Abstract
To explore how decomposed Microcystis-dominant cyanobacterial blooms affect submerged macrophytes, the submerged plant Myriophyllum spicatum was exposed to cell extracts from microcystin (MC)- and non-MC-producing Microcystis strains in a laboratory experiment. Results showed that both Microcystis cell extracts exerted obvious damages to plant biomass, photosynthesis, primary and secondary metabolism measures, and resistance of plant antioxidant systems, with MC-producing Microcystis having stronger effects due to the presence of MCs. Cyanotoxins other than MCs responsible for the negative effects from both Microcystis strains needs further identification. The Shannon diversity and Chao1 indices of epiphytic and planktonic bacteria were decreased by the cell extracts from both Microcystis strains. However, epiphytic and planktonic bacterial communities responded differently to Microcystis cell extracts at the genus level. The dominant genera of planktonic bacteria including Enterobacter, Pseudomonas, and Novosphingobium from phylum Proteobacteria, Chryseobacterium from phylum Bacteroidetes, and Microbacterium from Actinobacteriota in the treatments with cell extracts were previously reported to have strains with algicidal and MC-degrading capabilities. Bacterial genes associated with energy production and conversion, amino acid transport and metabolism, and inorganic ion transport and metabolism, were more abundant in both treatments than the control for planktonic bacteria, but less abundant for epiphytic bacteria. We speculate that planktonic bacterial communities have the potential to use and degrade substances derived from Microcystis cell extracts, which may be beneficial for M. spicatum to alleviate damages from Microcystis. Further research is needed to verify the structure and function dynamics of epiphytic and planktonic bacteria in the interaction between cyanobacteria and submerged macrophytes.
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Data Availability Statement
All datasets generated and/or analyzed during this study are available from the corresponding author on reasonable request.
References
Amorim C A, Ulisses C, Moura A N. 2017. Biometric and physiological responses of Egeria densa Planch. cultivated with toxic and non-toxic strains of Microcystis. Aquatic Toxicology, 191: 201–208, https://doi.org/10.1016/j.aquatox.2017.08.012.
Bai G L, Zhang Y, Yan P et al. 2020. Spatial and seasonal variation of water parameters, sediment properties, and submerged macrophytes after ecological restoration in a long-term (6 year) study in Hangzhou West Lake in China: submerged macrophyte distribution influenced by environmental variables. Water Research, 186: 116379, https://doi.org/10.1016/j.watres.2020.116379.
Bates D, Maechler M, Bolker B et al. 2012. Lme4: Linear mixed-effects models using S4 classes. R Package Version: 0.999999-2. R Foundation for Statistical Computing, Vienna. http://cran.r-project.org/web/packages/lme4/lme4.pdf.
Berg K A, Lyra C, Sivonen K et al. 2009. High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. The ISME Journal, 3 (3): 314–325, https://doi.org/10.1038/ismej.2008.110.
Bormans M, Savar V, Legrand B et al. 2020. Cyanobacteria and cyanotoxins in estuarine water and sediment. Aquatic Ecology, 54 (2), 625–640, https://doi.org/10.1007/s10452-020-09764-y.
Briand E, Bormans M, Gugger M et al. 2016. Changes in secondary metabolic profiles of Microcystis aeruginosa strains in response to intraspecific interactions. Environmental Microbiology, 18 (2): 384–400, https://doi.org/10.1111/1462-2920.12904.
Burford M A, Carey C C, Hamilton D P et al. 2020. Perspective: advancing the research agenda for improving understanding of cyanobacteria in a future of global change. Harmful Algae, 91: 101601, https://doi.org/10.1016/j.hal.2019.04.004.
Burke C, Thomas T, Lewis M et al. 2011. Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. The ISME Journal, 5 (4): 590–600, https://doi.org/10.1038/ismej.2010.164.
Chen C Y, Pan G, Shi W Q et al. 2018. Clay flocculation effect on microbial community composition in water and sediment. Frontiers in Environmental Science, 6: 60, https://doi.org/10.3389/fenvs.2018.00060.
Dai R H, Liu H J, Qu J H et al. 2009. Effects of amino acids on microcystin production of the Microcystis aeruginosa. Journal of Hazardous Materials, 161(2-3): 730–736, https://doi.org/10.1016/j.jhazmat.2008.04.015.
Dziga D, Wasylewski M, Wladyka B et al. 2013. Microbial degradation of microcystins. Chemical Research in Toxicology, 26(6): 841–852, https://doi.org/10.1021/tx4000045.
Fadrosh D W, Ma B, Gajer P et al. 2014. An improved dualindexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome, 2(1): 6, https://doi.org/10.1186/2049-2618-2-6.
Fan Z, Han R M, Ma J et al. 2016. Submerged macrophytes shape the abundance and diversity of bacterial denitrifiers in bacterioplankton and epiphyton in the Shallow Fresh Lake Taihu, China. Environmental Science and Pollution Research, 23(14): 14102–14114, https://doi.org/10.1007/s11356-016-6390-1.
Finkler Ferreira T, Crossetti L O, Motta Marques D M L et al. 2018. The structuring role of submerged macrophytes in a large subtropical shallow lake: clear effects on water chemistry and phytoplankton structure community along a vegetated-pelagic gradient. Limnologica, 69: 142–154, https://doi.org/10.1016/j.limno.2017.12.003.
Gao Y N, Dong J, Fu Q Q et al. 2017. Allelopathic effects of submerged macrophytes on phytoplankton. Allelopathy Journal, 40(1): 1–22, https://doi.org/10.26651/2017-40-1-1062.
Gong L X, Zhang S H, Chen D Q et al. 2018. Response of biofilms-leaves of two submerged macrophytes to high ammonium. Chemosphere, 192: 152–160, https://doi.org/10.1016/j.chemosphere.2017.09.147.
Guo X L, Liu X L, Pan J L et al. 2015. Synergistic algicidal effect and mechanism of two diketopiperazines produced by Chryseobacterium sp. strain GLY-1106 on the harmful bloom-forming Microcystis aeruginosa. Scientific Reports 5: 1–12, https://doi.org/10.1038/srep14720.
Harke M J, Steffen M M, Gobler C J et al. 2016. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae, 54: 4–20, https://doi.org/10.1016/j.hal.2015.12.007.
He D, Ren L J, Wu Q L. 2014. Contrasting diversity of epibiotic bacteria and surrounding bacterioplankton of a common submerged macrophyte, Potamogeton crispus, in freshwater lakes. FEMS Microbiology Ecology, 90 (3): 551–562, https://doi.org/10.1111/1574-6941.12414.
Hempel M, Blume M, Blindow I et al. 2008. Epiphytic bacterial community composition on two common submerged macrophytes in brackish water and freshwater. B MC Microbiology, 8: 58, https://doi.org/10.1186/1471-2180-8-58.
Hilt S, Ghobrial M G N, Gross E M. 2006. In situ allelopathic potential of Myriophyllum verticillatum (Haloragaceae) against selected phytoplankton species. Journal of Phycology 42 (6): 1189–1198, https://doi.org/10.1111/j.1529-8817.2006.00286.x.
Hilt S, Gross E M. 2008. Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes?. Basic and Applied Ecology, 9(4): 422–432, https://doi.org/10.1016/j.baae.2007.04.003.
Hoke A K, Reynoso G, Smith M R et al. 2021. Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere. PLoS One, 16(9): e0257017, https://doi.org/10.1371/journal.pone.0257017.
Janssen E M L. 2019. Cyanobacterial peptides beyond microcystins - a review on co-occurrence, toxicity, and challenges for risk assessment. Water Research, 151: 488–499, https://doi.org/10.1016/j.watres.2018.12.048.
Jiang J L, Gu X Y, Song R et al. 2011. Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara. Journal of Hazardous Materials, 190(1-3): 188–196, https://doi.org/10.1016/j.jhazmat.2011.03.023.
Jiang M Q, Zhou Y P, Ji X Y et al. 2019a. Responses of leaf-associated biofilms on the submerged macrophyte Vallisneria natans during harmful algal blooms. Environmental Pollution, 246: 819–826, https://doi.org/10.1016/j.envpol.2018.12.081.
Jiang M Q, Zhou Y P, Wang N et al. 2019b. Allelopathic effects of harmful algal extracts and exudates on biofilms on leaves of Vallisneria natans. Science of the Total Environment, 655: 823–830, https://doi.org/10.1016/j.scitotenv.2018.11.296.
Kumar P, Hegde K, Brar S K et al. 2018. Biodegradation of microcystin-LR using acclimatized bacteria isolated from different units of the drinking water treatment plant. Environmental Pollution, 242: 407–416, https://doi.org/10.1016/j.envpol.2018.07.008.
Le Manach S, Khenfech N, Huet H et al. 2016. Genderspecific toxicological effects of chronic exposure to pure microcystin-LR or complex Microcystis aeruginosa extracts on adult Medaka fish. Environmental Science & Technology, 50(15): 8324–8334, https://doi.org/10.1021/acs.est.6b01903.
Levén L, Eriksson A R B, Schnürer A. 2007. Effect of process temperature on bacterial and archaeal communities in two methanogenic bioreactors treating organic household waste. FEMS Microbiology Ecology, 59(3): 683–693, https://doi.org/10.1111/j.1574-6941.2006.00263.x.
Lezcano M Á, Velázquez D, Quesada A et al. 2017. Diversity and temporal shifts of the bacterial community associated with a toxic cyanobacterial bloom: an interplay between microcystin producers and degraders. Water Research, 125: 52–61, https://doi.org/10.1016/j.watres.2017.08.025.
Li J M, Li J, Shi G et al. 2016. Discerning biodegradation and adsorption of microcystin-LR in a shallow semienclosed bay and bacterial community shifts in response to associated process. Ecotoxicology and Environmental Safety, 132: 123–131, https://doi.org/10.1016/j.ecoenv.2016.05.033.
Li Q, Gu P, Zhang C et al. 2020a. Combined toxic effects of anatoxin-a and microcystin-LR on submerged macrophytes and biofilms. Journal of Hazardous Materials, 389: 122053, https://doi.org/10.1016/j.jhazmat.2020.122053.
Li Q, Gu P, Zhang H et al. 2020b. Response of submerged macrophytes and leaf biofilms to the decline phase of Microcystis aeruginosa: antioxidant response, ultrastructure, microbial properties, and potential mechanism. Science of the Total Environment, 699: 134325, https://doi.org/10.1016/j.scitotenv.2019.134325.
Li Y M, Wang J, Zhang A et al. 2015. Enhancing the quantity and quality of short-chain fatty acids production from waste activated sludge using CaO2 as an additive. Water Research, 83: 84–93, https://doi.org/10.1016/j.watres.2015.06.021.
Liu L M, Yang J, Yu Z et al. 2015. The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. The ISME Journa l, 9(9): 2068–2077, https://doi.org/10.1038/ismej.2015.29.
Liu Q, Liu M M, Zhang Q et al. 2019. Epiphytic bacterial community composition on the surface of the submerged macrophyte Myriophyllum spicatum in a low-salinity sea area of Hangzhou Bay. Oceanological and Hydrobiological Studies, 48(1): 43–55, https://doi.org/10.1515/ohs-2019-0005.
Liu Q, Sun B, Huo Y Z et al. 2018. Nutrient bioextraction and microalgae growth inhibition using submerged macrophyte Myriophyllum spicatum in a low salinity area of East China Sea. Marine Pollution Bulletin, 127: 67–72, https://doi.org/10.1016/j.marpolbul.2017.11.031.
Liu Y, Chen Y X, Fang H Y et al. 2021. Relationship between morphospecies and microcystin-producing genotypes of Microcystis species in Chinese freshwaters. Journal of Oceanology and Limnology, 39(5): 1926–1937, https://doi.org/10.1007/s00343-020-0276-2.
Liu Y, Xu Y, Wang Z J et al. 2016. Dominance and succession of Microcystis genotypes and morphotypes in Lake Taihu, a large and shallow freshwater lake in China. Environmental Pollution, 219: 399–408, https://doi.org/10.1016/j.envpol.2016.05.021.
Niu Y, Shen H, Chen J et al. 2011. Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Research, 45(14): 4169–4182, https://doi.org/10.1016/j.watres.2011.05.022.
Perrin Y, Bouchon D, Delafont V et al. 2019. Microbiome of drinking water: a full-scale spatio-temporal study to monitor water quality in the Paris distribution system. Water Research, 149: 375–385, https://doi.org/10.1016/j.watres.2018.11.013.
Pflugmacher S. 2002. Possible allelopathic effects of cyanotoxins, with reference to microcystin-LR, in aquatic ecosystems. Environmental Toxicology, 17(4): 407–413, https://doi.org/10.1002/tox.10071.
Pivokonsky M, Safarikova J, Baresova M et al. 2014. A comparison of the character of algal extracellular versus cellular organic matter produced by cyanobacterium, diatom and green alga. Water Research, 51: 37–46, https://doi.org/10.1016/j.watres.2013.12.022.
Plaas H E, Paerl H W. 2021. Toxic cyanobacteria: a growing threat to water and air quality. Environmental Science & Technology, 55(1): 44–64, https://doi.org/10.1021/acs.est.0c06653.
R Development Core Team. 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.Rproject.org/.
Rastogi R P, Sinha R P, Incharoensakdi A. 2014. The cyanotoxin-microcystins: current overview. Reviews in Environmental Science and Bio / Technology, 13(2): 215–249, https://doi.org/10.1007/s11157-014-9334-6.
Rolland D C, Haury J, Marmonier P et al. 2015. Effect of macrophytes on flow conditions and deposition of suspended particles in small streams: an experimental study using artificial vegetation. Revue des Sciences de L'Eau, 28(3): 231–245, https://doi.org/10.7202/1034012ar.
Shi L M, Huang Y X, Zhang M et al. 2017. Bacterial community dynamics and functional variation during the long-term decomposition of cyanobacterial blooms in-vitro. Science of the Total Environment, 598: 77–86, https://doi.org/10.1016/j.scitotenv.2017.04.115.
Sidelev S, Zubishina A, Chernova E. 2020. Distribution of microcystin-producing genes in Microcystis colonies from some Russian freshwaters: is there any correlation with morphospecies and colony size? Toxicon, 184: 136–142, https://doi.org/10.1016/j.toxicon.2020.06.005.
Smutná M, Babica P, Jarque S et al. 2014 Acute, chronic and reproductive toxicity of complex cyanobacterial blooms in Daphnia magna and the role of microcystins. Toxicon., 79: 11–18, https://doi.org/10.1016/j.toxicon.2013.12.009.
Steiner K, Wood S A, Puddick J et al. 2017. A comparison of bacterial community structure, activity and microcystins associated with formation and breakdown of a cyanobacterial scum. Aquatic Microbial Ecology, 80(3): 243–256, https://doi.org/10.3354/ame01852.
Stüven J, Pflugmacher S. 2007. Antioxidative stress response of Lepidium sativum due to exposure to cyanobacterial secondary metabolites. Toxicon, 50(1): 85–93, https://doi.org/10.1016/j.toxicon.2007.02.019.
Švanys A, Paškauskas R, Hilt S. 2014. Effects of the allelopathically active macrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study. Hydrobiologia, 737(1): 57–66, https://doi.org/10.1007/s10750-013-1782-4.
Svircev Z, Drobac D, Tokodi N et al. 2017. Toxicology of microcystins with reference to cases of human intoxications and epidemiological investigations of exposures to cyanobacteria and cyanotoxins. Archives of Toxicology, 91(2): 621–650, https://doi.org/10.1007/s00204-016-1921-6.
Teeling H, Fuchs B M, Becher D et al. 2012. Substratecontrolled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science, 336(6081): 608–611, https://doi.org/10.1126/science.1218344.
Villacorte L O, Ekowati Y, Neu T R et al. 2015. Characterisation of algal organic matter produced by bloom-forming marine and freshwater algae. Water Research, 73: 216–230, https://doi.org/10.1016/j.watres.2015.01.028.
Wang H J, Xu C, Liu Y et al. 2021. From unusual suspect to serial killer: cyanotoxins boosted by climate change may jeopardize megafauna. The Innovation, 2 (2): 100092, https://doi.org/10.1016/j.xinn.2021.100092.
Wang J P, Wang C, Li J H et al. 2018. Comparative genomics of degradative Novosphingobium strains with special reference to microcystin-degrading Novosphingobium sp. THN1. Frontiers in Microbiology, 9: 2238, https://doi.org/10.3389/fmicb.2018.02238.
Wang Y J, Cao X Y, Zeng J et al. 2020. Distinct shifts in bacterioplankton community composition and functional gene structure between macrophyte- and phytoplanktondominated regimes in a large shallow lake. Limnology and Oceanography, 65(S1): S208–S219 https://doi.org/10.1002/lno.11373.
Wijewardene L, Wu N C, Fohrer N et al. 2022. Epiphytic biofilms in freshwater and interactions with macrophytes: current understanding and future directions. Aquatic Botany, 176: 103467, https://doi.org/10.1016/j.aquabot.2021.103467.
Wood K A, O'Hare M T, McDonald C et al. 2017. Herbivore regulation of plant abundance in aquatic ecosystems. Biologica l Reviews, 92(2): 1128–1141, https://doi.org/10.1111/brv.12272.
Wu A P, Cao T, Wu S K et al. 2009. Trends of superoxide dismutase and soluble protein of aquatic plants in lakes of different trophic levels in the middle and lower reaches of the Yangtze River, China. Journal of Integrative Plant Biology, 51(4): 414–422, https://doi.org/10.1111/j.1744-7909.2009.00814.x.
Wu Q L, Zwart G, Wu J F et al. 2007. Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China. Environmental Microbiology, 9(11): 2765–2774, https://doi.org/10.1111/j.1462-2920.2007.01388.x.
Wu Y L, Li L, Gan N Q et al. 2014. Seasonal dynamics of water bloom-forming Microcystis morphospecies and the associated extracellular microcystin concentrations in large, shallow, eutrophic Dianchi Lake. Journal of Environmental Scienc es, 26(9): 1921–1929, https://doi.org/10.1016/j.jes.2014.06.031.
Xiao M, Li M, Reynolds C S. 2018. Colony formation in the cyanobacterium Microcystis. Biological Reviews, 93(3): 1399–1420, https://doi.org/10.1111/brv.12401.
Yang W, Zheng Z M, Lu K H et al. 2020. Manipulating the phytoplankton community has the potential to create a stable bacterioplankton community in a shrimp rearing environment. Aquaculture, 520: 734789, https://doi.org/10.1016/j.aquaculture.2019.734789.
Zhang M, Cao T, Ni L Y et al. 2010. Carbon, nitrogen and antioxidant enzyme responses of Potamogeton crispus to both low light and high nutrient stresses. Environmental and Experimental Botany, 68(1): 44–50, https://doi.org/10.1016/j.envexpbot.2009.09.003.
Zhang W Z, Gu P, Zheng X W et al. 2021. Ecological damage of submerged macrophytes by fresh cyanobacteria (FC) and cyanobacterial decomposition solution (CDS). Journal of Hazardous Materials, 401: 123372, https://doi.org/10.1016/j.jhazmat.2020.123372.
Zhang Y Y, Vo Duy S, Munoz G et al. 2022. Phytotoxic effects of microcystins, anatoxin-a and cylindrospermopsin to aquatic plants: a meta-analysis. Science of the Total Environment, 810: 152104, https://doi.org/10.1016/j.scitotenv.2021.152104.
Zheng X, Feng L, Jiang W D et al. 2020. The regulatory effects of pyridoxine deficiency on the grass carp ( Ctenopharyngodon idella ) gill barriers immunity, apoptosis, antioxidant, and tight junction challenged with Flavobacterium columnar. Fish & Shellfish Immunology, 105: 209–223, https://doi.org/10.1016/j.fsi.2020.07.036.
Zhu J Y, Liu B Y, Wang J et al. 2010. Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte ( Myriophyllum spicatum ) and its secretion. Aquatic Toxicology, 98(2): 196–203, https://doi.org/10.1016/j.aquatox.2010.02.011.
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Supported by the National Program for the Introduction of High-end Foreign Experts (No. G2021026024L), the National Natural Science Foundation of China (Nos. 31700405, U1904124), the Major Public Welfare Projects in Henan Province (No. 201300311300), and the Breeding Project of Henan Normal University (No. HNU2021PL05)
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Gao, Y., Yang, H., Gao, X. et al. Ecological damage of submerged macrophyte Myriophyllum spicatum by cell extracts from microcystin (MC)- and non-MC-producing cyanobacteria, Microcystis. J. Ocean. Limnol. 40, 1732–1749 (2022). https://doi.org/10.1007/s00343-022-1449-y
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DOI: https://doi.org/10.1007/s00343-022-1449-y