental parameters were analyzed during a pre-bloom period of A. anophagefferens in June 2014. Dissolved organic nitrogen (DON) and phosphorus (DOP) contributed more than half of the total dissolved nutrient pools. Approximately 60–70% of the enzyme activities were associated with phytoplankton of size >5 μm. The hydrolysis rates of LAP were approximately 5 to 20 fold higher than those of AP and α, β-GLUs. The ratios of β-GLU activities: LAP activities indicated the hydrolysis potential related to proteins rather than polysaccharides. The differences in turnover time among the enzymes suggested that DOP was firstly hydrolyzed and recycled in the water in the early minutes, followed by the hydrolysis of DON and dissolved organic carbon (DOC)(in hours). Results suggest that the hydrolysis of DOM, in particular DOP, might significantly contribute to the occurrences of brown tides in the coastal waters of Qinhuangdao, China.
Detection of the suspected neurotoxin β-methylamino-l-alanine (BMAA) in cyanobacterial blooms from multiple water bodies in Eastern Australia Harmful Algae (IF 4.138) Pub Date : 2018-03-27 Brendan J. Main, Lee C. Bowling, Matthew P. Padula, David P. Bishop, Simon M. Mitrovic, Gilles J. Guillemin, Kenneth J. Rodgers
Comparison of loop-mediated isothermal amplification with hyperbranched rolling circle amplification as a simple detection method for Heterosigma akashiwo Harmful Algae (IF 4.138) 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 4.138) 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 4.138) 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 4.138) 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 4.138) 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.
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 4.138) 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.
Interactions between nitrogen form, loading rate, and light intensity on Microcystis and Planktothrix growth and microcystin production Harmful Algae (IF 4.138) Pub Date : 2018-02-08 Justin D. Chaffin, Timothy W. Davis, Derek J. Smith, Mikayla M. Baer, Gregory J. Dick
The toxin-producing, bloom-forming cyanobacterial genera Microcystis and Planktothrix require fixed nitrogen (N), such as nitrate, ammonium, or organic N (e.g., urea) for growth and production of microcystins (MC). Bioavailable N can enter lakes in pulses via tributary discharge and through in-lake recycling, which can maintain low N concentrations. Additionally, light intensity has been suggested to play a role in MC production. This study examined how three forms of N (nitrate, ammonium, and urea) interacted with N loading rate (one large pulse vs. many small pulses) and light intensity to stimulate Microcystis and Planktothrix growth and MC production using nutrient enrichment experiments. Enrichments of nitrate, ammonium, and urea resulted in greater cyanobacterial biovolumes and MC concentrations than phosphorus-only enrichments, and there was no difference between pulse (100 μmol/L) and press treatments (8.3 μmol/L every 4 h). Analysis of mcyD transcripts showed significant up-regulation within 4 h of ammonium and urea enrichment. High light intensities (300 μmol photons/m2/s) with N enrichment resulted in greater cyanobacterial biovolumes and MC concentrations than lower light intensities (30 and 3 μmol photons/m2/s). Overall, the results suggest Microcystis and Planktothrix can use many forms of N and that high light intensities enhance MC production during elevated N concentrations. Moreover, the results here further demonstrate the importance of considering N, as well as P, in management strategies aimed at mitigating cyanobacterial blooms.
Feeding and grazing impact by the bloom-forming euglenophyte Eutreptiella eupharyngea on marine eubacteria and cyanobacteria Harmful Algae (IF 4.138) 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.
Time series models of decadal trends in the harmful algal species Karlodinium veneficum in Chesapeake Bay Harmful Algae (IF 4.138) 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.
Remote quantification of Cochlodinium polykrikoides blooms occurring in the East Sea using geostationary ocean color imager (GOCI) Harmful Algae (IF 4.138) Pub Date : 2018-03-04 Jae Hoon Noh, Wonkook Kim, Seung Hyun Son, Jae-Hyun Ahn, Young-Je Park
Accurate and timely quantification of widespread harmful algal bloom (HAB) distribution is crucial to respond to the natural disaster, minimize the damage, and assess the environmental impact of the event. Although various remote sensing-based quantification approaches have been proposed for HAB since the advent of the ocean color satellite sensor, there have been no algorithms that were validated with in-situ quantitative measurements for the red tide occurring in the Korean seas. Furthermore, since the geostationary ocean color imager (GOCI) became available in June 2010, an algorithm that exploits its unprecedented observation frequency (every hour during the daytime) has been highly demanded to better track the changes in spatial distribution of red tide. This study developed a novel red tide quantification algorithm for GOCI that can estimate hourly chlorophyll-a (Chl a) concentration of Cochlodinium (Margalefidinium) polykrikoides, one of the major red tide species around Korean seas. The developed algorithm has been validated using in-situ Chl a measurements collected from a cruise campaign conducted in August 2013, when a massive C. polykrikoides bloom devastated Korean coasts. The proposed algorithm produced a high correlation (R2 = 0.92) with in-situ Chl a measurements with robust performance also for high Chl a concentration (300 mg/m3) in East Sea areas that typically have a relatively low total suspended particle concentration (<0.5 mg/m3).
Blurred lines: Multiple freshwater and marine algal toxins at the land-sea interface of San Francisco Bay, California Harmful Algae (IF 4.138) Pub Date : 2018-03-10 Melissa B. Peacock, Corinne M. Gibble, David B. Senn, James E. Cloern, Raphael M. Kudela
San Francisco Bay (SFB) is a eutrophic estuary that harbors both freshwater and marine toxigenic organisms that are responsible for harmful algal blooms. While there are few commercial fishery harvests within SFB, recreational and subsistence harvesting for shellfish is common. Coastal shellfish are monitored for domoic acid and paralytic shellfish toxins (PSTs), but within SFB there is no routine monitoring for either toxin. Dinophysis shellfish toxins (DSTs) and freshwater microcystins are also present within SFB, but not routinely monitored. Acute exposure to any of these toxin groups has severe consequences for marine organisms and humans, but chronic exposure to sub-lethal doses, or synergistic effects from multiple toxins, are poorly understood and rarely addressed. This study documents the occurrence of domoic acid and microcystins in SFB from 2011 to 2016, and identifies domoic acid, microcystins, DSTs, and PSTs in marine mussels within SFB in 2012, 2014, and 2015. At least one toxin was detected in 99% of mussel samples, and all four toxin suites were identified in 37% of mussels. The presence of these toxins in marine mussels indicates that wildlife and humans who consume them are exposed to toxins at both sub-lethal and acute levels. As such, there are potential deleterious impacts for marine organisms and humans and these effects are unlikely to be documented. These results demonstrate the need for regular monitoring of marine and freshwater toxins in SFB, and suggest that co-occurrence of multiple toxins is a potential threat in other ecosystems where freshwater and seawater mix.
Population dynamic of bloom-forming Microcystis aeruginosa in the presence of the invasive bivalve Limnoperna fortunei Harmful Algae (IF 4.138) Pub Date : 2018-03-08 Fabiano Alcísio e Silva, Alessandra Giani
Genome variation in nine co-occurring toxic Cylindrospermopsis raciborskii strains Harmful Algae (IF 4.138) Pub Date : 2018-03-21 Anusuya Willis, Jason N. Woodhouse, Sarah E. Ongley, Aaron R. Jex, Michele A. Burford, Brett A. Neilan
Cyanobacteria form harmful algal blooms and are highly adapted to a range of habitats, in part due to their phenotype plasticity. This plasticity is partially the result of co-existence of multiple strains within a single population. The toxic cyanobacterium Cylindrospermopsis raciborskii has remarkable phenotypic plasticity, strain variation and environmental adaptation resulting in an expansion of its global range. To understand the genetic basis of the high level of plasticity within a C. raciborskii population, the genomes of nine co-occurring strains were compared. The strains differed in morphology, toxin cell quotas and physiology, despite being obtained from a single water sample. Comparative genomics showed that three coiled strains were 3.9 Mbp in size, with 3544 ± 11 genes, while straight strains were 3.8 Mbp in size, with 3485 ± 20 genes. The core proteome comprised 86% of the genome and consisted of 2891 orthologous groups (OGs), whereas the variable genome comprised ∼14% (847 OGs), and the strain specific genome only ∼1% (433 OGs).There was a high proportion of variable strain-specific genes for the very closely related strains, which may underpin strain differentiation. The variable genes were associated with environmental responses and adaptation, particularly phage defence, DNA repair, membrane transport, and stress, illustrative of the adaptability of the strains in response to environmental and biological stressors. This study shows that high genomic variability exists between co-occurring strains and may be the basis of strain phenotypic differences and plasticity of populations. Therefore management and prediction of blooms of this harmful species requires different approaches to capture this strain variability.
Realized niche analysis of phytoplankton communities involving HAB: Phaeocystis spp. as a case study Harmful Algae (IF 4.138) 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 4.138) 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.
Molecular detection of harmful cyanobacteria and expression of their toxin genes in Dutch lakes using multi-probe RNA chips Harmful Algae (IF 4.138) 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.
Effects of modified clay used for the control of harmful algal blooms on Alexandrium pacificum cysts Harmful Algae (IF 4.138) Pub Date : 2018-01-08 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.
Advection of Karenia brevis blooms from the Florida Panhandle towards Mississippi coastal waters Harmful Algae (IF 4.138) 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.
Niche separation of Baltic Sea cyanobacteria during bloom events by species interactions and autecological preferences Harmful Algae (IF 4.138) Pub Date : 2018-01-13 Falk Eigemann, Marc Schwartke, Heide Schulz-Vogt
Akinete germination chamber: An experimental device for cyanobacterial akinete germination and plankton emergence Harmful Algae (IF 4.138) 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
Development of a qPCR assay to detect and quantify ichthyotoxic flagellates along the Norwegian coast, and the first Norwegian record of Fibrocapsa japonica (Raphidophyceae) Harmful Algae (IF 4.138) Pub Date : 2018-05-16 Anette Engesmo, David Strand, Sandra Gran-Stadniczeñko, Bente Edvardsen, Linda K. Medlin, Wenche Eikrem
Blooms of ichthyotoxic microalgae pose a great challenge to the aquaculture industry world-wide, and there is a need for fast and specific methods for their detection and quantification in monitoring programs. In this study, quantitative real-time PCR (qPCR) assays for the detection and enumeration of three ichthyotoxic flagellates: the dinoflagellate Karenia mikimotoi (Miyake & Kominami ex Oda) Hansen & Moestrup and the two raphidophytes Heterosigma akashiwo (Hada) Hada ex Hara & Chihara and Fibrocapsa japonica Toriumi & Takano were developed. Further, a previously published qPCR assay for the dinoflagellate Karlodinium veneficum (Ballantine) Larsen was used. Monthly samples collected for three years (Aug 2009–Jun 2012) in outer Oslofjorden, Norway were analysed, and the results compared with light microscopy cell counts. The results indicate a higher sensitivity and a lower detection limit (down to 1 cell L−1) for both qPCR assays. Qualitative and semi-quantitative results were further compared with those obtained by environmental 454 high throughput sequencing (HTS, metabarcoding) and scanning electron microscopy (SEM) examination from the same samplings. All four species were detected by qPCR and HTS and/or SEM in outer Oslofjorden (Aug 2009–Jun 2012); Karlodinium veneficum was present year-round, whereas Karenia mikimotoi, Heterosigma akashiwo and Fibrocapsa japonica appeared mainly during the autumn in all three years. This is the first observation of Fibrocapsa japonica in Norwegian coastal waters. This species has previously been recorded off the Swedish west coast and German Bight, which may suggest a northward dispersal.
Morphology and toxicity of Pseudo-nitzschia species in the northern Benguela Upwelling System Harmful Algae (IF 4.138) Pub Date : 2018-05-03 Deon C. Louw, Gregory J. Doucette, Nina Lundholm
The Benguela upwelling system, considered the world’s most productive marine ecosystem, has a long record of potentially toxic diatoms belonging to the genus Pseudo-nitzschia. Species of Pseudo-nitzschia were reported as early as 1936 from the northern Benguela upwelling system (nBUS). For the current study, long-term phytoplankton monitoring data (2004–2011) for the Namibian coast were analysed to examine inshore and offshore temporal distribution of Pseudo-nitzschia species, their diversity and ultrastructure. The potentially toxigenic P. pungens and P. australis were the dominant inshore species, whereas offshore Pseudo-nitzschia showed a higher diversity that also included potentially toxic species. During a warming event, a community shift from P. pungens and P. australis dominance to P. fraudulenta and P. multiseries was documented in the central nBUS. A case study of a toxic event (August 2004) revealed that P. australis and P. pungens were present at multiple inshore and offshore stations, coincident with fish (pilchard) and bird mortalities reported from the central part of Namibia. Toxin analyses (LC–MS/MS) of samples collected from June to August 2004 revealed the presence of particulate domoic acid (DA) in seawater at multiple stations (maximum ∼180 ng DA/L) in the >0.45 μm size-fraction, as well as detectable DA (0.12 μg DA/g) in the gut of one of two pilchard samples tested. These findings indicate that DA may have been associated with the fish and bird mortalities reported from this event in the nBUS. However, the co-occurrence of very high biomass phytoplankton blooms suggests that other explanations may be possible.
Exploring dinoflagellate biology with high-throughput proteomics Harmful Algae (IF 4.138) Pub Date : 2018-04-16 David Morse, Sirius P.K Tse, Samuel C.L. Lo
Dinoflagellates are notorious for their ability to form the harmful algal blooms known as “red tides,” yet the mechanisms underlying bloom formation remain poorly understood. Despite recent advances in nucleic acid sequencing, which have generated transcriptomes from a wide range of species exposed to a variety of different conditions, measuring changes in RNA levels have not generally produced great insight into dinoflagellate cell biology or environmental physiology, nor do we have a thorough grasp on the molecular events underpinning bloom formation. Not only is the transcriptomic response of dinoflagellates to environmental change generally muted, but there is a markedly low degree of congruency between mRNA expression and protein expression in dinoflagellates. Herein we discuss the application of high-throughput proteomics to the study of dinoflagellate biology. By profiling the cellular protein complement (the proteome) instead of mRNA (the transcriptome), the biomolecular events that underlie the changes of phenotypes can be more readily evaluated, as proteins directly determine the structure and the function of the cell. Recent advances in proteomics have seen this technique become a high-throughput method that is now able to provide a perspective different from the more commonly employed nucleic acid sequencing. We suggest that the time is ripe to exploit these new technologies in addressing the many mysteries of dinoflagellate biology, such as how the symbiotic dinoflagellate inhabiting reef corals acclimate to increases in temperature, as well as how harmful algal blooms are initiated at the sub-cellular level. Furthermore, as dinoflagellates are not the only eukaryotes that demonstrate muted transcriptional responses, the techniques addressed within this review are amenable to a wide array of organisms.
Circadian and irradiance effects on expression of antenna protein genes and pigment contents in dinoflagellate Prorocentrum donghaiense (Dinophycae) Harmful Algae (IF 4.138) Pub Date : 2018-04-16 Xinguo Shi, Ling Li, Senjie Lin
PCP and acpPC are the two major antennae proteins that bind pigments in peridinin-containing dinoflagellates. The relationship between antennae proteins and cellular pigments at molecular level is still poorly understood. Here we identified and characterized the two antennae protein genes in dinoflagellate Prorocentrum donghaiense under different light conditions. The mature PCP protein was 32 kDa, while acpPC was a polyprotein each of 19 kDa. Both genes showed higher expression under low light than under high light, suggesting their possible role in a low light adaptation mechanism. The two genes showed differential diel expression rhythm, with PCP being more highly expressed in the dark than in the light period and acpPC the other way around. HPLC analysis of cellular pigments indicated a diel change of chlorophyll c2, but invariability of other pigments. A stable peridinin: chlorophyll a pigment ratio was detected under different light intensities and over the diel cycle, although the diadinoxanthin:chlorophyll a ratio increased significantly with light intensity. The results suggest that 1) PCP and acpPC genes are functionally distinct, 2) PCP and acpPC can function under low light as an adaptive mechanism in P. donghaiense, 3). the ratios of diadinoxanthin:chlorophyll a and peridinin: chlorophyll a can potentially be used as an indicator of algal photophysiological status and a pigment signature respectively under different light conditions in P. donghaiense.
Allelopathic interactions between the benthic toxic dinoflagellate Ostreopsis cf. ovata and a co-occurring diatom Harmful Algae (IF 4.138) Pub Date : 2018-04-16 Eva Ternon, Anne-Sophie Pavaux, Sophie Marro, Olivier P. Thomas, Rodolphe Lemée
For decades the microphytobenthos assemblage in the coastal Mediterranean Sea has been regularly colonized by the toxic benthic dinoflagellate Ostreopsis cf. ovata. This harmful algal species is a toxin producer and occupies the same ecological niche as various diatoms. Surprisingly, there are only few insights reported on the physiological responses of diatoms to blooms of O. cf. ovata The chemical interactions of O. cf. ovata with the co-occurring diatom Licmophora paradoxa was studied using a bioassay (measuring impact of cell-free culture filtrate) and a co-culture approach (separate by a membrane) to investigate the effects of the exometabolome and its mode of action. Bioassays highlighted a toxic effect of the exometabolome of O. cf. ovata on the diatom photosynthetic activity. However, the co-cultures revealed that these toxic effects do not occur through remote allelopathy. Contact or close interactions between cells of the two species is most likely needed to impair the diatom growth. Ovatoxins are suspected to be the toxic metabolites secreted by O. cf. ovata although the current set of data did not give confirmation of this assumption. Interestingly, the exometabolome of L. paradoxa impaired the growth and the photochemistry of O. cf. ovata in both bioassays and co-cultures. Some biomarkers possibly involved for the effect were identified using a metabolomic approach and may correspond to oxylipins, however a bacterial source of the bioactive metabolites is also considered.
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