Microbial Ecology

, Volume 59, Issue 3, pp 523–532 | Cite as

Archaea, Bacteria, and Algal Plastids Associated with the Reef-Building Corals Siderastrea stellata and Mussismilia hispida from Búzios, South Atlantic Ocean, Brazil

  • Monica M. Lins-de-Barros
  • Ricardo P. Vieira
  • Alexander M. Cardoso
  • Vivian A. Monteiro
  • Aline S. Turque
  • Cynthia B. Silveira
  • Rodolpho M. Albano
  • Maysa M. Clementino
  • Orlando B. Martins
Invertebrate Microbiology

Abstract

Reef-building corals may be seen as holobiont organisms, presenting diverse associated microbial communities. Best known is the symbiotic relationship with zooxanthellae, but Archaea, Bacteria, fungi, viruses, and algal plastids are also abundant. Until now, there is little information concerning microbial communities associated with Brazilian corals. The present study aims to describe the diversity of Archaea, Bacteria, and eukaryotic algal plastid communities associated with two sympatric species, Siderastrea stellata and Mussismilia hispida, from Southeastern Brazil, using 16S rRNA gene libraries. Since corals present a high number of other associated invertebrates, coral barcoding (COI) was performed to confirm the exclusive occurrence of coral DNA in our samples. Our analysis yielded 354 distinct microbial OTUs, represented mainly by novel phylotypes. Richness (Chao1 and ACE) and diversity (H') estimations of the microbial communities associated with both species were high and comparable to other studies. Rarefaction analyses showed that microbial diversity of S. stellata is higher than that of M. hispida. Libshuff comparative analyses showed that the highest microbial community similarity between the two coral species occurred in the bacterial libraries, while archaeal and plastidial communities were significantly different. Crenarchaeota dominated archaeal communities, while Proteobacteria was the most abundant bacterial phylum, dominated by alpha-Proteobacteria. Plastids were also represented by novel phylotypes and did not match with any 16S rRNA sequences of Cyanobacteria and zooxanthellae from GenBank. Our data improves the pool of available information on Brazilian coral microbes and shows corals as sources of diverse prokaryotic and picoeukaryotic communities.

References

  1. 1.
    Muller-Parker G, D'Élia CF (1997) Interactions between corals and their symbiotic algae. In: Birkeland CE (ed) Life and death of coral reefs. Chapman Hall, New York, pp 97–113Google Scholar
  2. 2.
    Rosenberg E, Kellogg CA, Rohwer F (2007) Coral microbiology. Oceanography 20:146–154Google Scholar
  3. 3.
    Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Progr Ser 243:1–10CrossRefGoogle Scholar
  4. 4.
    Kellogg CA (2004) Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273:81–88CrossRefGoogle Scholar
  5. 5.
    Siboni N, Ben-Dov E, Sivan A, Kushmaro A (2008) Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10:2979–2990CrossRefPubMedGoogle Scholar
  6. 6.
    Wegley L, Yu Y, Breitbart M, Casas V, Kline DI, Rohwer F (2004) Coral-associated Archaea. Mar Ecol Prog Ser 273:89–96CrossRefGoogle Scholar
  7. 7.
    Fine M, Roff G, Ainsworth TD, Hoegh-Guldberg O (2006) Phototrophic microendoliths bloom during coral “white syndrome”. Coral Reefs 25:577–581CrossRefGoogle Scholar
  8. 8.
    Yellowless D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694CrossRefGoogle Scholar
  9. 9.
    Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:1752. doi:10.1111/j.1462-2920.2009.01935.x CrossRefGoogle Scholar
  10. 10.
    Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073CrossRefPubMedGoogle Scholar
  11. 11.
    Klaus JS, Frias-Lopez J, Bonheyo GT, Heikoop JM, Fouke BW (2005) Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interespecific and spatial variation. Coral Reefs 24:129–137CrossRefGoogle Scholar
  12. 12.
    Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362CrossRefPubMedGoogle Scholar
  13. 13.
    Johnston IS, Rohwer F (2007) Microbial landscapes on the outer tissue surfaces of the reef-building coral Porites compressa. Coral Reefs 26:375–383CrossRefGoogle Scholar
  14. 14.
    Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sc 69:357–371Google Scholar
  15. 15.
    Yoneshigue-Valentin Y, Valentin JL (1992) Macroalgae of the Cabo Frio upwelling region, Brazil: ordination of communities. In: Seeliger U (ed) Coastal plant communities of Latin America. Academic, New York, pp 31–50Google Scholar
  16. 16.
    Oigman-Pszczol S, Creed JC (2004) Size structure and spatial distribution of the corals Mussismilia hispida and Siderastrea stellata (Scleractinia) at Armação dos Búzios, Brazil. Bull Mar Sc 74:433–448Google Scholar
  17. 17.
    Reis AMM, Araújo SD Jr, Moura RL, Francini-Filho RB, Pappas G Jr, Coelho AMA, Kruger RH, Thompson FL (2009) Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis. J Appl Microbiol 4:1378–1387CrossRefGoogle Scholar
  18. 18.
    Chimetto LA, Brocchi M, Gondo M, Thompson CC, Gomez-Gil B, Thompson FL (2009) Genomic diversity of vibrios associated with the Brazilian coral Mussismilia hispida and its sympatric zoanthids (Palythoa caribeaorum, Palythoa variabilis and Zoanthus solanderi). J Appl Microbiol 106:1818–1826CrossRefPubMedGoogle Scholar
  19. 19.
    Chimetto LA, Brocchi M, Thompson CC, Martins RCR, Ramos HR, Thompson FL (2008) Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida. System Appl Microbiol 31:312–319CrossRefGoogle Scholar
  20. 20.
    Clementino MM, Fernandes CC, Vieira RP, Cardoso AM, Polycarpo CR, Martins OB (2007) Archaeal diversity in naturally occurring and impacted environments from a tropical region. J Appl Microbiol 103:141–151CrossRefPubMedGoogle Scholar
  21. 21.
    Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703PubMedGoogle Scholar
  22. 22.
    Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959CrossRefPubMedGoogle Scholar
  23. 23.
    Wörheide G (2006) Low variation in partial Cytochrome Oxidase Subunit I (COI) mitochondrial sequences in the coralline Demosponge Astrosclera willeyana across the Indo-Pacific. Mar Biol (Berlin) 148:907–912CrossRefGoogle Scholar
  24. 24.
    Oliveira MC, Bhattacharya D (2000) Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids. Am J Bot 87:482–492CrossRefPubMedGoogle Scholar
  25. 25.
    Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512CrossRefPubMedGoogle Scholar
  26. 26.
    Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  27. 27.
    Otto TD, Vasconcellos EA, Gomes LHF, Moreira AS, Degrave WM, Mendonça-Lima L, Alves-Ferreira M (2008) ChromaPipe: a pipeline for analysis, quality control and management for a DNA sequencing facility. Gen Mol Res 7:861–871CrossRefGoogle Scholar
  28. 28.
    Edwing B, Hillier L, Wendl M, Green P (1998) Basecalling of automated sequencer traces using Phred accuracy assessment. Gen Res 8:175–185Google Scholar
  29. 29.
    Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA et al (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443CrossRefPubMedGoogle Scholar
  30. 30.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  31. 31.
    Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506CrossRefPubMedGoogle Scholar
  32. 32.
    Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  33. 33.
    Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  34. 34.
    Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245CrossRefPubMedGoogle Scholar
  35. 35.
    Schloss PD, Larget BR, Handelsman J (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70:5485–5492CrossRefPubMedGoogle Scholar
  36. 36.
    Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546CrossRefPubMedGoogle Scholar
  37. 37.
    Preston CM, Wu KY, Molinski TF, DeLong EF (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA 93:6241–6246CrossRefPubMedGoogle Scholar
  38. 38.
    Casas V, Kline DI, Wegley L, Yu Y, Breitbart M, Rohwer F (2004) Widespread association of a Rickettsiales-like bacterium with reef-building corals. Environ Microbiol 6:1137–1148CrossRefPubMedGoogle Scholar
  39. 39.
    Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174CrossRefPubMedGoogle Scholar
  40. 40.
    Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastrea franksi. Coral Reefs 20:85–91CrossRefGoogle Scholar
  41. 41.
    Francini-Filho RB, Moura RL, Thompson FL, Reis RM, Kaufman L, Kikuchi RKP, Leão ZMAN (2008) Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Abrolhos Bank, eastern Brazil). Mar Pollut Bull 56:1008–1014CrossRefPubMedGoogle Scholar
  42. 42.
    Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, Sugahara J et al (2006) Genomic analysis of the uncultivated marine Crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci USA 103:18296–18301CrossRefPubMedGoogle Scholar
  43. 43.
    Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl Environ Microbiol 73:5642–5647CrossRefPubMedGoogle Scholar
  44. 44.
    Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719CrossRefPubMedGoogle Scholar
  45. 45.
    Cooney RP, Pantos O, Le Tissier MDA, Barer MR, O’Donnell AG, Bythell JC (2002) Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ Microbiol 4:401–413CrossRefPubMedGoogle Scholar
  46. 46.
    Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259CrossRefPubMedGoogle Scholar
  47. 47.
    Sekar R, Mills DK, Remily ER, Voss JD, Richardson LL (2006) Microbial communities in the surface mucopolysaccharide layer and the black band microbial mat of black band-diseased Siderastrea siderea. Appl Environ Microbiol 72:5963–5973CrossRefPubMedGoogle Scholar
  48. 48.
    Barneah O, Ben-Dov E, Kramarsky-Winter E, Kushmaro A (2007) Characterization of black band disease in red sea stony corals. Environ Microbiol 9:1995–2006CrossRefPubMedGoogle Scholar
  49. 49.
    Pantos O, Cooney RP, Le Tissier MDA, Barer MR, O’Donnell AG, Bythell JC (2003) The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ Microbiol 5:370–382CrossRefPubMedGoogle Scholar
  50. 50.
    Vieira RP, Gonzalez AM, Cardoso AM, Oliveira DN, Albano RM, Clementino MM, Martins OB, Paranhos R (2008) Relationships between bsacterial diversity and environmental variables in a tropical marine environment, Rio de Janeiro. Environ Microbiol 10:189–199PubMedGoogle Scholar
  51. 51.
    Turque AS, Cardoso AM, Silveira CB, Vieira RP, Freitas FAD, Albano RM et al (2008) Bacterial communities of the marine sponges Hymeniacidon heliophila and Polymastia janeirensis and their environment in Rio de Janeiro, Brazil. Mar Biol 155:135–146CrossRefGoogle Scholar
  52. 52.
    Not F, Valentin K, Romari K, Lovejoy C, Massana R, Töbe K, Vaulot D, Medlin L (2007) Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science 315:252–254CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Monica M. Lins-de-Barros
    • 1
  • Ricardo P. Vieira
    • 1
  • Alexander M. Cardoso
    • 2
  • Vivian A. Monteiro
    • 1
  • Aline S. Turque
    • 1
  • Cynthia B. Silveira
    • 1
  • Rodolpho M. Albano
    • 3
  • Maysa M. Clementino
    • 4
  • Orlando B. Martins
    • 1
  1. 1.Laboratório de Biologia Molecular, Instituto de Bioquímica Médica, Centro de Ciências da SaúdeUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Centro Universitário Estadual da Zona OesteRio de JaneiroBrazil
  3. 3.Departamento de BioquímicaUniversidade do Estado do Rio de JaneiroRio de JaneiroBrazil
  4. 4.Instituto Nacional de Controle da Qualidade em Saúde-INCQS/FIOCRUZRio de JaneiroBrazil

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