Dredging mitigates cyanobacterial bloom in eutrophic Lake Nanhu: Shifts in associations between the bacterioplankton community and sediment biogeochemistry
Introduction
Bacterioplankton and phytoplankton are significant and integral components of aquatic microbial food webs by means of carbon source delivery and play critical roles in nutrient (e.g., carbon, nitrogen, and phosphorus sources) biogeochemical cycles (Liu et al., 2015; Isabwe et al., 2018). However, high abundances of bacterioplankton and phytoplankton can lead to algal blooms, which have become increasingly serious environmental problems as a consequence of water eutrophication and climate change (Chen et al., 2016; Te et al., 2017; Feuchtmayr et al., 2019). In freshwater ecosystems, phytoplankton blooms, also known as algal blooms, are dominated by cyanobacteria (which are regarded as one of the most important bacterioplankton types) (Te et al., 2017; Yan et al., 2017; Li et al., 2018; Zhu et al., 2019), and can dramatically alter ambient biogeochemical factors, such as oxygen exhaustion and water opacity (Chen et al., 2016). Cyanobacterial blooms are often closely correlated with other bacterioplankton (Chen et al., 2016; Su et al., 2017; Te et al., 2017), and cyanobacteria could release secondary metabolites (e.g., microcystin, anatoxin-a, and nodularin) into the water (Lezcano et al., 2017; Te et al., 2017; Omidi et al., 2019), which poisons aquatic organisms and threatens the safety of drinking water.
The excess internal and external inputs of phosphorus (P) and nitrogen (N) into water bodies are the main cause of cyanobacterial blooms (Davis et al., 2015; Li et al., 2019). Simultaneous N and P decreases or elimination are significant for bloom control due to N and P co-limitation of primary productivity that have been demonstrated to be a potential key process in freshwater environments (Paerl and Otten, 2016; Wang et al., 2018). A mainstream perspective is that controlling P concentrations in freshwater can successfully curb lake or reservoir eutrophication (Schindler et al., 2016). While water eutrophication cannot be restrained by decreasing N inputs since N2 fixation can offset N losses (Schindler et al., 2008; Wang et al., 2018). However, this view has been challenged and demonstrated to be incorrect for some eutrophic waters where N could also be significant factor for the control of water eutrophication (Paerl et al., 2010; Horst et al., 2014; Li et al., 2018). Controlling N and P inputs into freshwater is still an effective way to mitigate cyanobacterial blooms.
N and P concentrations, especially P, present periodic changes in freshwater ecosystems (Jing et al., 2015; Chen et al., 2019; Wang et al., 2019a). The external inputs of N and P can be controlled by limiting discharges of untreated sewage water. The internal inputs of N and P can be controlled by using dredging (Jing et al., 2015). Removal of sediments, also known as dredging, has been widely acknowledged as an effective measure for controlling cyanobacterial blooms (Lürling and Faassen, 2012; Jing et al., 2015; Bormans et al., 2016; Liu et al., 2016). Such large-scale anthropogenic disturbances ultimately profoundly improve water quality to decrease water turbidity, nutrients (e.g., C, N, and P sources), toxins, and heavy metal in both water and sediment (Jing et al., 2015; Ragnarsson et al., 2015; Oldenborg and Steinman, 2019). Previous researches have reported that dredging can significantly affect the composition of the sediment microbial community (Edlund and Jansson, 2006; Chiellini et al., 2013; Zhang et al., 2017), and thus could affect nutrient transfer from sediment to water. However, the mechanism of cyanobacterial blooms mitigation by dredging is not well clarified. In eutrophic water remediation by dredging, shifts in interconnection between the bacterioplankton community and sediment biogeochemistry have rarely been investigated.
Based on the development of high-throughput sequencing and bioinformatics, knowledge of the composition and diversity of microbial communities in bloom-influenced water bodies is gradually expanding. However, these studies mainly report the effects of nutrient changes only on the diversity and composition of microbial communities. Few relevant studies have focused on the function and interaction of the bacterioplankton community in freshwater ecosystems with cyanobacterial blooms. In this study, we aimed to explore the mechanisms of how dredging could mitigate cyanobacterial blooms. We hypothesize that 1) dredging can significantly change water physicochemical properties and sediment biogeochemistry; 2) dredging can clearly decrease the abundance of bacterioplankton and cyanobacteria as well as the algae content; 3) dredging can significantly alter the diversity, composition, function, and interaction of bacterioplankton communities.
Section snippets
Site description and sampling
Lake Nanhu in Wuhan, China (30°30′N, 114°21′E), is a shallow, eutrophic freshwater lake with an average depth of 1.2 m and a total surface area of 7.64 km2. Lake Nanhu is located near a university town and provides recreation and rainwater control, however, Lake Nanhu has experienced increasingly serious eutrophication due to heavy discharges of municipal wastewater and intensive aquaculture since the 1980s. Cyanobacterial blooms in Lake Nanhu begin at every April, gradually trends to be stable
Water and sediment physicochemical properties, total bacterioplankton and cyanobacteria abundance
The water temperature (20.87–25.23 °C); pH (7.11–7.90); DO (1.34–10.93 mg/L); turbidity (6.05–24.99 FTU); and nutrients including PO43--P (0.30–3.78 mg/L), NO2−-N (0.11–0.85 mg/L), NO3−-N (12.92–45.71 mg/L), and NH4+-N (0.92–9.54 mg/L) fluctuated for different sites and periods (Table S4). Similarly, the sediment physicochemical parameters, including IP (0.49–4.83 mg/g), OP (0.11–2.74 mg/g), NAIP (0.59–3.59 mg/g), AP (0.17–3.76 mg/g), TP (2.08–6.99 mg/g), Olsen P (0.02–0.78 mg/g), TC
Responses of water and sediment biogeochemistry to dredging
Dredging is an effective approach for mitigating cyanobacterial blooms by changing the water and sediment biogeochemistry (Zhang et al., 2017; Hernández-del Amo et al., 2019). Owing to strict policy of environmental protection, no great amounts of P and N were discharged into Lake Nanhu after implementing dredging project (unpublished data), suggesting only slight inputs of external N and P. The water physicochemical parameters of nutrients and turbidity significantly decreased, and the DO
Conclusions
The Lake Nanhu freshwater ecosystem was largely dominated by the cyanobacteria Candidatus sp., together with Synechococcus, Cylindrospermosis, Planktothrix, and Limnothrix. We found significant changes in the water physicochemical characteristics; the bacterioplankton community, including diversity, composition, interaction, and function; the sediment biogeochemistry, including physicochemical properties, C-, N-, P-, and S-cycling-related enzyme activity; N- and P-cycling-related gene
Credit author statement
Donglan He, Guojun Cheng and Wenjie Wan designed the whole experiment. Wenjie, Wan, Yunan Zhang, Xiaohua Li, and Yin Qin collected experimental samples and conducted all experiments. Wenjie Wan analyzed the data and wrote the manuscript. Wenjie Wan, Guojun Cheng, Xiaohua Li, and Donglan He revised the manuscript, and Donglan He submitted the manuscript.
Declaration of competing interest
The Authors declare no competing financial interest.
Acknowledgements
This work was supported by grants from the National Natural Science Foundation of China (grant number 31070087) and the Fundamental Research Funds for the Central Universities (grant number 2662015PY016 and 2662015PY116).
References (77)
- et al.
In situ, high-resolution evidence of phosphorus release from sediments controlled by the reductive dissolution of iron-bound phosphorus in a deep reservoir, southwestern China
Sci. Total Environ.
(2019) - et al.
Successional trajectories of bacterioplankton community over the complete cycle of a sudden phytoplankton bloom in the Xiangshan, Bay, East China Sea
Environ. Pollut.
(2016) - et al.
Temporal characterization of bacterial communities in a phytoremediation pilot plant aimed at decontamination polluted sediments dredged from Leghorn harbor
Italy. New Biotechnol.
(2013) - et al.
Mediation of functional gene and bacterial community profiles in the sediments of eutrophic Chaohu Lake by total nitrogen and season
Environ. Pollut.
(2019) - et al.
Effects of brownification and warming on algal blooms, metabolism and higher trophic levels in productive shallow lake mesocosms
Sci. Total Environ.
(2019) - et al.
Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa
Water Res.
(2014) - et al.
Community assembly processes underlying phytoplankton and bacterioplankton across a hydrological change in human-impacted river
Sci. Total Environ.
(2018) - et al.
Effects of sediment dredging on internal phosphorus: a comparative field study focused on iron and phosphorus forms in sediments
Ecol. Eng.
(2015) - et al.
Dredging project caused short-term positive effects on lake ecosystem health: a five-year follow-up study at the integrated lake ecosystem level
Sci. Total Environ.
(2019) - et al.
Diversity and temporal shifts of the bacterial community associated with a toxic cyanobacterial bloom: an interplay between microcystin producers and degraders
Water Res.
(2017)
Seasonal function succession and biogeographic zonation of assimilatory and dissimilatory nitrate-reducing bacterioplankton
Sci. Total Environ.
Phylogenetic shifts of bacterioplankton community composition along the Pearl Estuary: the potential impact of hypoxia and nutrients
Front. Microbiol.
Fifteen-year study of environmental dredging effect on variation of nitrogen and phosphorus exchange across the sediment-water interface of an urban lake
Environ. Pollut.
Periphytic biofilm: a buffer for phosphorus precipitation and release between sediments and water
Chemosphere
Controlling toxic cyanobacteria: effects of dredging and phosphorus-binding clay on cyanobacteria and microcystins
Water Res.
Changes in phosphorus removing performance and bacterial community structure in an enanced biological phosphorus removal reactor
Water Res.
Impact of sediment dredging on sediment phosphorus flux in a restored riparian wetland
Sci. Total Environ.
Short and long-term effects of hydraulic dredging on benthic communities and ocean quahog (Arctica islandica) populations
Mar. Environ. Res.
Evaluation and application of molecular denitrification monitoring methods in the northern Lake Tai, China
Sci. Total Environ.
Temporal patterns of phyto- and bacterioplankton and their relationships with environmental factors in Lake Taihu, China
Chemosphere
Decomposition of cyanobacterial bloom contributes to the formation and distribution of iron-bound phosphorus (Fe-P): insight for cycling mechanism of internal phosphorus loading
Sci. Total Environ.
Nitrate addition promotes the nitrogen cycling processes under the co-contaminated tetrabromo bisphenol A and copper condition in river sediment
Environ. Pollut.
Low flows and downstream decline in phytoplankton contribute to impaired water quality in the lower Minnesota River
Water Res.
Occurrence of anammox on suspended sediment (SPS) in oxic river water: effect of the SPS particle size
Chemosphere
Performance of physical and chemical methods in the co-reduction of internal phosphorus and nitrogen loading from the sediment of a black odorous river
Sci. Total Environ.
Successful control of phosphorus release from sediments using oxygen nano-bubble-modified minerals
Sci. Total Environ.
Seasonal succession and spatial distribution of bacterial community structure in a eutrophic freshwater Lake, Lake Taihu
Sci. Total Environ.
A new method for non-parametric multivariate analysis of variance
Austral Ecol.
High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms
ISME J.
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
Nat. Biotechnol.
Controlling internal phosphorus loading in lakes by physical methods to reduce cyanobacterial blooms: a review
Aquat. Ecol.
Oxygenation of hypoxic coastal Baltic Sea sediments impacts on chemistry, microbial community composition, and metabolism
Front. Microbiol.
PhnW-PhnX pathway in dinoflagellates not functional to utilize extracellular phosphonates
Front. Mar. Sci.
Prediction and tests of climate-based hypotheses of broad-scale variation in taxonomic richness
Ecol. Lett.
Effects of increasing nitrogen and phosphorus concentrations on phytoplankton community growth and toxicity during planktothrix blooms in Sandusky Bay, Lake Erie
Environ. Sci. Technol.
Widespread nitrogen fixation in sediments from diverse deep-sea sites of elevated carbon loading
Environ. Microbiol.
Changes in active bacterial communities before and after dredging of highly polluted Baltic Sea sediments
Appl. Environ. Microbiol.
Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes
Environ. Microbiol.
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