Abstract
Although organic-aggregate-associated bacteria play a pivotal role in microbial food webs and in the cycling of major elements, their community composition and diversity have not been extensively studied, especially in shallow freshwater systems. This study is among the first to explore intra-lake horizontal heterogeneity of organic-aggregate-associated bacterial community composition (OABC) in the large, shallow, and eutrophic Lake Taihu. During November 2006, samples were collected at four locations representing different trophic states and food web structures. Regional variability of OABC and diversity were studied by amplified ribosomal DNA restriction analysis and comparative analysis of four large 16S ribosomal RNA clone libraries. Our results demonstrate that OABC were numerically dominated by members of the β-proteobacteria (19.2–38.6%), Bacteroidetes (3.6–20.0%), and α-proteobacteria (11.5–19.2%) groups. The dominance of the Bacteroidetes group was related to algae-based aggregates. Horizontal heterogeneity of OABC exists within habitats, suggesting that the trophic state of the water and the physicochemical properties of organic aggregates (OA) play a key role. Diverse bacterial communities found on OA were substantially different from free-living ones. Comparative statistical analyses of the habitats of OA-associated bacteria highlight the potential ecological importance of the exchange between OABC and the surrounding planktonic community. Lastly, we found at least 45% of sequences closely related to ones previously found in soils, sludge, sediments, and other habitats. This demonstrates that microorganisms from terrestrial and sediment habitats are an important component of OA.
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Alldredge AL (1976) Discarded appendicularian houses as sources of food, surface habitats, and particulate organic matter in planktonic environments. Limnol Oceanogr 21:14–23
Alldredge AL, Silver MW (1988) Characteristics, dynamics and significance of marine snow. Prog Oceanog 20:41–82
Allgaier M, Grossart H-P (2006) Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany. Appl Environ Microbiol 72:3489–3497
Allgaier M, Grossart H-P (2006) Seasonal dynamics and phylogenetic diversity of free-living and particle-associated bacterial communities in four lakes in northeastern Germany. Aquat Microb Ecol 45:115–128
Allgaier M, Bruckner S, Jaspers E, Grossart H-P (2007) Intra- and inter-lake variability of free-living and particle-associated Actinobacteria communities. Environ Microbiol 9:2728–2741
Azam F, Richard AL (2001) Sea snow microcosms. Nature 414:495–498
Böckelmann U, Manz W, Neu TR, Szewzyk U (2000) Characterization of the microbial community of lotic organic aggregates (‘river snow’) in the Elbe River of Germany by cultivation and molecular methods. FEMS Microbiol Ecol 33:157–170
Bergström AK, Jansson M (2000) Bacterioplankton production in humic Lake Örträsket in relation to input of bacterial cells and input of allochthonous organic carbon. Microb Ecol 39:101–115
Caron DA, Davis PG, Madin LP, Sieburth JM (1982) Heterotrophic bacteria and bacterivorous protozoa in oceanic macroaggregates. Sciences 218:795–797
Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Statist 11:265–270
Chao A, Chazdon RL, Colwell RK, Shen T-J (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159
Chen Y, Qin B, Teubner K, Dokulil MT (2003) Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25:445–453
Crump BC, Hobbie JE (2005) Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr 50:1718–1729
DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free living marine bacterial assemblages. Limnol Oceanogr 38:924–934
Eiler A, Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6:1228–1243
Eiler A, Olsson JA, Bertilsson S (2006) Diurnal variations in the auto- and heterotrophic activity of cyanobacterial phycospheres (Gloeotrichia echinulata) and the identity of attached bacteria. Freshw Biol 51:298–311
Glöckner FO, Fuchs BM, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65:3721–3726
Grossart H-P, Simon M (1993) Limnetic macroscopic organic aggregates (lake snow): occurrence, characteristics, and microbial dynamics in Lake Constance. Limnol Oceanogr 38:532–546
Grossart H-P, Simon M (1998) Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquat Microb Ecol 15:127–140
Grossart H-P, Hietanen S, Ploug H (2003) Microbial dynamics on diatom aggregates in Øresund, Denmark. Mar Ecol Prog Ser 249:69–78
Grossart H-P, Tang KW, Kiorboe T, Ploug H (2007) Comparison of cell-specific activity between free-living and attached bacteria using isolates and natural assemblages. FEMS Microbiol Lett 266:194–200
Hahn MW (2003) Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Appl Environ Microbiol 69:5248–5254
Jin XC, Tu QY (eds) (1990) In: The standard methods for observation and analysis of lake eutrophication. 2nd edn. China Environmental Science Press, Beijing, pp 138–272 (in Chinese)
Kemp PF, Aller JY (2004) Estimating prokaryotic diversity: when are 16S rDNA libraries large enough? Limnol Oceanogr: Methods 2:114–125
Kepner R, Pratt JR (1994) Use of fluorochromes for direct enumeration of total bacteria in environmental samples: past and present. Microbiol Rev 58:603–615
Kiørboe T, Jackson GA (2001) Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol Oceanogr 46:1309–1318
Kiørboe T, Grossart H-P, Ploug H, Tang K (2002) Mechanisms and rates of bacterial colonization of sinking aggregates. Appl Environ Microbiol 68:3996–4006
Kirchman DL (2002) The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100
Maidak BL, Cole JR, Lilburn TG, Parker CT Jr, Saxman PR, Stredwick JM, Garrity GM, Li B, Olsen GJ, Pramanik S, Schmidt TM, Tiedje JM (2000) The RDP (Ribosomal Database Project) continues. Nucleic Acids Res 28:173–174
Maruyama T, Kato K, Yokoyama A, Tanaka T, Hiraishi A, Park HD (2003) Dynamics of microcystin-degrading bacteria in mucilage of Microcystis. Microb Ecol 46:279–288
McCarthy MJ, Lavrentyev PJ, Yang L, Zhang L, Chen Y, Qin B, Gardner WS (2007) Nitrogen dynamics and microbial food web structure during a summer cyanobacterial bloom in a subtropical, shallow, well-mixed, eutrophic lake (Lake Taihu, China). Hydrobiologia 581:195–207
Newton RJ, Kent AD, Triplett EW, McMahon KD (2006) Microbial community dynamics in a humic lake: differential persistence of common freshwater phylotypes. Environ Microbiol 8:956–970
Paerl HW (1974) Bacterial uptake of dissolved organic matter in relation to detrital aggregation in marine and freshwater systems. Limnol Oceanogr 19:966–972
Paerl HW, Prufert LE (1987) Oxygen-poor microzones as potential sites of microbial N2 fixation in nitrogen-depleted aerobic marine waters. Appl Environ Microbiol 53:1078–1087
Paerl HW, Shimp SL (1973) Preparation of filtered plankton and detritus for study with scanning electron microscopy. Limnol Oceanogr 18:802–805
Qin BQ, Xu PZ, Wu QL, Luo LC, Zhang YL (2007) Environmental issues of Lake Taihu, China. Hydrobiologia 581:3–14
Rashidan K, Bird D (2001) Role of predatory bacteria in the termination of a cyanobacterial bloom. Microb Ecol 41:97–105
Rath J, Wu KY, Herndl GJ, DeLong EF (1998) High phylogenetic diversity in a marine-snow-associated bacterial assemblage. Aquat Microb Ecol 14:261–269
Riemann L, Winding A (2001) Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microb Ecol 42:274–285
Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–967
Schweitzer B, Huber I, Amann R, Ludwig W, Simon M (2001) α- and β-proteobacteria control the consumption and release of amino acids on lake snow aggregates. Appl Environ Microbiol 67:632–645
Selje N, Simon M (2003) Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany. Aquat Microb Ecol 30:221–237
Simon M, Grossart H-P, Schweitzer B, Ploug H (2002) Microbial ecology of organic aggregates in aquatic ecosystems. Aquat Microb Ecol 28:175–211
Smith DC, Simon M, Alldredge AL, Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139–141
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci 101:11030–11035
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Vannini C, Pockl M, Petroni G, Wu QL, Lang E, Stackebrandt E, Schrallhammer M, Richardson PM, Hahn MW (2007) Endosymbiosis in statu nascendi: close phylogenetic relationship between obligately endosymbiotic and obligately free-living Polynucleobacter strains (Betaproteobacteria). Environ Microbiol 9:347–359
Velji MI, Albright LJ (1993) Improved sample preparation for enumeration of aggregated aquatic substrate bacteria. In: Kemp PF, F. Sherr B, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis, Boca Raton, pp 139–142
Warnecke F, Amann R, Pernthaler J (2004) Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environ Microbiol 6:242–253
Weiss P, Schweitzer B, Amann R, Simon M (1996) Identification in situ and dynamics of bacteria on limnetic organic aggregates (lake snow). Appl Environ Microbiol 62:1998–2005
Worm J, Søndergaard M (1998) Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat Microb Ecol 14:19–28
Wu QL, Hahn MW (2006) Differences in structure and dynamics of Polynucleobacter communities in a temperate and a subtropical lake, revealed at three phylogenetic levels. FEMS Microbiol Ecol 57:67–79
Wu QL, Hahn MW (2006) High predictability of the seasonal dynamics of a species-like Polynucleobacter population in a freshwater lake. Environ Microbiol 8:1660–1666
Wu Q, Chen Y, Xu K, Liu Z, Hahn M (2007) Intra-habitat heterogeneity of microbial food web structure under the regime of eutrophication and sediment resuspension in the large subtropical shallow Lake Taihu, China. Hydrobiologia 581:241–254
Wu QL, Zwart G, Wu J, Kamst-van Agterveld MP, Liu S, Hahn MW (2007) Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China. Environ Microbiol 9:2765–2774
Wu X, Xi W, Ye W, 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
Xing P, Kong F (2007) Intra-habitat heterogeneity of environmental factors regulating bacterioplankton community composition in Lake Taihu, China. Aquat Microb Ecol 48:113–122
Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322
Zwart G, Crump BC, Agterveld MPK-v, Hagen F, Han S-K (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155
Acknowledgements
We thank Dr. Qinglong Wu, Dr. Meijun Chen, and Dr. Peng Xing for providing valuable advice. Dr. Guangwei Zhu and Shurong Qian provided much appreciated field support on sample collections. Taihu Laboratory for Lake Ecosystem Research, Chinese Academy of Sciences is thanked for providing data on chemistry and phytoplankton. We also thank Guijuan Xie and Yi Zhang for experimental assistance. We especially thank Prof. Hans W. Paerl for his careful review and insightful comments on an earlier version of the manuscript. This research was supported by the National Natural Science Foundation of China (grant no. 40573062) and the Knowledge Innovation Program of the Chinese Academy of Sciences (grant no. kzcx2-yw-419). Finally, we thank the anonymous reviewers and the editor for their thoughtful and constructive comments.
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Tang, X., Gao, G., Qin, B. et al. Characterization of Bacterial Communities Associated with Organic Aggregates in a Large, Shallow, Eutrophic Freshwater Lake (Lake Taihu, China). Microb Ecol 58, 307–322 (2009). https://doi.org/10.1007/s00248-008-9482-8
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DOI: https://doi.org/10.1007/s00248-008-9482-8