Hostname: page-component-848d4c4894-sjtt6 Total loading time: 0 Render date: 2024-06-26T08:02:00.737Z Has data issue: false hasContentIssue false

Diversity and abundance of aerobic anoxygenic phototrophic bacteria in two cyanobacterial bloom-forming lakes in China

Published online by Cambridge University Press:  25 October 2010

Limei Shi
Affiliation:
State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210093, P. R. China 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 Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210093, P. R. China 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
Zhuting Chen
Affiliation:
State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210093, P. R. China
Yawei Zhou
Affiliation:
State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210093, P. R. China
Pengfu Li*
Affiliation:
State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210093, 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
*
*Corresponding authors: pengfuli@nju.edu.cn, fxkong@niglas.ac.cn
*Corresponding authors: pengfuli@nju.edu.cn, fxkong@niglas.ac.cn
Get access

Abstract

Aerobic anoxygenic phototrophic (AAP) bacteria are widely distributed in marine and freshwater ecosystems. The aims of this study were to investigate the diversity and abundance of AAP bacteria in cyanobacterial bloom-forming eutrophic lakes and to study the association of AAP bacteria with the bloom-forming cyanobacteria. Analysis of pufM gene (the light-reaction center gene) clone libraries indicated that in eutrophic lakes (Lake Taihu and Lake Chaohu, China) with cyanobacterium Microcystis blooms, the AAP bacteria were related to members of Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria. In Lake Taihu and Lake Chaohu, Alphaproteobacteria accounted for 81.5% and 75.0% of Microcystis-associated AAP bacteria, respectively, and 84.6% and 72.5% of free-living AAP bacteria, respectively. The predominance of Alphaproteobacteria in the two lakes was different from the previously reported predominance of Betaproteobacteria in freshwater lakes. Quantitative real-time PCR analysis indicated that in Lake Taihu and Lake Chaohu, AAP bacteria represented an important part of the bacterial community associated with Microcystis, and the abundance of Microcystis-associated AAP bacteria (18.3% and 11.7%, respectively) was higher than that of free-living AAP bacteria (5.1% and 7.9%, respectively). The abundance of AAP bacteria in the two bloom-forming lakes was higher than the previously reported level in other eutrophic freshwater bodies.

Type
Research Article
Copyright
© EDP Sciences, 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allgaier, M., Uphoff, H., Felske, A. and Wagner-Dobler, I., 2003. Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl. Environ. Microbiol. , 69, 50515059.CrossRefGoogle ScholarPubMed
Béjà, O., Suzuki, M.T., Heidelberg, J.F., Nelson, W.C., Preston, C.M., Hamada, T., Eisen, J.A., Fraser, C.M. and Delong, E.F., 2002. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature , 415, 630633.CrossRefGoogle ScholarPubMed
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, 1322.CrossRefGoogle Scholar
Cottrell, M.T., Mannino, A. and Kirchman, D.L., 2006. Aerobic anoxygenic phototrophic bacteria in the Mid-Atlantic Bight and the North Pacific Gyre. Appl. Environ. Microbiol. , 72, 557564.CrossRefGoogle ScholarPubMed
Eiler, A., 2006. Evidence for the ubiquity of mixotrophic bacteria in the upper ocean: implications and consequences. Appl. Environ. Microbiol. , 72, 74317437.CrossRefGoogle ScholarPubMed
Harashima, K., Kawazoe, K., Yoshida, I. and Kamata, H., 1987. Light stimulated aerobic growth of Erythrobacter species OCh 114. Plant Cell Physiol. , 28, 365374.Google Scholar
Hu, H.J. and Wei, Y.X., 2006. The freshwater algae of China: Systematics, taxonomy and ecology, Scientific Press, China (in Chinese).Google Scholar
Hu, Y., Du, H., Jiao, N.Z. and Zeng, Y., 2006. Abundant presence of the gamma-like proteobacterial pufM gene in oxic seawater. FEMS Microbiol. Lett. , 263, 200206.CrossRefGoogle ScholarPubMed
Jiang, H., Dong, H., Yu, B., Li, Y., Ji, S., Liu, X. and Zhang, C., 2007. Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan Plateau. Environ. Microbiol. , 9, 26032621.CrossRefGoogle Scholar
Jiang, H., Dong, H., Yu, B., Ye, Q., Shen, J., Rowe, H. and Zhang, C., 2008. Dominance of putative marine benthic archaea in Qinghai Lake, northwestern China. Environ. Microbiol. , 10, 23552367.CrossRefGoogle Scholar
Jiang, H.C., Dong, H.L., Yu, B.S., Lv, G., Deng, S.C., Wu, Y.J., Dai, M.H. and Jiao, N.Z., 2009. Abundance and diversity of aerobic anoxygenic phototrophic bacteria in saline lakes on the Tibetan plateau. FEMS Microbiol. Ecol. , 67, 268278.CrossRefGoogle ScholarPubMed
Jiao, N.Z., Zhang, Y., Zeng, Y.H., Hong, N., Liu, R.L., Chen, F. and Wang, P.X., 2007. Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environ. Microbiol. , 9, 30913099.CrossRefGoogle ScholarPubMed
Jin, X.C. and Tu, Q.Y., 1990. Handbook of eutrophication investigation of lake (2nd edn.), China Environmental Science Press, Beijing, China (in Chinese).Google Scholar
Karl, D.M., 2002. Microbiological oceanography – hidden in a sea of microbes. Nature , 415, 590591.CrossRefGoogle Scholar
Karr, E.A., Sattley, W.M., Jung, D.O., Madigan, M.T. and Achenbach, L.A., 2003. Remarkable diversity of phototrophic purple bacteria in a permanently frozen Antarctic lake. Appl. Environ. Microbiol. , 69, 49104914.CrossRefGoogle Scholar
Kodama, M., Doucette, G.J. and Green, D.H., 2006. Relationships between bacteria and harmful algae. In: Granéli, E. and Turner, J.T. (eds.), Ecology of harmful algae, 189, Springer-Verlag, Berlin Heidelberg, 243255.CrossRefGoogle Scholar
Kolber, Z.S., Van Dover, C.L., Niederman, R.A. and Falkowski, P.G., 2000. Bacterial photosynthesis in surface waters of the open ocean. Nature , 407, 177179.Google ScholarPubMed
Kolber, Z.S., Plumley, F.G., Lang, A.S., Beatty, J.T., Blankenship, R.E., VanDover, C.L., Vetriani, C., Koblížek, M., Rathgeber, C. and Falkowski, P.G., 2001. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science , 292, 24922495.CrossRefGoogle ScholarPubMed
Lafay, B., Ruimy, R., Detraubenberg, C.R., Breitmayer, V., Gauthier, M.J. and Christen, R., 1995. Roseobacter algicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflagellate Prorocentrum lima . Int. J. Syst. Bacteriol. , 45, 290296.CrossRefGoogle Scholar
Lami, R., Cottrell, M.T., Ras, J., Ulloa, O., Obernosterer, I., Claustre, H., Kirchman, D.L. and Lebaron, P., 2007. High abundances of aerobic anoxygenic photosynthetic bacteria in the South Pacific Ocean. Appl. Environ. Microbiol. , 73, 41984205.CrossRefGoogle ScholarPubMed
Mašín, M., Nedoma, J., Pechar, L. and Koblížek, M., 2008. Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environ. Microbiol. , 10, 19881996.Google ScholarPubMed
Nadkarni, M., Martin, F.E., Jacques, N.A. and Hunter, N., 2002. Determination of bacterial load by real-time PCR using a broad range (universal) probe and primer set. Microbiology , 148, 257266.CrossRefGoogle Scholar
Prokic, I., Brummer, F., Brigge, T., Gortz, H.D., Gerdts, G., Schutt, C., Elbrachter, M. and Muller, W.E.G., 1998. Bacteria of the genus Roseobacter associated with the toxic dinoflagellate Prorocentrum lima . Protist , 149, 347357.CrossRefGoogle ScholarPubMed
Rinta-Kanto, J.M., Ouellette, A.J., Boyer, G.L., Twiss, M.R., Bridgeman, T.B. and Wilhelm, 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, 41984205.CrossRefGoogle ScholarPubMed
Schwalbach, M.S. and Fuhrman, J.A., 2005. Wide-ranging abundances of aerobic anoxygenic phototrophic bacteria in the world ocean revealed by epifluorescence microscopy and quantitative PCR. Limnol. Oceanogr. , 50, 620628.CrossRefGoogle Scholar
Shiba, T., 1991. Roseobacter litoralis gen. nov. sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a . Syst. Appl. Microbiol. , 14, 140145.CrossRefGoogle Scholar
Tillett, D. and Neilan, B.A., 2000. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J. Phycol. , 36, 251258.CrossRefGoogle Scholar
Waidner, L.A. and Kirchman, D.L., 2005. Aerobic anoxygenic photosynthesis genes and operons in uncultured bacteria in the Delaware River. Environ. Microbiol. , 7, 18961908.CrossRefGoogle ScholarPubMed
Waidner, L.A. and Kirchman, D.L., 2007. Aerobic anoxygenic phototrophic bacteria attached to particles in turbid maters of the Delaware and Chesapeake estuaries. Appl. Environ. Microbiol. , 73, 39363944.CrossRefGoogle Scholar
Waidner, L.A. and Kirchman, D.L., 2008. Diversity and distribution of ecotypes of the aerobic anoxygenic phototrophy gene, pufM, in the Delaware estuary. Appl. Environ. Microbiol. , 74, 40124021.CrossRefGoogle ScholarPubMed
Worm, J. and Søndergaard, M., 1998. Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat. Microb. Ecol. , 14, 1928.CrossRefGoogle Scholar
Yurkov, V.V. and Beatty, J.T., 1998. Aerobic anoxygenic phototrophic bacteria. Microbiol. Mol. Biol. Rev. , 62, 695724.Google ScholarPubMed
Yurkov, V.V. and Gorlenko, V.M., 1990. Erythrobacter sibiricus sp. nov., a new freshwater aerobic species containing bacteriochlorophyll a . Microbiology , 59, 8589.Google Scholar
Yurkova, N., Rathgeber, C., Swiderski, J., Stackebrandt, E., Beatty, J.T., Hall, K.J. and Yurkov, V., 2002. Diversity, distribution and physiology of the aerobic phototrophic bacteria in the mixolimnion of a meromictic lake. FEMS Microbiol. Ecol. , 40, 191204.CrossRefGoogle ScholarPubMed