The effect of cylindrospermopsin on the bacterioplankton community: a microcosm experiment on water from Dishui Lake, Shanghai, China

Sicheng YIN; Ruohan HUANG; Erik JEPPESEN; Lijing CHEN; Liqing WANG; Xin FANG; Wei ZHANG

doi:10.1007/s00343-022-2081-6

Your Location：

Home >

Browse articles >

The effect of cylindrospermopsin on the bacterioplankton community: a microcosm experiment on water from Dishui Lake, Shanghai, China

Special Section: Cyanobacterial blooms in China: ecology, toxicity, and treatment | Updated：2023-05-19

- The effect of cylindrospermopsin on the bacterioplankton community: a microcosm experiment on water from Dishui Lake, Shanghai, China
- Journal of Oceanology and Limnology Vol. 40, Issue 5, Pages: 1829-1839(2022)
- Affiliations：
  
  1.Engineering Research Center of Environmental DNA and Ecological Water Health Assessment, Shanghai Ocean University, Shanghai 201306, China
  2.Department of Ecoscience, Aarhus University, Silkeborg 8600, Denmark
  3.Sino-Danish Centre for Education and Research (SDC), University of Chinese Academy of Sciences, Beijing 100049, China
  4.Limnology Laboratory and EKOSAM, Department of Biological Sciences, Middle East Technical University, Ankara 06800, Turkey
  5.Institute of Marine Sciences, Middle East Technical University, Mersin 33731, Turkey
  6.School of Business, Macau University of Science and Technology, Taipa, Macao 999078, China
- Author bio：
  
  Wei ZHANG,weizhang@shou.edu.cn
- Funds：
- DOI：10.1007/s00343-022-2081-6
  CLC：
- Received：27 February 2022，
  
  Accepted：02 April 2022，
  
  Online First：06 June 2022，
  
  Published：2022-09
- Accepted：
Scan QR Code
Sicheng YIN, Ruohan HUANG, Erik JEPPESEN, et al. The effect of cylindrospermopsin on the bacterioplankton community: a microcosm experiment on water from Dishui Lake, Shanghai, China[J]. Journal of Oceanology and Limnology, 2022, 40(5): 1829-1839.
DOI：

Sicheng YIN, Ruohan HUANG, Erik JEPPESEN, et al. The effect of cylindrospermopsin on the bacterioplankton community: a microcosm experiment on water from Dishui Lake, Shanghai, China[J]. Journal of Oceanology and Limnology, 2022, 40(5): 1829-1839. DOI： 10.1007/s00343-022-2081-6.

摘要

Abstract

Eutrophication and climate warming have intensified the global expansion of invasive cyanobacteria such as

Cylindrospermopsis

spp. and

Chrysosporum

spp. Cylindrospermopsin (CYN) produced by species of the latter two genera may harm phytoplankton

zooplankton

and fishes. However

effects of CYN on the bacterioplankton community have not been studied. Based on high-throughput sequencing

we explored the effect of CYN on the structure and function of the bacterioplankton community by adding pure CYN to in-situ water collected from a brackish coastal shallow lake: Dishui Lake

China. We found that most bacterioplankton taxa had a certain tolerance potential to CYN

but that high concentrations of CYN (40 µg/L) caused a significant decrease in microbial abundance and functional groups. Of the dominant phyla

Actinobacteria had the strongest tolerance to CYN. Network analysis indicated that CYN caused shifts in the community structure of the bacterioplankton

reducing community stability and structural complexity. High CYN concentrations also reduced the correlation between the different bacterioplankton groups

and the abundances of some bacterial taxa associated with the denitrification function and the process of carbon transfer in the microbial food web were inhibited. Our study provides new insight into the response of the bacterioplankton communities to harmful algal toxins produced by cyanobacteria.

关键词

Keywords

references

Bagatini I L, Eiler A, Bertilsson S et al. 2014. Host-specificity and dynamics in bacterial communities associated with Bloom-forming freshwater phytoplankton. PLoS One , 9 (1): e85950, https://doi.org/10.1371/journal.pone.0085950.

Bar-Yosef Y, Sukenik A, Hadas O et al. 2010. Enslavement in the water body by toxic Aphanizomenon ovalisporum , inducing alkaline phosphatase in phytoplanktons. Current Biology , 20 (17): 1557–1561, https://doi.org/10.1016/j.cub.2010.07.032.

Bednarska A, Pietrzak B, Pijanowska J. 2014. Effect of poor manageability and low nutritional value of cyanobacteria on Daphnia magna life history performance. Journal of Plankton Research , 36 (3): 838–847, https://doi.org/10.1093/plankt/fbu009.

Beyer D, Surányi G, Vasas G et al. 2009. Cylindrospermopsin induces alterations of root histology and microtubule organization in common reed ( Phragmites australis ) plantlets cultured in vitro . Toxicon , 54 (4): 440–449, https://doi.org/10.1016/j.toxicon.2009.05.008.

Bloem J, Breure A M. 2003. Bioindicators/biomonitors-principles, assessment, concepts. In: Markert B A, Breure A M, Zechmeister H G eds. Microbial Indicators: Trace Metals and Other Contaminants in the Environment. Elsevier, Amsterdam. p. 259–282.

Briland R D, Stone J P, Manubolu M et al. 2020. Cyanobacterial blooms modify food web structure and interactions in western Lake Erie. Harmful Algae , 92 : 101586, https://doi.org/10.1016/j.hal.2019.03.004.

Burford M A, Beardall J, Willis A et al. 2016. Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii . Harmful Algae , 54 (4): 44–53, https://doi.org/10.1016/j.hal.2015.10.012.

Campos A, Araújo P, Pinheiro C et al. 2013. Effects on growth, antioxidant enzyme activity and levels of extracellular proteins in the green alga Chlorella vulgaris exposed to crude cyanobacterial extracts and pure microcystin and cylindrospermopsin. Ecotoxicology and Environmental Safety , 94 : 45–53, https://doi.org/10.1016/j.ecoenv.2013.04.019.

Caporaso J G, Lauber C L, Walters W A et al. 2011. Global patterns of 16s rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America , 108 (S11): 4516–4522, https://doi.org/10.1073/pnas.1000080107.

Carey C C, Brown B L, Cottingham K L. 2017. The cyanobacterium Gloeotrichia echinulata increases the stability and network complexity of phytoplankton communities. Ecosphere , 8 (7): e01830, https://doi.org/10.1002/ecs2.1830.

Chen G Y, Zheng Z H, Bai M X et al. 2020. Chronic effects of microcystin-LR at environmental relevant concentrations on photosynthesis of Typha angustifolia Linn. Ecotoxicology , 29 (5): 514–523, https://doi.org/10.1007/s10646-020-02196-2.

Chen H, Jiang J G. 2011. Toxic effects of chemical pesticides (trichlorfon and dimehypo) on Dunaliella salina . Chemosphere , 84 (5): 664–670, https://doi.org/10.1016/j.chemosphere.2011.03.032.

Choi H J, Kim B H, Kim J D et al. 2005. Streptomyces neyagawaensis as a control for the hazardous biomass of Microcystis aeruginosa (cyanobacteria) in eutrophic freshwaters. Biological Control , 33 (3): 335–343, https://doi.org/10.1016/j.biocontrol.2005.03.007.

Copley S D, Dhillon J K. 2002. Lateral gene transfer and parallel evolution in the history of glutathione biosynthesis genes. Genome Biology , 3 (5): research0025.1, https://doi.org/10.1186/gb-2002-3-5-research0025.

Dong H H, Jiang X Y, Sun S S et al. 2019. A cascade of a denitrification bioreactor and an aerobic biofilm reactor for heavy oil refinery wastewater treatment. RSC Advances , 9 (13): 7495–7504, https://doi.org/10.1039/C8RA10510C.

Fadel A, Atoui A, Lemaire B J et al. 2014. Dynamics of the toxin cylindrospermopsin and the cyanobacterium Chrysosporum ( Aphanizomenon ) ovalisporum in a Mediterranean eutrophic reservoir. Toxins , 6 (11): 3041–3057, https://doi.org/10.3390/toxins6113041.

Feng K, Zhang Z J, Cai W W et al. 2017. Biodiversity and species competition regulate the resilience of microbial biofilm community. Molecular Ecology , 26 (21): 6170–6182, https://doi.org/10.1111/mec.14356.

Huang F, Pan L Q, Lv N et al. 2017. Characterization of novel Bacillus strain N31 from mariculture water capable of halophilic heterotrophic nitrification-aerobic denitrification. Journal of Bioscience and Bioengineering , 124 (5): 564–571, https://doi.org/10.1016/j.jbiosc.2017.06.008.

Hyenstrand P, Rohrlack T, Beattie K A et al. 2003. Laboratory studies of dissolved radiolabelled microcystin-LR in lake water. Water Research , 37 (14): 3299–3306, https://doi.org/10.1016/S0043-1354(03)00180-5.

Jámbrik K, Máthé C, Vasas G et al. 2010. Cylindrospermopsin inhibits growth and modulates protease activity in the aquatic plants Lemna minor L. and Wolffia arrhiza (L. ) Horkel. Acta Biologica Hungarica , 61 (S1): 77–94, https://doi.org/10.1556/ABiol.61.2010.Suppl.9.

Jiang Y G, Xiao P, Yu G L et al. 2014. Sporadic distribution and distinctive variations of Cylindrospermopsin genes in cyanobacterial strains and environmental samples from Chinese freshwater bodies. Applied and Environmental Microbiology , 80 (17): 5219–5230, https://doi.org/10.1128/AEM.00551-14.

Kara E L, Hanson P C, Hu Y H et al. 2013. A decade of seasonal dynamics and co-occurrences within freshwater bacterioplankton communities from eutrophic Lake Mendota, WI, USA. The ISME Journal , 7 (3): 680–684, https://doi.org/10.1038/ismej.2012.118.

Lance E, Alonzo F, Tanguy M et al. 2011. Impact of microcystin-producing cyanobacteria on reproductive success of Lymnaea stagnalis (Gastropoda, Pulmonata) and predicted consequences at the population level. Ecotoxicology , 20 (4): 719–730, https://doi.org/10.1007/s10646-011-0613-5.

Lance E, Paty C, Bormans M et al. 2007. Interactions between cyanobacteria and gastropods: Ⅱ. Impact of toxic Planktothrix agardhii on the life-history traits of Lymnaea stagnalis . Aquatic Toxicology , 81 (4): 389–396, https://doi.org/10.1016/j.aquatox.2006.12.019.

Lei L M, Peng L, Huang X H et al. 2014. Occurrence and dominance of Cylindrospermopsis raciborskii and dissolved cylindrospermopsin in urban reservoirs used for drinking water supply, South China. Environmental Monitoring and Assessment , 186 (5): 3079–3090, https://doi.org/10.1007/s10661-013-3602-8.

Li J M, Li J, Shi G et al. 2016. Discerning biodegradation and adsorption of microcystin-LR in a shallow semi-enclosed 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.

Lin Q, You W H, Xu F J et al. 2014. Zooplankton community structure and its relationship with environmental factors in Dishui Lake. Acta Ecologica Sinica , 34 (23): 6918–6929, https://doi.org/10.5846/stxb201303060360. (in Chinese with English abstract)

Lu Z, Lei L M, Lu Y et al. 2021. Phosphorus deficiency stimulates dominance of Cylindrospermopsis through facilitating cylindrospermopsin-induced alkaline phosphatase secretion: Integrating field and laboratory-based evidences. Environmental Pollution , 290 : 117946, https://doi.org/10.1016/j.envpol.2021.117946.

Murray R E, Knowles R. 2003. Production of NO and N 2 O in the presence and absence of C 2 H 2 by soil slurries and batch cultures of denitrifying bacteria. Soil Biology and Biochemistry , 35 (8): 1115–1122, https://doi.org/10.1016/S0038-0717(03)00163-9.

Newman M E J. 2003. The structure and function of complex networks. SIAM Review , 45 (2): 167–256.

Pohnert G, Steinke M, Tollrian R. 2007. Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends in Ecology & Evolution , 22 (4): 198204, https://doi.org/10.1016/j.tree.2007.01.005.

Rzymski P, Poniedzialek B, Kokociński M et al. 2014. Interspecific allelopathy in cyanobacteria: cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa . Harmful Algae , 35 : 1–8, https://doi.org/10.1016/j.hal.2014.03.002.

Shi W L, Jiang R D, Ma T H et al. 2018. Molecular ecological network analysis of sedimental microbial community and its response to environmental factors in different trophic status areas of Taihu Lake. Journal of Nanjing University ( Natural Science ), 54 (5): 1045–1056. https://doi.org/10.13232/j.cnki.jnju.2018.05.021. (in Chinese with English abstract)

Singh D P, Tyagi M B, Kumar A et al. 2001. Antialgal activity of a hepatotoxin-producing cyanobacterium, Microcystis aeruginosa . World Journal of Microbiology and Biotechnology , 17 (1): 15–22, https://doi.org/10.1023/A:1016622414140.

Takahashi M, Yamada T, Tanno M et al. 2011. Nitrate removal efficiency and bacterial community dynamics in denitrification processes using poly (L-lactic acid) as the solid substrate. Microbes and Environments , 26 (3): 212–219, https://doi.org/10.1264/jsme2.ME11107.

Tian H L, Zhao J Y, Zhang H Y et al. 2015. Bacterial community shift along with the changes in operational conditions in a membrane-aerated biofilm reactor. Applied Microbiology and Biotechnology , 99 (7): 3279–3290, https://doi.org/10.1007/s00253-014-6204-7.

Valdor R, Aboal M. 2007. Effects of living cyanobacteria, cyanobacterial extracts and pure microcystins on growth and ultrastructure of microalgae and bacteria. Toxicon , 49 (6): 769–779, https://doi.org/10.1016/j.toxicon.2006.11.025.

Wang L Z, Priscu J C. 1994. Stimulation of aquatic bacterial activity by cyanobacteria. Hydrobiologia , 277 (3): 145–158.

Wilhelm S W, Farnsley S E, Lecleir G R et al. 2011. The relationships between nutrients, cyanobacterial toxins and the microbial community in Taihu (Lake Tai), China. Harmful Algae , 10 (2): 207–215, https://doi.org/10.1016/j.hal.2010.10.001.

Wilson A E, Sarnelle O, Tillmanns A R. 2006. Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnology and Oceanography , 51 (4): 1915–1924, https://doi.org/10.4319/lo.2006.51.4.1915.

Yan X C, Xu X G, Wang M Y et al. 2017. Climate warming and cyanobacteria blooms: looks at their relationships from a new perspective. Water Research , 125 : 449–457, https://doi.org/10.1016/j.watres.2017.09.008.

Yang C Y, Li D H, Liu Y D. 2008. The effect of microcystin on the growth and some physio-biochemical characteristics of representative microbial species. Acta Hydrobiologica Sinica , 32 (6): 818–823, https://doi.org/10.3724/sp.j.1035.2008.00818.

Zhang W, Jeppesen E, Wang M M et al. 2017. Allelopathic effect boosts Chrysosporum ovalisporum dominance in summer at the expense of Microcystis panniformis in a shallow coastal water body. Environmental Science and Pollution Research , 24 (5): 4666–4675, https://doi.org/10.1007/s11356-016-8149-0.

Zhang W, Shang G X, Zhang J Y et al. 2018. First report of bloom forming cyanobacterial species Chrysosporum ovalisporum in China. Plant Science Journal , 36 (2): 185–190, https://doi.org/10.11913/PSJ.2095-0837.2018.2018. (in Chinese with English abstract)

Zhou Q L, Li K M, Xie J et al. 2009. Role and functions of beneficial microorganisms in sustainable aquaculture. Bioresource Technology , 100 (16): 3780–3786, https://doi.org/10.1016/j.biortech.2008.12.037.

Zhu G Y, Chen P P. 2012. Cytotoxicities and oxidative damage mechanisms of Ctenopharyngodon idellus lymphocytes to cylindrospermopsin. Acta Scientiae Circumstantiae , 32 (5): 1199–1205, https://doi.org/10.13671/j.hjkxxb.2012.05.005.

Zhu P C, Li Y C, Gao Y F et al. 2021. Insight into the effect of nitrogen-rich substrates on the community structure and the co-occurrence network of thermophiles during lignocellulose-based composting. Bioresource Technology , 319 : 124111, https://doi.org/10.1016/j.biortech.2020.124111.

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

Molecular analyses of bacterioplankton communities with highly abundant Vibrio clades: a case study in Bohai Sea coastal waters

The ecological risks of hydrogen peroxide as a cyanocide: its effect on the community structure of bacterioplankton

The morphological and molecular detection for the presence of toxic Cylindrospermopsis (Nostocales, Cyanobacteria) in Beijing city, China

Drivers of coastal bacterioplankton community diversity and structure along a nutrient gradient in the East China Sea

Influence of Structural Parameters of Diversion Cone on Smooth Effect of Gas Ejection Bottom Pressure Impact

Related Author

Shuping WANG

Yuan ZHANG

Jia HE

Xiaobo JIA

Jianing LIN

Qinglin WANG

Meng LI

Lizhou LIN

Related Institution

College of Animal Science and Technology, Hebei Normal University of Science and Technology

Institute for Advanced Study, Shenzhen University

State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences

State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences

University of Chinese Academy of Sciences

Address：Editorial Office of JOL, 88 Haijun Rd. Qingdao, 266000, China
Tel：+86-532-82898754 Email：jol@qdio.ac.cn
Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19 京公网安备11010802024621
It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.

⁰