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Changes in abundance and community structure of bacteria associated with buoyant Microcystis colonies during the decline of cyanobacterial bloom (autumn–winter transition)

Published online by Cambridge University Press:  01 December 2011

Limei Shi ,
Yuanfeng Cai ,
Fanxiang Kong  and
Yang Yu
Limei Shi
Affiliation:
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing 210008, P.R. China
Yuanfeng Cai
Affiliation:
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing 210008, P.R. China
Fanxiang Kong*
Affiliation:
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing 210008, P.R. China
Yang Yu
Affiliation:
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing 210008, P.R. China
*
*Corresponding author: fxkong@niglas.ac.cn
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Abstract

The structure and composition of the bacterial community associated with buoyant Microcystis colonies were monitored during the decline of a cyanobacterial bloom (from October 13, 2009 to January 27, 2010). When temperature decreased, the ratio between the colony-associated bacteria and the Microcystis gradually decreased as estimated by a quantitative real-time polymerase chain reaction (qRT-PCR)-based approach. Diversity of bacterial communities was determined through denaturing gradient gel electrophoresis (DGGE) of 16S rRNA gene fragments. Cluster analysis of the DGGE profiles showed that most of the bacterial communities associated with Microcystis colonies collected on the nearby dates were clustered together. The bacterial clones from four clone libraries in different months were classified into 5, 12, 6 and 12 operational taxonomic units, most of which were affiliated with Gammaproteobacteria, Alphaproteobacteria and Bacteroidetes. Shift in dominance from pathogenic Aeromonas sp. to Shewanella sp. capable of remineralization of many organic materials was observed, and both species seemed to be associated with Microcystis colonies along with the bloom decline. These results indicated that the potential harmful effects of the Microcystis bloom on the safety of lake water during the decline period should be taken into account.

Keywords

Microcystisassociated bacteriaabundancediversitydecline
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 47 , Issue 4 , 2011 , pp. 355 - 362
Copyright
© EDP Sciences, 2011

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References

Amemiya, Y., Kato, K., Okino, T. and Nakayama, O., 1990. Changes in the chemical composition of carbohydrates and proteins in surface water during a bloom of Microcystis in Lake Suwa. Ecol. Res. , 5, 153–162.CrossRefGoogle Scholar
Asai, R., Horiguchi, Y., Yoshida, A., McNiven, S., Tahira, P., Ikebukuro, K., Uchiyama, S., Masuda, Y. and Karube, I., 2001. Detection of phycobilin pigments and their seasonal change in Lake Kasumigaura using a sensitive in situ fluorometric sensor. Anal. Lett. , 34, 2521–2533.CrossRefGoogle Scholar
Bell, W.H. and Mitchell, R., 1972. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol. Bull. , 143, 264–277.CrossRefGoogle Scholar
Berg, K.A., Lyra, C., Sivonen, K., Paulin, L., Suomalainen, S., Tuomi, P. and Rapala, J., 2009. High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. ISME J. , 3, 314–325.CrossRefGoogle ScholarPubMed
Berman, T. and Viner-Mozzini, Y., 2001. Abundance and characteristics of polysaccharide and proteinaceous particles in Lake Kinneret. Aquat. Microb. Ecol. , 24, 255–264.CrossRefGoogle Scholar
Bianucci, F., Bernagozzi, M., Sacchetti, R. and Bisbini, P., 2001. Determination of Aeromonas spp. and Pseudomonas spp. in chlorinated water supply. Ann. Ig. , 13, 185–189.Google ScholarPubMed
Borrell, N., Figueras, M.J. and Guarro, J., 1998. Phenotypic identification of Aeromonas genomospecies from clinical and environmental sources. Can. J. Microbiol. , 44, 103–108.CrossRefGoogle ScholarPubMed
Bostroëm, B., Pettersson, A.K. and Ahlgren, I., 1989. Seasonal dynamics of a cyanobacteria-dominated microbial community in surface sediments of a shallow eutrophic lake. Aquat. Sci. , 51, 153–178.CrossRefGoogle Scholar
Brettar, I. and Höfle, M.G., 1993. Nitrous oxide producing heterotrophic bacteria from the water column of the Baltic sea: abundance and molecular identification. Mar. Ecol. Prog. Ser. , 94, 253–265.CrossRefGoogle Scholar
Brunberg, A.K., 1995. Microbial activity and phosphorus dynamics in eutrophic lake sediments enriched with Microcystis colonies. Freshw. Biol. , 33, 541–555.CrossRefGoogle Scholar
Brunberg, A.K., 1999. Contribution of bacteria in the mucilage of Microcystis spp. (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol. Ecol. , 29, 13–22.CrossRefGoogle Scholar
Casamatta, D. and Wickstrom, C., 2000. Sensitivity of two disjunct bacterioplankton communities to exudates from the cyanobacterium Microcystis aeruginosa . Microb. Ecol. , 41, 64–73.CrossRefGoogle Scholar
Davis, T.W., Berry, D.L., Boyer, G.L. and Gobler, C.J., 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae , 8, 715–725.CrossRefGoogle Scholar
Eiler, A. and Bertilsson, S., 2004. Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ. Microbiol. , 6, 1228–1243.CrossRefGoogle ScholarPubMed
Grossart, H.-P. and Simon, M., 1997. Formation of macroscopic organic aggregates (lake snow) in a large lake: The significance of transparent exopolymer particles, phytoplankton, and zooplankton. Limnol. Oceanogr. , 42, 1651–1659.CrossRefGoogle Scholar
Jin, X. and Tu, Q., 1990. The standard methods for observation and analysis of lake eutrophication (2nd edn), China Environmental Science Press, Beijing (in Chinese).Google Scholar
Kangatharalingam, N., Wang, L. and Priscu, J.C., 1991. Evidence for bacterial chemotaxis to cyanobacteria from a radioassay technique. Appl. Environ. Microbiol. , 57, 2395–2398.CrossRefGoogle ScholarPubMed
Kirchman, D.L., 2002. The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. , 39, 91–100.Google ScholarPubMed
Kormas, K.A., Vardaka, E., Moustaka-Gouni, M., Kontoyanni, V., Petridou, E., Gkelis, S. and Neofitou, C., 2010. Molecular detection of potentially toxic cyanobacteria and their associated bacteria in lake water column and sediment. World J. Microbiol. Biotechnol. , 26, 1473–1482.CrossRefGoogle Scholar
Manage, P.M., Kawabata, Z. and Nakano, S.I., 2000. Algicidal effects of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat. Microb. Ecol. , 22, 111–117.CrossRefGoogle Scholar
Muyzer, G., de Waal, E.C. and Uitterlinden, A.G., 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. , 59, 695–700.CrossRefGoogle ScholarPubMed
Nealson, K.H., Moser, D.P., and Saffarini, D.A., 1995. Anaerobic electron acceptor chemotaxis in Shewanella putrefaciens . Appl. Environ. Microbiol. , 61, 1551–1554.CrossRefGoogle ScholarPubMed
Pan, G., Hu, Z., Lei, A. and Li, S., 2008. Effect of crude microcystin on the viable but non-culturable state of Aeromonas sobria in aquatic environment. J. Lake Sci. , 20, 105–109 (in Chinese).Google Scholar
Pearl, H.W., 1988. Growth and reproductive strategies of freshwater bluegreen algae (cyanobacteria). In: Sandgren, C.D. (ed.), Growth and reproductive strategies of freshwater phytoplankton, Cambridge University Press, Cambridge, 261–315.Google Scholar
Pettibone, G.W., 1998. Population dynamics of Aeromonas spp. in an urban river watershed. J. Appl. Microbiol. , 85, 723–730.CrossRefGoogle Scholar
Rashidan, K.K. and Bird, D.F., 2001. Role of predatory bacteria in the termination of a cyanobacterial bloom. Microb. Ecol. , 41, 97–105.CrossRefGoogle ScholarPubMed
Reynolds, C.S., 2006. The ecology of phytoplankton, Cambridge University Press, Cambridge, 384 p.Google Scholar
Reynolds, C.S., Jaworski, G.H.M., Cmiech, H.A. and Leedale, G.F., 1981. On the annual cycle of the blue-green alga Microcystis aeruginosa Kutz Emend Elenkin. Proc. R. Soc. Lond. Ser. B. , 293, 419–477.Google Scholar
Riemann, L. and Winding, A., 2001. Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microb. Ecol. , 42, 274–285.CrossRefGoogle ScholarPubMed
Rinta-Kanto, J.M., Ouellette, A.J., Boyer, G.L., Twiss, M.R., Bridgeman, T.B. and Willhelm, S.W., 2005. Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Environ. Sci. Technol. , 39, 4198–4205.CrossRefGoogle ScholarPubMed
Rooney-Varga, J.N., Giewat, M.W., Savin, M.C., Sood, S., LeGresley, M. and Martin, J.L., 2005. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb. Ecol. , 49, 163–175.CrossRefGoogle Scholar
Salomon, P.S., Janson, S. and Granéli, E., 2003. Molecular identification of bacteria associated with filaments of Nodularia spumigena and their effect on the cyanobacterial growth. Harmful Algae , 2, 261–272.CrossRefGoogle Scholar
Schuster, S. and Herndl, G.J., 1995. Formation and significance of transparent exopolymeric particles in the northern Adriatic Sea. Mar. Ecol. Prog. Ser. , 124, 227–236.CrossRefGoogle Scholar
Shi, L.M., Cai, Y.F., Yang, H.L., Xing, P., Li, P.F., Kong, L.D. and Kong, F.X., 2009. Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. J. Environ. Sci. , 21, 1581–1590.CrossRefGoogle ScholarPubMed
Shi, L.M., Cai, Y.F., Wang, X.Y., Li, P.F., Yu, Y. and Kong, F.X., 2010. Community structure of bacteria associated with Microcystis colonies from cyanobacterial blooms. J. Freshw. Ecol. , 25, 193–203.CrossRefGoogle Scholar
Sigee, D.C., 2005. Freshwater microbiology, John Wiley and Sons Ltd., West Sussex, England, 524 p.Google Scholar
Singh, L., Sairam, M., Agarwal, M.K. and Alam, S.I., 2000. Characterization of Aeromonas hydrophila strains and their evaluation for biodegradation of night soil. World J. Microbiol. Biotechnol. , 16, 625–630.CrossRefGoogle Scholar
Steppe, T.F., Olson, J.B., Paerl, H.W., Litaker, R.W. and Belnap, J., 1996. Consortial N2 fixation: a strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol. Ecol. , 21, 149–156.CrossRefGoogle Scholar
Tillett, D. and Neilan, B.A., 2000. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J. Phycol. , 36, 251–258.CrossRefGoogle Scholar
Valeria, A.M., Ricardo, E.J., Stephan, P. and Alberto, W.D., 2006. Degradation of microcystin-RR by Sphingomonas sp. CBA4 isolated from San Roque reservoir (Córdoba-Argentina). Biodegradation , 17, 447–455.CrossRefGoogle Scholar
Van Hannen, E.J., Zwart, G., Van Agterveld, M.P., Gons, H.J., Ebert, J. and Laanbroek, H.J., 1999. Changes in bacterial and eukaryotic community structure after mass lysis of filamentous cyanobacteria associated with viruses. Appl. Environ. Microbiol. , 65, 795–801.CrossRefGoogle ScholarPubMed
Van der Westhuizen, A.J., Eloff, J.N. and Krüger, G.H.J., 1986. Effect of temperature and light intensity (fluence rate) on the composition of the toxin of the cyanobacterium Microcystis aeruginosa (UV-006). Arch. für Hydrobiol. , 108, 145–154.Google Scholar
Verspagen, J.M.H., Snelder, E.O.F.M., Visser, P.M., Johnk, K.D., Ibelings, B.W., Mur, L.R. and Huisman, J., 2005. Benthic–pelagic coupling in the population dynamics of the harmful cyanobacterium Microcystis . Freshw. Biol. , 50, 854–867.CrossRefGoogle Scholar
Worm, J. and Søndergaard, M., 1998. Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat. Microb. Ecol. , 14, 19–28.CrossRefGoogle Scholar
Wu, X., Xi, W., Ye, W. and Yang, H., 2007. Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiol. Ecol. , 61, 85–96.CrossRefGoogle ScholarPubMed
Zheng, X.H., Xiao, L., Ren, J. and Yang, L.Y., 2008. Variation of bacterial community composition in the outbreak and decline of Microcystis spp. bloom in Lake Xuanwu. Huan Jing Ke Xue , 29, 2956–2962 (in Chinese).Google ScholarPubMed