Advertisement

Microbial Ecology

, Volume 66, Issue 1, pp 73–83 | Cite as

Analysis of the Attached Microbial Community on Mucilaginous Cyanobacterial Aggregates in the Eutrophic Lake Taihu Reveals the Importance of Planctomycetes

  • Hai-Yuan Cai
  • Zai-sheng Yan
  • Ai-Jie Wang
  • Lee R. Krumholz
  • He-Long JiangEmail author
Environmental Microbiology

Abstract

The phylogenetic diversity of the microbial community assemblage of the carpet-like mucilaginous cyanobacterial blooms in the eutrophic Lake Taihu was investigated. 16S ribosomal DNA clone libraries produced from the DNA of cyanobacterial assemblages that had been washed to remove unattached bacteria contained only cyanobacteria. However, a further treatment which included grinding the freeze-dried material to physically detach cells followed by the removal of larger cells by filtration allowed us to detect a large variety of bacteria within the cyanobacterial bloom community. Interestingly, the dominant members of the microbial community were Planctomycetes followed by CytophagaFlavobacteriumBacteroides (CFB), Betaproteobacteria, and Gammaproteobacteria. The analysis of the 16S ribosomal DNA clone libraries made from enrichment culture revealed much higher phylogenetic diversity of bacteria. Dominant bacterial groups in the enrichment system were identified as members of the Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria subdivisions, CFB group, and Planctomycetes. In addition, the clone libraries constructed from Planctomycetes-specific 16S ribosomal RNA primers also verified that the enrichment allowed a diversity of Planctomycetes to proliferate, although the community composition was altered after enrichment.

Keywords

Clone Library Cyanobacterial Bloom Bacterial Community Composition Microcystis Bloom Rare Biosphere 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by grants from the National Science and Technology Major Project of China (2012ZX07101-010), the National Natural Science Foundation of China (31100021 and 51079139), the Knowledge Innovation Program of the Chinese Academy of Sciences (KZCX2-EW-314), Open Research Foundation of Nanjing Institute of Geography and Limnology (NIGLAS2010QD12), Natural Science Foundation of Jiangsu Province of China (SBK201122829), and Chinese Academy of Sciences Visiting Professorships for Senior International Scientists (2011T1Z37).

Supplementary material

248_2013_224_MOESM1_ESM.doc (246 kb)
Table S1 The nearest neighbors of 16S rRNA gene sequences retrieved from the physically-detached sample and enrichment sample. The clones from physically-detached sample were marked with yellow. The sequence identity was based on gapped-BLAST analysis. Accession number of the nearest neighbor was marked in parenthesis. Isolation environment of the nearest neighbor was retrieved from GenBank database. (DOC 246 kb)
248_2013_224_MOESM2_ESM.doc (1 mb)
Fig. S1 Enrichment microcosm at the beginning of experiments (A) and at the end of experiments (B). (DOC 1059 kb)
248_2013_224_Fig8_ESM.jpg (90 kb)
Fig. S2

Neighbour-joining tree of Alphaproteobacteria 16S rRNA gene sequences obtained from the PD library and ER library. (JPEG 90 kb)

248_2013_224_MOESM3_ESM.tif (593 kb)
High resolution image (TIFF 593 kb)

References

  1. 1.
    Bengtsson MM, Ovreas L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:26CrossRefGoogle Scholar
  2. 2.
    Berendt RF (1981) Influence of blue-green algae (cyanobacteria) on survival of Legionella pneumophila in aerosols. Infect Immun 32:690–692PubMedGoogle Scholar
  3. 3.
    Berg KA, Lyra C, Sivonen K, Paulin L, Suomalainen S, Tuomi P, Rapala J (2009) High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. ISME J 3:314–325PubMedCrossRefGoogle Scholar
  4. 4.
    Briee C, Moreira D, Lopez-Garcia P (2007) Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Res Microbiol 158:213–227PubMedCrossRefGoogle Scholar
  5. 5.
    Delong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934CrossRefGoogle Scholar
  6. 6.
    De Wever A, Muylaert K, Van der Gucht K, Pirlot S, Cocquyt C, Descy JP, Plisnier PD, Vyverman W (2005) Bacterial community composition in Lake Tanganyika: vertical and horizontal heterogeneity. Appl Environ Microbiol 71:5029–5037PubMedCrossRefGoogle Scholar
  7. 7.
    Eiler A, Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6:1228–1243PubMedCrossRefGoogle Scholar
  8. 8.
    Elshahed MS, Youssef NH, Luo QW, Najar FZ, Roe BA, Sisk TM, Bühring SI, Hinrichs KU, Krumholz LR (2007) Phylogenetic and metabolic diversity of Planctomycetes from anaerobic, sulfide- and sulfur-rich Zodletone Spring, Oklahoma. Appl Environ Microbiol 73:4707–4716PubMedCrossRefGoogle Scholar
  9. 9.
    Elshahed MS, Youssef NH, Spain AM, Sheik C, Najar FZ, Sukharnikov LO, Roe BA, Davis JP, Schloss PD, Krumholz LR (2008) Novelty and uniqueness patterns of rare members of the soil biosphere. Appl Environ Microbiol 74:5422–5428PubMedCrossRefGoogle Scholar
  10. 10.
    Frangeul L, Quillardet P, Castets AM, Humbert JF, Matthijs HC, Cortez D, Tolonen A, Zhang CC, Gribaldo S, Kehr JC, Zilliges Y, Ziemert N, Becker S, Talla E, Latifi A, Billault A, Lepelletier A, Dittmann E, Bouchier C, de Marsac NT (2008) Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics 9:274PubMedCrossRefGoogle Scholar
  11. 11.
    Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci USA 106:22427–22432PubMedCrossRefGoogle Scholar
  12. 12.
    Giovannoni SJ, Delong EF, Olsen GJ, Pace NR (1988) Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. J Bacteriol 170:720–726PubMedGoogle Scholar
  13. 13.
    Glöckner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, Gade D, Beck A, Borzym K, Heitmann K, Rabus R, Schlesner H, Amann R, Reinhardt R (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100:8298–8303PubMedCrossRefGoogle Scholar
  14. 14.
    Guo L (2007) Doing battle with the green monster of Lake Taihu. Science 317:116CrossRefGoogle Scholar
  15. 15.
    Havens KE (2007) Cyanobacteria blooms: effects on aquatic ecosystems, vol. 619. In: Hudnell KH (ed) Cyanobacterial harmful algal blooms: state of the science and research. Springer, New York, pp 675–732Google Scholar
  16. 16.
    Hovanec TA, Taylor LT, Blakis A, Delong EF (1998) Nitrospira-like bacteria associated with nitrite oxidation in freshwater aquaria. Appl Environ Microbiol 64:258–264PubMedGoogle Scholar
  17. 17.
    Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69:1030–1042PubMedCrossRefGoogle Scholar
  18. 18.
    Jenkins O, Byrom D, Jones D (1987) Methylophilus: a new genus of methanol-utilizing bacteria. Int J Syst Bacteriol 37:446–448CrossRefGoogle Scholar
  19. 19.
    Kolmonen E, Sivonen K, Rapala J, Haukka K (2004) Diversity of cyanobacteria and heterotrophic bacteria in cyanobacterial blooms in Lake Joutikas, Finland. Aquat Microb Ecol 36:201–211CrossRefGoogle Scholar
  20. 20.
    Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrant E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  21. 21.
    Li H, Xing P, Wu QL (2012) Characterization of the bacterial community composition in a hypoxic zone induced by Microcystis blooms in Lake Taihu, China. FEMS Microbiol Ecol 79:773–784PubMedCrossRefGoogle Scholar
  22. 22.
    Li N, Zhang L, Li F, Wang Y, Zhu Y, Kang H, Wang S, Qin S (2011) Metagenome of microorganisms associated with the toxic cyanobacteria Microcystis aeruginosa analyzed using the 454 sequencing platform. Chinese J Oceanol Limnol 29:505–513CrossRefGoogle Scholar
  23. 23.
    Lin B, Hyacinthe C, Bonneville S, Braster M, Van Cappellen P, Roling WF (2007) Phylogenetic and physiological diversity of dissimilatory ferric iron reducers in sediments of the polluted Scheldt estuary, Northwest Europe. Environ Microbiol 9:1956–1968PubMedCrossRefGoogle Scholar
  24. 24.
    McCarthy MJ, Lavrentyev PJ, Yang L, Zhang L, Chen Y, Boqiang Q, 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 581:195–207CrossRefGoogle Scholar
  25. 25.
    Morris RM, Longnecker K, Giovannoni SJ (2006) Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom. Environ Microbiol 8:1361–1370PubMedCrossRefGoogle Scholar
  26. 26.
    Nalin R, Simonet P, Vogel TM, Normand P (1999) Rhodanobacter lindaniclasticus gen. nov., sp. nov., a lindane-degrading bacterium. Int J Syst Bacteriol 49:19–23PubMedCrossRefGoogle Scholar
  27. 27.
    Neufeld JD, Boden R, Moussard H, Schafer H, Murrell JC (2008) Substrate-specific clades of active marine methylotrophs associated with a phytoplankton bloom in a temperate coastal environment. Appl Environ Microbiol 74:7321–7328PubMedCrossRefGoogle Scholar
  28. 28.
    Niu Y, Shen H, Chen J, Xie P, Yang X, Tao M, Ma ZM, Qi M (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res 45:4169–4182PubMedGoogle Scholar
  29. 29.
    Otsuka S, Suda S, Li R, Matsumoto S, Watanabe MM (2000) Morphological variability of colonies of Microcystis morphospecies in culture. J gen appl microbial 46:39–50CrossRefGoogle Scholar
  30. 30.
    Paerl HW (1996) Microscale physiological and ecological studies of aquatic cyanobacteria: macroscale implications. Microsc Res Technol 33:47–72CrossRefGoogle Scholar
  31. 31.
    Paerl HW, Xu H, McCarthy MJ, Zhu G, Qin B, Li Y, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45:1973–1983PubMedCrossRefGoogle Scholar
  32. 32.
    Pedros-Alio C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14:257–263PubMedCrossRefGoogle Scholar
  33. 33.
    Pollet T, Tadonléké RD, Humbert JF (2011) Comparison of primer sets for the study of Planctomycetes communities in lentic freshwater ecosystems. Environ Microbiol Rep 3:254–261CrossRefGoogle Scholar
  34. 34.
    Pope P, Patel B (2008) Metagenomic analysis of a freshwater toxic cyanobacteria bloom. Microbiol Ecol 64:9–27CrossRefGoogle Scholar
  35. 35.
    Qin B, Zhu G, Gao G, Zhang Y, Li W, Paerl HW, Carmichael WW (2010) A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environ Manage 45:105–112PubMedCrossRefGoogle Scholar
  36. 36.
    Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  37. 37.
    Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506PubMedCrossRefGoogle Scholar
  38. 38.
    Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4374–4376PubMedCrossRefGoogle Scholar
  39. 39.
    Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120PubMedCrossRefGoogle Scholar
  40. 40.
    Stadtländer C (2007) Scanning electron microscopy and transmission electron microscopy of Mollicutes: challenges and opportunities. In: Méndez-Vilas A, Díaz J (eds) Modern research and educational topics in microscopy. Formatex, Badajoz, pp 122–131Google Scholar
  41. 41.
    Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  42. 42.
    Tang KW, Dziallas C, Grossart HP (2011) Zooplankton and aggregates as refuge for aquatic bacteria: protection from UV, heat and ozone stresses used for water treatment. Environ Microbiol 13:378–390PubMedCrossRefGoogle Scholar
  43. 43.
    Tao M, Xie P, Chen J, Qin BQ, Zhang DW, Niu Y, Zhang M, Wang Q, Wu LY (2012) Use of a generalized additive model to investigate key abiotic factors affecting microcystin cellular quotas in heavy bloom areas of Lake Taihu. PLoS One 7:e32020PubMedCrossRefGoogle Scholar
  44. 44.
    Tison DL, Pope DH, Cherry WB, Fliermans CB (1980) Growth of Legionella pneumophila in association with blue-green algae (cyanobacteria). Appl Environ Microbiol 39:456–459PubMedGoogle Scholar
  45. 45.
    Tuomainen J, Hietanen S, Kuparinen J, Martikainen PJ, Servomaa K (2006) Community structure of the bacteria associated with Nodularia sp. (Cyanobacteria) aggregates in the Baltic Sea. Microbial Ecol 52:513–522CrossRefGoogle Scholar
  46. 46.
    Urakami T, Sasaki J, Suzuki KI, Komagata K (1995) Characterization and description of Hyphomicrobium denitrificans sp. nov. Int J Syst Bacteriol 45:528–532CrossRefGoogle Scholar
  47. 47.
    Visser PM, Ibelings BW, Van der Veer B, Koedood J, Mur LR (1996) Artificial mixing prevents nuisance blooms of the cyanobacterium Microcystis in Lake Nieuwe Meer, The Netherlands. Freshwater Biol 36:435–450CrossRefGoogle Scholar
  48. 48.
    Wang L, Priscu JC (1994) Stimulation of aquatic bacterial activity by cyanobacteria. Hydrobiologia 277:145–158CrossRefGoogle Scholar
  49. 49.
    Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites: a short review. Toxicol Appl Pharmacol 203:201–218PubMedCrossRefGoogle Scholar
  50. 50.
    Wilhelm SW, Farnsleya SE, LeCleira GR, Laytonb AC, Satchwellc MF, DeBruynd JM, Boyerc GL, Zhu G, Paerl HW (2011) The relationships between nutrients, cyanobacterial toxins and the microbial community in Taihu (Lake Tai), China. Harmful Algae 10:207–221CrossRefGoogle Scholar
  51. 51.
    Worm J, Søndergaard M (1998a) Alcian Blue-stained particles in a eutrophic lake. J Plankton Res 20:179–186CrossRefGoogle Scholar
  52. 52.
    Worm J, Sondergaard M (1998b) Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat Microb Ecol 14:19–28CrossRefGoogle Scholar
  53. 53.
    Xing P, Kong FX (2007) Intra-habitat heterogeneity of environmental factors regulating bacterioplankton community composition in Lake Taihu, China. Aquat Microb Ecol 46:113–122CrossRefGoogle Scholar
  54. 54.
    Xing P, Li H, Liu Q, Zheng J (2012) Composition of the archaeal community involved in methane production during the decomposition of Microcystis blooms in the laboratory. Can J Microbiol 58:1153–1158PubMedCrossRefGoogle Scholar
  55. 55.
    Yagi O, Hashimoto A, Iwasaki K, Nakajima M (1999) Aerobic degradation of 1,1,1-trichloroethane by Mycobacterium spp. isolated from soil. Appl Environ Microbiol 65:4693–4696PubMedGoogle Scholar
  56. 56.
    Zhang P, Chen Y, Zhou Q, Zheng X, Zhu X, Zhao Y (2010) Understanding short-chain fatty acids accumulation enhanced in waste activated sludge alkaline fermentation: kinetics and microbiology. Environ Sci Technol 44:9343–9348PubMedCrossRefGoogle Scholar
  57. 57.
    Zhang X, Chen C, Ding J, Hou A, Li Y, Niu Z, Su X, Xu Y, Laws EA (2010) The 2007 water crisis in Wuxi, China: analysis of the origin. J Hazard Mater 182:130–135PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Hai-Yuan Cai
    • 1
  • Zai-sheng Yan
    • 1
  • Ai-Jie Wang
    • 2
  • Lee R. Krumholz
    • 3
  • He-Long Jiang
    • 1
    Email author
  1. 1.State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and LimnologyChinese Academy of SciencesNanjingPeople’s Republic of China
  2. 2.State Key Laboratory of Urban Water Resource and EnvironmentHarbin Institute of TechnologyHarbinPeople’s Republic of China
  3. 3.Department of Botany and MicrobiologyUniversity of OklahomaNormanUSA

Personalised recommendations