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Spatiotemporal Variation of Bacterial Community Composition and Possible Controlling Factors in Tropical Shallow Lagoons

  • Microbiology of Aquatic Systems
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Abstract

Bacterial community composition (BCC) has been extensively related to specific environmental conditions. Tropical coastal lagoons present great temporal and spatial variation in their limnological conditions, which, in turn, should influence the BCC. Here, we sought for the limnological factors that influence, in space and time, the BCC in tropical coastal lagoons (Rio de Janeiro State, Brazil). The Visgueiro lagoon was sampled monthly for 1 year and eight lagoons were sampled once for temporal and spatial analysis, respectively. BCC was evaluated by bacteria-specific PCR-DGGE methods. Great variations were observed in limnological conditions and BCC on both temporal and spatial scales. Changes in the BCC of Visgueiro lagoon throughout the year were best related to salinity and concentrations of NO −3 , dissolved phosphorus and chlorophyll-a, while changes in BCC between lagoons were best related to salinity and dissolved phosphorus concentration. Salinity has a direct impact on the integrity of the bacterial cell, and it was previously observed that phosphorus is the main limiting nutrient to bacterial growth in these lagoons. Therefore, we conclude that great variations in limnological conditions of coastal lagoons throughout time and space resulted in different BCCs and salinity and nutrient concentration, particularly dissolved phosphorus, are the main limnological factors influencing BCC in these tropical coastal lagoons.

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References

  1. Alonso C, Zeder M, Piccini C, Conde D, Pernthaler J (2009) Ecophysiological differences of betaproteobacterial populations in two hydrochemically distinct compartments of a subtropical lagoon. Environ Microbiol 11:867–876

    Article  PubMed  Google Scholar 

  2. Clementino MM, Vieira RP, Cardoso AM, Nascimento APA, Silveira CB, Riva TC, Gonzalez ASM, Paranhos R, Albano RM, Ventosa A, Martins OB (2008) Prokaryotic diversity in one of the largest hypersaline coastal lagoons in the world. Extremophiles 12:595–604

    Article  CAS  PubMed  Google Scholar 

  3. Colwell RK (2006) EstimateS: statistical estimation of species richness and shared species from samples, Version 8. Persistent URL <purl.oclc.org/estimates>

  4. de Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758

    Article  PubMed  Google Scholar 

  5. del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541

    Article  Google Scholar 

  6. Eiler A, Langenheder S, Bertilsson S, Tranvik LJ (2003) Heterotrophic bacterial growth efficiency and community structure at different natural organic carbon concentrations. Appl Environ Microbiol 69:3701–3709

    Article  CAS  PubMed  Google Scholar 

  7. Esteves FA, Caliman A, Santangelo JM, Guariento RD, Farjalla VF, Bozelli RL (2008) Neotropical coastal lagoons: an appraisal of their biodiversity, functioning, threats and conservation management. Braz J Biol 68:967–981

    Article  CAS  PubMed  Google Scholar 

  8. Farjalla VF, Faria BM, Esteves FA (2002) The relationship between DOC and planktonic bacteria in tropical coastal lagoons. Arch Hydrobiol 156:97–119

    Article  Google Scholar 

  9. Farjalla VF, Marinho CC, Faria BM, Amado AM, Esteves FA, Bozelli RL, Giroldo D (2009) Synergy of fresh and accumulated organic matter to bacterial growth. Microb Ecol 57:657–666

    Article  CAS  PubMed  Google Scholar 

  10. Farjalla VF, Amado AM, Suhett AL, Meirelles-Pereira F (2009) DOC removal paradigms in highly humic aquatic ecosystems. Environ Sci Pollut Res 16:531–538

    Article  CAS  Google Scholar 

  11. Fierer N, Morse JL, Berthrong ST, Bernhardt ES, Jackson RB (2007) Environmental controls on the landscape-scale biogeography of stream bacterial communities. Ecology 88:2162–2173

    Article  PubMed  Google Scholar 

  12. Fisher MM, Klug JL, Lauster G, Newton M, Triplett EW (2000) Effects of resources and trophic interactions on freshwater bacterioplankton diversity. Microb Ecol 40:125–138

    CAS  PubMed  Google Scholar 

  13. Fontes MLS, Abreu PC (2009) Spatiotemporal variation of bacterial assemblages in a shallow subtropical coastal lagoon in Southern Brazil. Microb Ecol 58:140–152

    Article  PubMed  Google Scholar 

  14. Gasol JM, Casamayor EO, Joint I, Garde K, Gustavson K, Benlloch S, Diéz B, Schauer M, Massana R, Pedrós-Alió C (2004) Control of heterotrophic prokaryotic abundance and growth rate in hypersaline planktonic environments. Aquat Microb Ecol 34:193–206

    Article  Google Scholar 

  15. Golterman HL, Clymo RS, Ohnstad MAM (1978) Methods of physical and chemical analysis of fresh water. Blackwell Scientific Publishers, Oxford, p 214

    Google Scholar 

  16. Guixa-Boixereu N, Calderón-Paz JI, Heldal M, Bratbak G, Pedrós-Alió C (1996) Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat Microb Ecol 11:215–227

    Article  Google Scholar 

  17. Hedges JI, Keil RG (1999) Organic geochemical perspectives on estuarine processes: sorption reactions and consequences. Mar Chem 65:55–65

    Article  CAS  Google Scholar 

  18. Hu CM, Muller-Karger FE, Zepp RG (2002) Absorbance, absorption coefficient, and apparent quantum yield: a comment on common ambiguity in the use of these optical concepts. Limnol Oceanogr 47:1261–1267

    Google Scholar 

  19. Jeppesen E, Søndergaard M, Pedersen AR, Jurgens K, Strzelczak A, Lauridsen TL, Johansson LS (2007) Salinity induced regime shift in shallow brackish lagoons. Ecosystems 10:47–57

    Article  CAS  Google Scholar 

  20. Judd KE, Crump BC, Kling GW (2006) Variation in dissolved organic matter controls bacterial production and community composition. Ecology 87:2068–2079

    Article  PubMed  Google Scholar 

  21. Kan J, Suzuki MT, Wang K, Evans SE, Chen F (2007) High temporal but low spatial heterogeneity of bacterioplankton in the Chesapeake bay. Appl Environ Microbiol 73:6776–6789

    Article  CAS  PubMed  Google Scholar 

  22. Kjerfve B, Schettini CAF, Knoppers B, Lessa G, Ferreira HO (1996) Hydrology and salt balance in a large, hypersaline coastal lagoon: Lagoa de Araruama, Brazil. Estuar Coast Shelf Sci 42:701–725

    Article  CAS  Google Scholar 

  23. Koroleff F (1978) Determination of ammonia. In: Grasshoff K, Ehrhardt M, Remling K (eds) Methods of seawater analysis. Verlag Chemie, Republic of Germany, pp 151–157

    Google Scholar 

  24. Lindström ES, Kamst-Van Agterveld MP, Zwart G (2005) Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol 71:8201–8206

    Article  PubMed  Google Scholar 

  25. Loisel P, Harmand J, Zemb O, Latrille E, Lobry C, Delgenes JP et al (2006) Denaturing gradient electrophoresis (DGE) and single-strand conformation polymorphism (SSCP) molecular fingerprintings revisited by simulation and used as a tool to measure microbial diversity. Environ Microbiol 8:720–731

    Article  CAS  PubMed  Google Scholar 

  26. Melo S, Bozelli RL, Esteves FA (2007) Temporal and spatial fluctuations of phytoplankton in a tropical coastal lagoon, south-eastern Brazil. Braz J Biol 67:475–483

    Article  CAS  PubMed  Google Scholar 

  27. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-eletrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  Google Scholar 

  28. Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73:127–141

    Article  CAS  PubMed  Google Scholar 

  29. Nusch EA, Palme G (1975) Biologische methoden für die praxis der gewässeruntersuchung. GWF–Wasser/Abwasser 116:562–565

    Google Scholar 

  30. Øvreås L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373

    PubMed  Google Scholar 

  31. Pedrós-Alió C, Calderon-Paz JI, MacLean MH, Medina G, Marrasé C, Gasol JM, Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol Ecol 32:143–155

    PubMed  Google Scholar 

  32. Pinhassi J, Gomez-Consarnau L, Alonso-Saez L, Sala MM, Vidal M, Pedros-Alio C, Gasol JM (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44:241–252

    Article  Google Scholar 

  33. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160

    Article  CAS  PubMed  Google Scholar 

  34. Reche I, Pulido-Villena E, Morales-Baquero R, Casamayor EO (2005) Does ecosystem size determine aquatic bacterial richness? Ecology 86:1715–1722

    Article  Google Scholar 

  35. Santangelo JM, Rocha AM, Bozelli RL, Carneiro LS, Esteves FA (2007) Zooplankton responses to sandbar opening in a tropical eutrophic coastal lagoon. Estuar Coast Shelf Sci 71:657–668

    Article  Google Scholar 

  36. Stepanauskas R, Farjalla VF, Tranvik LJ, Svensson JM, Esteves FA, Graneli W (2000) Bioavailability and sources of DOC and DON in macrophyte stands of a tropical coastal lake. Hydrobiologia 436:241–248

    Article  CAS  Google Scholar 

  37. Suhett AL, Amado AM, Enrich-Prast A, Esteves F, Farjalla VF (2007) Seasonal changes of DOC photo-oxidation rates in a tropical humic lagoon: the role of rainfall as a major regulator. Can J Fish Aquat Sci 64:1266–1272

    Article  CAS  Google Scholar 

  38. Suzuki MS, Ovalle ARC, Pereira EA (1998) Effects of sand bar openings on some limnological variables in a hypertrophic tropical coastal lagoon of Brazil. Hydrobiologia 368:111–122

    Article  CAS  Google Scholar 

  39. Suzuki M, Figueiredo R, Castro S, Silva C, Pereira E, Silva J, Aragon G (2002) Sand bar opening in a coastal lagoon (Iquipari) in the northern region of Rio de Janeiro State: hydrological and hydrochemical changes. Braz J Biol 62:51–62

    Article  CAS  PubMed  Google Scholar 

  40. Suzuki MT (1999) Effect of protistan bacterivory on coastal bacterioplankton diversity. Aquat Microb Ecol 20:261–272

    Article  Google Scholar 

  41. Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, Jeppesen E, Conde-Porcuna JM, Schwenk K, Zwart G, Degans H, Vyverman W, De Meester L (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. PNAS 104:20404–20409

    Article  PubMed  Google Scholar 

  42. Williams WD (1998) Salinity as a determinant of the structure of biological communities in salt lakes. Hydrobiologia 381:191–201

    Article  Google Scholar 

  43. Williams WD, Boulton AJ, Taaffe RG (1990) Salinity as a determinant of salt lake fauna—a question of scale. Hydrobiologia 197:257–266

    Article  CAS  Google Scholar 

  44. Woodcock S, Curtis TP, Head IM, Lunn M, Sloan WT (2006) Taxa-area relationships for microbes: the unsampled and the unseen. Ecol Lett 9:805–812

    Article  PubMed  Google Scholar 

  45. Wu QL, Zwart G, Wu J, Agterveld M, 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

    Article  CAS  PubMed  Google Scholar 

  46. Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239

    Article  CAS  PubMed  Google Scholar 

  47. Yu YH, Yan QY, Feng WS (2008) Spatiotemporal heterogeneity of plankton communities in Lake Donghu, China, as revealed by PCR-denaturing gradient gel electrophoresis and its relation to biotic and abiotic factors. FEMS Microbiol Ecol 63:328–337

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

T.L. is grateful to CAPES and FAPERJ Institutions for a post-graduate scholarship (Bolsa Nota 10—FAPERJ). R. Peixoto provided skilful assistance in DGGE analyses. A.L. Suhett kindly reviewed early draft versions of the manuscript and offered helpful suggestions for its improvement. International Foundation for Science (IFS Grant A/4006-1) and Petroleo Brasileiro SA (PETROBRAS) supported this research.

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Authors and Affiliations

  1. Laboratório de Limnologia, Departamento Ecologia, Instituto de Biologia, CCS-UFRJ, Rio de Janeiro, RJ, 21941-590, Brazil, POBox 68020

    Thaís Laque, Vinicius F. Farjalla & Francisco A. Esteves

  2. Núcleo em Ecologia e Desenvolvimento Sustentável de Macaé (NUPEM/UFRJ), Macaé, Agência Correio Macaé, Centro, Rio de Janeiro, Brazil, POBox 119331

    Vinicius F. Farjalla & Francisco A. Esteves

  3. Instituto de Microbiologia Prof. Paulo de Góes, CCS-UFRJ, Rio de Janeiro, RJ, 21941-590, Brazil

    Alexandre S. Rosado

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  1. Thaís Laque
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  2. Vinicius F. Farjalla
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  3. Alexandre S. Rosado
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  4. Francisco A. Esteves
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Correspondence to Vinicius F. Farjalla.

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Laque, T., Farjalla, V.F., Rosado, A.S. et al. Spatiotemporal Variation of Bacterial Community Composition and Possible Controlling Factors in Tropical Shallow Lagoons. Microb Ecol 59, 819–829 (2010). https://doi.org/10.1007/s00248-010-9642-5

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  • DOI: https://doi.org/10.1007/s00248-010-9642-5

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