Relationship between morphospecies and microcystinproducing genotypes of <italic style="font-style: italic">Microcystis</italic> species in Chinese freshwaters

Yang LIU; Youxin CHEN; Haiyan FANG; Hanyang LU; Xingqiang WU; Gongliang YU; Shin-ichi NAKANO; Renhui LI

doi:10.1007/s00343-020-0276-2

Your Location：

Home >

Browse articles >

Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters

Ecology | Updated：2023-04-27

- Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters
- Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters
- 海洋湖沼学报（英文） 2021年39卷第5期页码：1926-1937
- Affiliations：
  
  1.College of Life Science, Henan Normal University, Xinxiang 453007, China
  2.Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
  3.Center for Ecological Research, Kyoto University, Shiga 520-2113, Japan
  4.College of Life and Environmental Sciences, Wenzhou University, Wenzhou 325000, China
  5.Journal of Henan Normal University, Xinxiang 453007, China
- Author bio：
  
  Renhui LI, E-mail: renhui.li@wzu.edu.cn, reli@ihb.ac.cn
- Funds：
  
  the Science and Technology Project of Henan Province(19A180018);the Science and Technology Project of Henan Province(192102310306);the Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences(2018001);© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2021
- DOI：10.1007/s00343-020-0276-2
  中图分类号：
- 收稿：2020-07-22，
  
  录用：2020-9-29，
  
  网络首发：2020-11-10，
  
  纸质出版：2021-09
- Accepted：
Scan QR Code
Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters[J]. 海洋湖沼学报（英文）, 2021,39(5):1926-1937.

Yang LIU, Youxin CHEN, Haiyan FANG, et al. Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters[J]. Journal of Oceanology and Limnology, 2021, 39(5): 1926-1937.
Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters[J]. 海洋湖沼学报（英文）, 2021,39(5):1926-1937. DOI： 10.1007/s00343-020-0276-2.

Yang LIU, Youxin CHEN, Haiyan FANG, et al. Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters[J]. Journal of Oceanology and Limnology, 2021, 39(5): 1926-1937. DOI： 10.1007/s00343-020-0276-2.

摘要

Abstract

Twenty water bodies in China were sampled

and 186 strains of different

Microcystis

species were isolated

from which eight morphospecies were identified and 43 stains containing the

mcyB

gene were detected. Phylogenetic analysis based on the

mcyB

gene indicated that the microcystin (MC)-producing

Microcystis

in China could be divided into two groups (I and II) and showed significant differences between the two groups. The maximum sequence similarity was 69.1%. Microcystins (MCs) were measured by high-performance liquid chromatography (HPLC) analysis

and no microcystin-RR (MC-RR) was detected in some strains belonging to Group II. Compared to other regions of the world

the proportion of Chinese MC-producing

Microcystis

was different

and the regional differences were more obvious. A whole-cell polymerase chain reactio (PCR) assay was conducted to analyze the proportion of the

mcyB

gene in the laboratory cultured and field cultured

Microcystis

. The proportion of four morphospecies (

M. vividis

M. ichthyoblabe

M. novacekii

and

M. aeruginosa

) that contained the

mcyB

gene exceeded 50% in the field cultured samples. Compared with former studies

M. aeruginosa

was the most likely morphotype that can produce MCs in the world. This study provided new insight of

Microcystis

hazard assessment and field monitoring.

关键词

Keywords

references

T J Attard , M D Carter , M X Fang , R C Johnson , G E Reid . Structural characterization and absolute quantification of microcystin peptides using collision-induced and ultraviolet photo-dissociation tandem mass spectrometry . Journal of the American Society for Mass Spectrometry , 2018 . 29 ( 9 ): 1 812 - 1 825 . DOI: 10.1021/jasms.8b05898 http://doi.org/10.1021/jasms.8b05898 .

S Cirés , L Wörmer , D Carrasco , A Quesada . Sedimentation patterns of toxin-producing Microcystis morphospecies in freshwater reservoirs . Toxins , 2013 . 5 ( 5 ): 939 - 957 . DOI: 10.3390/toxins5050939 http://doi.org/10.3390/toxins5050939 .

J Dyble , G L Fahnenstiel , R W Litaker , D F Millie , P A Tester . Microcystin concentrations and genetic diversity of Microcystis in the Lower Great Lakes . Environmental Toxicology , 2008 . 23 ( 4 ): 507 - 516 . DOI: 10.1002/tox.20370 http://doi.org/10.1002/tox.20370 .

A M Hotto , M F Satchwell , D L Berry , C J Gobler , G L Boyer . Spatial and temporal diversity of microcystins and microcystin-producing genotypes in Oneida Lake, NY . Harmful Algae , 2008 . 7 ( 5 ): 671 - 681 . DOI: 10.1016/j.hal.2008.02.001 http://doi.org/10.1016/j.hal.2008.02.001 .

C A Howitt . Amplification of DNA from whole cells of cyanobacteria using PCR . Biotechniques , 1996 . 21 ( 1 ): 32 - 34 . DOI: 10.2144/96211bm05 http://doi.org/10.2144/96211bm05 .

Ichimura T. 1979. Media for blue-green algae. In: Nishizawa K, Chihara M eds. Methods in Algalogical Studies. Kyouritsu, Tokyo, p. 294–305.

D Jungmann , K U Ludwichowski , V Faltin , J Benndorf . A field study to investigate environmental factors that could effect microcystin synthesis of a Microcystis population in the Bautzen reservoir . Internationale Revue der Gesamten Hydrobiologie und Hydrographie , 1996 . 81 ( 4 ): 493 - 501 . DOI: 10.1002/iroh.19960810402 http://doi.org/10.1002/iroh.19960810402 .

Kimura M. 1980. Kimura's two-parameter model of Models of DNA Evolution. In: Felsenstein J ed. 2004. Inferring Phylogenies. Sunderland, Massachusetts: Sinauer Associates, Inc.

Komárek J, Anagnostidis K. 1998. Cyanoprokaryota 1. Teil: chroococcales. In: Ettl H, Gärtner G, Heynig H, Mollenhauer D eds. Süßwasserflora von Mitteleuropa, Bd 19/1. Gustav Fischer, Jena, p. 164–190.

J Komárek , J Komárková . Review of the European Microcystis morphospecies (Cyanoprokaryotes) from nature . Fottea , 2002 . 2 ( 1 ): 1 - 24 . http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.1022.1794&rep=rep1&type=pdf http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.1022.1794&rep=rep1&type=pdf , .

S Kumar , G Stecher , M Li , C Knyaz , K Tamura . MEGA X: molecular evolutionary genetics analysis across computing platforms . Molecular Biology and Evolution , 2018 . 35 ( 6 ): 1 547 - 1 549 . DOI: 10.1093/molbev/msy096 http://doi.org/10.1093/molbev/msy096 .

R Kurmayer , E Dittmann , J Fastner , I Chorus . Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany) . Microbial Ecology , 2002 . 43 ( 1 ): 107 - 118 . DOI: 10.1007/s00248-001-0039-3 http://doi.org/10.1007/s00248-001-0039-3 .

V Le Ai Nguyen , Y Tanabe , H Matsuura , K Kaya , M M Watanabe . Morphological, biochemical and phylogenetic assessments of water-bloom-forming tropical morphospecies of Microcystis (Chroococcales, Cyanobacteria) . Phycological Research , 2012 . 60 ( 3 ): 208 - 222 . DOI: 10.1111/j.1440-1835.2012.00650.x http://doi.org/10.1111/j.1440-1835.2012.00650.x .

Y Liu , W H Tan , X Q Wu , Z X Wu , G L Yu , R H Li . First report of microcystin production in Microcystis smithii Komárek and Anagnostidis (Cyanobacteria) from a water bloom in Eastern China . Journal of Environmental Sciences , 2011 . 23 ( 1 ): 102 - 107 . DOI: 10.1016/S1001-0742(10)60379-8 http://doi.org/10.1016/S1001-0742(10)60379-8 .

Y Liu , Y Xu , Z J Wang , P Xiao , G L Yu , G X Wang , R H Li . Dominance and succession of Microcystis genotypes and morphotypes in Lake Taihu, a large and shallow freshwater lake in China . Environmental Pollution , 2016 . 219 399 - 408 . DOI: 10.1016/j.envpol.2016.05.021 http://doi.org/10.1016/j.envpol.2016.05.021 .

K Meißner , E Dittmann , T Börner . Toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa contain sequences homologous to peptide synthetase genes . FEMS Microbiology Letters , 1996 . 135 ( 2-3 ): 295 - 303 . DOI: 10.1111/j.1574-6968.1996.tb08004.x http://doi.org/10.1111/j.1574-6968.1996.tb08004.x .

B Mikalsen , G Boison , O M Skulberg , J Fastner , W Davies , T M Gabrielsen , K Rudi , K S Jakobsen . Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains . Journal of Bacteriology , 2003 . 185 ( 9 ): 2 774 - 2 785 . DOI: 10.1128/JB.185.9.2774-2785.2003 http://doi.org/10.1128/JB.185.9.2774-2785.2003 .

B A Neilan , D Jacobs , D D Therese , L L Blackall , P R Hawkins , P T Cox , A E Goodman . rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis . International Journal of Systematic and Evolutionary Microbiology , 1997 . 47 ( 3 ): 693 - 697 . DOI: 10.1099/00207713-47-3-693 http://doi.org/10.1099/00207713-47-3-693 .

S Otsuka , S Suda , R H Li , S Matsumoto , M M Watanabe . Morphological variability of colonies of Microcystis morphospecies in culture . The Journal of General and Applied Microbiology , 2000 . 46 ( 1 ): 39 - 50 . DOI: 10.2323/jgam.46.39 http://doi.org/10.2323/jgam.46.39 .

S Otsuka , S Suda , R H Li , M Watanabe , H Oyaizu , S Matsumoto , M M Watanabe . 16S rDNA sequences and phylogenetic analyses of Microcystis strains with and without phycoerythrin . FEMS Microbiology Letters , 1998 . 164 ( 1 ): 119 - 124 . DOI: 10.1111/j.1574-6968.1998.tb13076.x http://doi.org/10.1111/j.1574-6968.1998.tb13076.x .

S Otsuka , S Suda , R H Li , M Watanabe , H Oyaizu , S Matsumoto , M M Watanabe . Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence . FEMS Microbiology Letters , 1999a . 172 ( 1 ): 15 - 21 . DOI: 10.1111/j.1574-6968.1999.tb13443.x http://doi.org/10.1111/j.1574-6968.1999.tb13443.x .

S Otsuka , S Suda , R H Li , M Watanabe , H Oyaizu , S Matsumoto , M M Watanabe . Characterization of morphospecies and strains of the genus Microcystis (Cyanobacteria) for a reconsideration of species classification . Phycological Research , 1999b . 47 ( 3 ): 189 - 197 . DOI: 10.1046/j.1440-1835.1999.00162.x http://doi.org/10.1046/j.1440-1835.1999.00162.x .

T G Otten , H W Paerl . Phylogenetic inference of colony isolates comprising seasonal Microcystis blooms in Lake Taihu, China . Microbial Ecology , 2011 . 62 ( 4 ): 907 - 918 . DOI: 10.1007/s00248-011-9884-x http://doi.org/10.1007/s00248-011-9884-x .

K A Palinska , W Liesack , E Rhiel , W E Krumbein . Phenotype variability of identical genotypes: the need for a combined approach in cyanobacterial taxonomy demonstrated on Merismopedia -like isolates . Archives of Microbiology , 1996 . 166 ( 4 ): 224 - 233 . DOI: 10.1007/s002030050378 http://doi.org/10.1007/s002030050378 .

H Pan , L R Song , Y D Liu , Y Z Zhu , Q Shen . Characterization of toxic waterbloom-forming cyanobacteria by modified PCR . Acta Hydrobiologica Sinica , 2001 . 25 ( 2 ): 159 - 166 . DOI: 10.3321/j.issn:1000-3207.2001.02.009 http://doi.org/10.3321/j.issn:1000-3207.2001.02.009 .

O M Pérez-Carrascal , Y Terrat , A Giani , N Fortin , C W Greer , N Tromas , B J Shapiro . Coherence of Microcystis species revealed through population genomics . The ISME Journal , 2019 . 13 ( 12 ): 2887 - 2900 . DOI: 10.1038/s41396-019-0481-1 http://doi.org/10.1038/s41396-019-0481-1 .

A Rantala , D P Fewer , M Hisbergues , L Rouhiainen , J Vaitomaa , T Börner , K Sivonen . Phylogenetic evidence for the early evolution of microcystin synthesis . Proceedings of the National Academy of Sciences of the United States of America , 2004 . 101 ( 2 ): 568 - 573 . DOI: 10.1073/pnas.0304489101 http://doi.org/10.1073/pnas.0304489101 .

K Shan , M S Shang , B T Zhou , L Li , X X Wang , H Yang , L R Song . Application of Bayesian network including Microcystis morphospecies for microcystin risk assessment in three cyanobacterial bloom-plagued lakes, China . Harmful Algae , 2019 . 83 14 - 24 . DOI: 10.1016/j.hal.2019.01.005 http://doi.org/10.1016/j.hal.2019.01.005 .

L Q Shen , S C Ma , F F Cai , G L Yu , S C Li , R H Li . Polyphasic examination on Merismopedia tenuissima CHAB 7021 from Ganjiang River, China revealed the polyphyly of the genus Merismopedia (Cyanobacteria) . Journal of Oceanology and Limnology , 2018 . 36 ( 4 ): 1 157 - 1 165 . DOI: 10.1007/s00343-018-7341-0 http://doi.org/10.1007/s00343-018-7341-0 .

S Sidelev , A Zubishina , E Chernova . Distribution of microcystin-producing genes in Microcystis colonies from some Russian freshwaters: is there any correlation with morphospecies and colony size? . Toxicon , 2020 . 184 136 - 142 . DOI: 10.1016/j.toxicon.2020.06.005 http://doi.org/10.1016/j.toxicon.2020.06.005 .

L R Song , T Sano , R H Li , M M Watanabe , Y D Liu , K Kaya . Microcystin production of Microcystis viridis (cyanobacteria) under different culture conditions . Phycological Research , 1998 . 46 ( S2 ): 19 - 23 . DOI: 10.1046/j.1440-1835.1998.00120.x http://doi.org/10.1046/j.1440-1835.1998.00120.x .

W H Tan , Y Liu , Z X Wu , S Lin , G L Yu , B S Yu , R H Li . CpcBA -IGS as an effective marker to characterize Microcystis wesenbergii (Komárek) Komárek in Kondrateva (cyanobacteria) . Harmful Algae , 2010 . 9 ( 6 ): 607 - 612 . DOI: 10.1016/j.hal.2010.04.011 http://doi.org/10.1016/j.hal.2010.04.011 .

Y Tanabe , K Kaya , M M Watanabe . Evidence for recombination in the microcystin synthetase ( mcy ) genes of toxic cyanobacteria Microcystis spp . Journal of Molecular Evolution , 2004 . 58 ( 6 ): 633 - 641 . DOI: 10.1007/s00239-004-2583-1 http://doi.org/10.1007/s00239-004-2583-1 .

S Tsujimura , H Tsukada , H Nakahara , T Nakajima , M Nishino . Seasonal variations of Microcystis populations in sediments of Lake Biwa, Japan . Hydrobiologia , 2000 . 434 ( 1 ): 183 - 192 . DOI: 10.1023/A:1004077225916 http://doi.org/10.1023/A:1004077225916 .

V M Vasconcelos , E Pereira . Cyanobacteria diversity and toxicity in a wastewater treatment plant (Portugal) . Water Research , 2001 . 35 ( 5 ): 1 354 - 1 357 . DOI: 10.1016/S0043-1354(00)00512-1 http://doi.org/10.1016/S0043-1354(00)00512-1 .

L Via-Ordorika , J Fastner , R Kurmayer , M Hisbergues , E Dittmann , J Komarek , M Erhard , I Chorus . Distribution of microcystin-producing and non-microcystin-producing Microcystis sp.in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies . Systematic and Applied Microbiology , 2004 . 27 ( 5 ): 592 - 602 . DOI: 10.1078/0723202041748163 http://doi.org/10.1078/0723202041748163 .

H J Wang , C Xu , Y Liu , E Jeppesen , J C Svenning , J Wu , J G Wu , W X Zhang , T J Zhou , P Wang , S Nangombe , J Ma , H T Duan , J Y Fang , P Xie . From unusual suspect to serial killer: cyanotoxins boosted by climate change may jeopardize megafauna . The Innovation , 2021 . 2 ( 2 ): 100092 DOI: 10.1016/j.xinn.2021.100092 http://doi.org/10.1016/j.xinn.2021.100092 .

Z J Wang , G F Song , Y G Li , G L Yu , X Y Hou , Z X Gan , R H Li . The diversity, origin, and evolutionary analysis of geosmin synthase gene in cyanobacteria . Science of the Total Environment , 2019 . 689 789 - 796 . DOI: 10.1016/j.scitotenv.2019.06.468 http://doi.org/10.1016/j.scitotenv.2019.06.468 .

WHO. 1998. Guidelines for Drinking-Water Quality, Volume 2- Health Criteria and Other Supporting Information. Addendum. 2 nd edn. World Health Organization, Geneva.

C Wiedner , P M Visser , J Fastner , J S Metcalf , G A Codd , L R Mur . Effects of light on the microcystin content of Microcystis Strain PCC 7806 . Applied and Environmental Microbiology , 2003 . 69 ( 3 ): 1 475 - 1 481 . DOI: 10.1128/AEM.69.3.1475-1481.2003 http://doi.org/10.1128/AEM.69.3.1475-1481.2003 .

Z X Wu , N Q Gan , L R Song . Genetic diversity: geographical distribution and toxin profiles of Microcystis strains (cyanobacteria) in China . Journal of Integrative Plant Biology , 2007 . 49 ( 3 ): 262 - 269 . DOI: 10.1111/j.1744-7909.2007.00368.x http://doi.org/10.1111/j.1744-7909.2007.00368.x .

M Xiao , A Willis , M A Burford , M Li . Review: a meta-analysis comparing cell-division and cell-adhesion in Microcystis colony formation . Harmful Algae , 2017 . 67 85 - 91 . DOI: 10.1016/j.hal.2017.06.007 http://doi.org/10.1016/j.hal.2017.06.007 .

Y Xu , Z X Wu , B S Yu , X Peng , G L Yu , Z H Wei , G X Wang , R H Li . Non-microcystin producing Microcystis wesenbergii (Komárek) Komárek (Cyanobacteria) representing a main waterbloom-forming species in Chinese waters . Environmental Pollution , 2008 . 156 ( 1 ): 162 - 167 . DOI: 10.1016/j.envpol.2007.12.027 http://doi.org/10.1016/j.envpol.2007.12.027 .

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Selection of protocols for phytoplankton pigment analysis: a comparative study

Effects of aeration induced turbulence on colonial morphology and microcystin release of the bloom-forming cyanoabcterium Microcystis

Structural and functional analyses of microcystinase A: optimized heterologous expression, stability, and degradability

Synergistic microcystin degradation by a novel bacterium isolated from shrimp pond and fulvic acids

基于LMI极点配置的高空台飞行环境模拟系统PI增益调度控制研究

Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters

Relationship between morphospecies and microcystinproducing genotypes of Microcystis species in Chinese freshwaters

DOI：10.1007/s00343-020-0276-2

摘要

Abstract

关键词

Keywords

references