Skip to main content
Log in

Metagenomic Analysis of Healthy and White Plague-Affected Mussismilia braziliensis Corals

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Coral health is under threat throughout the world due to regional and global stressors. White plague disease (WP) is one of the most important threats affecting the major reef builder of the Abrolhos Bank in Brazil, the endemic coral Mussismilia braziliensis. We performed a metagenomic analysis of healthy and WP-affected M. braziliensis in order to determine the types of microbes associated with this coral species. We also optimized a protocol for DNA extraction from coral tissues. Our taxonomic analysis revealed Proteobacteria, Bacteroidetes, Firmicutes, Cyanobacteria, and Actinomycetes as the main groups in all healthy and WP-affected corals. Vibrionales, members of the CytophagaFlavobacteriumBacteroides complex, Rickettsiales, and Neisseriales were more abundant in the WP-affected corals. Diseased corals also had more eukaryotic metagenomic sequences identified as Alveolata and Apicomplexa. Our results suggest that WP disease in M. braziliensis is caused by a polymicrobial consortium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Osinga R, Schutter M, Griffioen B, Wijffels RH, Verreth JA, Shafir S, Henard S, Taruffi M, Gili C, Lavorano S (2011) The biology and economics of coral growth. Mar Biotechnol (NY) 13:658–671

    Article  CAS  Google Scholar 

  2. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422

    Article  PubMed  CAS  Google Scholar 

  3. Cypriano-Souza AL, Fernandez GP, Lima-Rosa CAV, Engel MH, Bonatto SL (2010) Microsatellite genetic characterization of the humpback whale (Megaptera novaeangliae) breeding ground off Brazil (breeding stock A). J Hered 101:189–200

    Article  PubMed  CAS  Google Scholar 

  4. Freitas MO, Abilhoa V, Silva GHDE (2011) Feeding ecology of Lutjanus analis (Teleostei: Lutjanidae) from Abrolhos Bank, Eastern Brazil. Neotrop Ichthyol 9:411–418

    Article  Google Scholar 

  5. De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119

    Article  PubMed  Google Scholar 

  6. Déath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci U S A 109(44):17995–17999

    Google Scholar 

  7. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    Article  PubMed  CAS  Google Scholar 

  8. Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302

    Article  Google Scholar 

  9. Madin JS, Connolly SR (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480

    Article  PubMed  CAS  Google Scholar 

  10. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L, Hatay M, Hall D, Brown E, Haynes M, Krause L, Sala E, Sandin SA, Thurber RV, Willis BL, Azam F, Knowlton N, Rohwer F (2008) Microbial ecology of four coral atolls in the Northern Line Islands. PLoS One 3:e1584

    Article  PubMed  Google Scholar 

  11. McDole T, Nulton J, Barott KL, Felts B, Hand C, Hatay M, Lee H, Nadon MO, Nosrat B, Salamon P, Bailey B, Sandin SA, Vargas-Angel B, Youle M, Zgliczynski BJ, Brainard RE, Rohwer F (2012) Assessing coral reefs on a pacific-wide scale using the microbialization score. PLoS One 7:e43233

    Article  PubMed  CAS  Google Scholar 

  12. Leao ZM, Kikuchi RK (2005) A relic coral fauna threatened by global changes and human activities, Eastern Brazil. Mar Pollut Bull 51:599–611

    Article  PubMed  CAS  Google Scholar 

  13. Austin B, Austin D, Sutherland R, Thompson F, Swings J (2005) Pathogenicity of vibrios to rainbow trout (Oncorhynchus mykiss, Walbaum) and Artemia nauplii. Environ Microbiol 7:1488–1495

    Article  PubMed  Google Scholar 

  14. Sussman M, Willis BL, Victor S, Bourne DG (2008) Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. PLoS One 3:e2393

    Article  PubMed  Google Scholar 

  15. Sussman M, Mieog JC, Doyle J, Victor S, Willis BL, Bourne DG (2009) Vibrio zinc-metalloprotease causes photoinactivation of coral endosymbionts and coral tissue lesions. PLoS One 4:e4511

    Article  PubMed  Google Scholar 

  16. Santos EO, Alves N Jr, Dias GM, Mazotto AM, Vermelho A, Vora GJ, Wilson B, Beltran VH, Bourne DG, Le Roux F, Thompson FL (2011) Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J 5:1471–1483

    Article  Google Scholar 

  17. Bruce T, Meirelles PM, Garcia G, Paranhos R, Rezende CE, de Moura RL, Filho RF, Coni EO, Vasconcelos AT, Amado Filho G, Hatay M, Schmieder R, Edwards R, Dinsdale E, Thompson FL (2012) Abrolhos Bank reef health evaluated by means of water quality, microbial diversity, benthic cover, and fish biomass data. PLoS One 7:e36687

    Article  PubMed  CAS  Google Scholar 

  18. 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 10:2979–2990

    Article  PubMed  CAS  Google Scholar 

  19. Lins-de-Barros MM, Vieira RP, Cardoso AM, Monteiro VA, Turque AS, Silveira CB, Albano RM, Clementino MM, Martins OB (2010) Archaea, Bacteria, and algal plastids associated with the reef-building corals Siderastrea stellata and Mussismilia hispida from Buzios, South Atlantic Ocean, Brazil. Microb Ecol 59:523–532

    Article  PubMed  CAS  Google Scholar 

  20. Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254–260

    Article  PubMed  CAS  Google Scholar 

  21. Amend AS, Barshis DJ, Oliver TA (2012) Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J 6:1291–1301

    Article  PubMed  CAS  Google Scholar 

  22. de Castro AP, Araujo SD Jr, Reis AM, Moura RL, Francini-Filho RB, Pappas G Jr, Rodrigues TB, Thompson FL, Kruger RH (2010) Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from eastern Brazil. Microb Ecol 59:658–667

    Article  PubMed  Google Scholar 

  23. Cardenas A, Rodriguez LM, Pizarro V, Cadavid LF, Arevalo-Ferro C (2012) Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease. ISME J 6:502–512

    Article  PubMed  CAS  Google Scholar 

  24. Wilson B, Aeby GS, Work TM, Bourne DG (2012) Bacterial communities associated with healthy and Acropora white syndrome-affected corals from American Samoa. FEMS Microbiol Ecol 80:509–520

    Article  PubMed  CAS  Google Scholar 

  25. Cróquer AB, C; Elliott, A; Sweet, M (2012) Bacterial assemblages shifts from healthy to yellow band disease states in the dominant reef coral Montastria faveolata. Environmental Microbiology Reports: 1–10

  26. Littman R, Willis BL, Bourne DG (2011) Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ Microbiol Report 3:651–660

    Article  CAS  Google Scholar 

  27. 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 9:2707–2719

    Article  PubMed  CAS  Google Scholar 

  28. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  29. Reis AM, Araujo SD Jr, Moura RL, Francini-Filho RB, Pappas G Jr, Coelho AM, Kruger RH, Thompson FL (2009) Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis. J Appl Microbiol 106:1378–1387

    Article  PubMed  CAS  Google Scholar 

  30. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380

    PubMed  CAS  Google Scholar 

  31. Willner D, Thurber RV, Rohwer F (2009) Metagenomic signatures of 86 microbial and viral metagenomes. Environ Microbiol 11:1752–1766

    Article  PubMed  CAS  Google Scholar 

  32. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21:1552–1560

    Article  PubMed  CAS  Google Scholar 

  33. Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinforma 9:386

    Article  CAS  Google Scholar 

  34. Kristiansson E, Hugenholtz P, Dalevi D (2009) ShotgunFunctionalizeR: an R-package for functional comparison of metagenomes. Bioinformatics 25:2737–2738

    Article  PubMed  CAS  Google Scholar 

  35. Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26:715–721

    Article  PubMed  CAS  Google Scholar 

  36. Morrow KM, Moss AG, Chadwick NE, Liles MR (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 78:6438–6449

    Article  PubMed  CAS  Google Scholar 

  37. Littman RAWB, Pfeffer C, Bourne DG (2009) Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiol Ecol 68:152–163

    Article  PubMed  CAS  Google Scholar 

  38. Prosser JI (2010) Replicate or lie. Environ Microbiol 12:1806–1810

    Article  PubMed  CAS  Google Scholar 

  39. Kvennefors EC, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS One 5:e10401

    Article  PubMed  Google Scholar 

  40. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–U382

    Article  PubMed  CAS  Google Scholar 

  41. LaJeunesse TC, Lambert G, Andersen RA, Coffroth MA, Galbraith DW (2005) Symbiodinium (Pyrrophyta) genome sizes (DNA content) are the smallest among dinoflagellates. J Phycol 42:746–748

    Google Scholar 

  42. Leão ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. Latin America coral reefs. Elsevier, Amsterdam, pp 9–52

    Book  Google Scholar 

  43. Toller WW, Rowan R, Knowlton N (2002) Genetic evidence for a protozoan (phylum Apicomplexa) associated with corals of the Montastraea annularis species complex. Coral Reefs 21:143–146

    Google Scholar 

  44. Janouškovec J, Horák A, Barott KL, Rohwer FL, Keeling PJ (2012) Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Curr Biol 22:R518–R519

    Article  PubMed  Google Scholar 

  45. Wooldridge S (2010) Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? Bioessays 32:615–625

    Article  PubMed  CAS  Google Scholar 

  46. Koike K, Jimbo M, Sakai R, Kaeriyama M, Muramoto K, Ogata T, Maruyama T, Kamiya H (2004) Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biol Bull 207:80–86

    Article  PubMed  CAS  Google Scholar 

  47. Francini-Filho RB, Moura RL, Thompson FL, Reis RM, Kaufman L, Kikuchi RK, Leão ZM (2008) Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Abrolhos Bank, eastern Brazil). Mar Pollut Bull 56:1008–1014

    Article  PubMed  CAS  Google Scholar 

  48. 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 5:370–382

    Article  PubMed  CAS  Google Scholar 

  49. Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009) Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3:512–521

    Article  PubMed  CAS  Google Scholar 

  50. Casas V, Kline DI, Wegley L, Yu YN, Breitbart M, Rohwer F (2004) Widespread association of a Rickettsiales-like bacterium with reef-building corals. Environ Microbiol 6:1137–1148

    Article  PubMed  Google Scholar 

  51. Kline DI, Vollmer SV (2011) White Band Disease (type I) of endangered caribbean acroporid corals is caused by pathogenic bacteria. Sci Rep-UK 1

  52. Wexler HM (2007) Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593–621

    Article  PubMed  CAS  Google Scholar 

  53. Kirchman DL (2008) In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New Jersey, p 606

    Chapter  Google Scholar 

  54. Lo Giudice A, Caruso C, Mangano S, Bruni V, De Domenico M, Michaud L (2012) Marine bacterioplankton diversity and community composition in an antarctic coastal environment. Microb Ecol 63:210–223

    Article  PubMed  Google Scholar 

  55. Frias-Lopez J, Klaus JS, Bonheyo GT, Fouke BW (2004) Bacterial community associated with black band disease in corals. Appl Environ Microbiol 70:5955–5962

    Article  PubMed  CAS  Google Scholar 

  56. Miller AW, Richardson LL (2011) A meta-analysis of 16S rRNA gene clone libraries from the polymicrobial black band disease of corals. FEMS Microbiol Ecol 75:231–241

    Article  PubMed  CAS  Google Scholar 

  57. Gregoracci GB, Nascimento JR, Cabral AS, Paranhos R, Valentin JL, Thompson CC, Thompson FL (2012) Structuring of bacterioplankton diversity in a large tropical bay. PLoS One 7:e31408

    Article  PubMed  CAS  Google Scholar 

  58. Godwin S, Bent E, Borneman J, Pereg L (2012) The role of coral-associated bacterial communities in Australian subtropical white syndrome of Turbinaria mesenterina. PLoS One 7:e44243

    Article  PubMed  CAS  Google Scholar 

  59. Kushmaro A, Loya Y, Fine M, Rosenberg E (1996) Bacterial infection and coral bleaching. Nature 380:396

    Article  CAS  Google Scholar 

  60. Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242

    Article  PubMed  CAS  Google Scholar 

  61. Hajishengallis G, Darveau RP, Curtis MA (2012) The keystone-pathogen hypothesis. Nat Rev Microbiol 10:717–725

    Article  PubMed  CAS  Google Scholar 

  62. Vega Thurber RL, Correa AMS (2011) Viruses of reef-building scleractinian corals. J Exp Mar Biol Ecol 408:102–113

    Article  Google Scholar 

  63. Kuznetsov YG, McPherson A (2011) Atomic force microscopy in imaging of viruses and virus-infected cells. Microbiol Mol Biol Rev 75:268–285

    Article  PubMed  CAS  Google Scholar 

  64. Eickbush TH, Jamburuthugoda VK (2008) The diversity of retrotransposons and the properties of their reverse transcriptases. Virus Res 134:221–234

    Article  PubMed  CAS  Google Scholar 

  65. Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28:913–922

    Article  PubMed  CAS  Google Scholar 

  66. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, Morell M, O’Shea KS, Moran JV, Gage FH (2009) L1 retrotransposition in human neural progenitor cells. Nature 460:1127–1131

    Article  PubMed  CAS  Google Scholar 

  67. Katzourakis A, Gifford RJ, Tristem M, Gilbert MT, Pybus OG (2009) Macroevolution of complex retroviruses. Science 325:1512

    Article  PubMed  CAS  Google Scholar 

  68. Poulter R, Butler M (1998) A retrotransposon family from the pufferfish (fugu) Fugu rubripes. Gene 215:241–249

    Article  PubMed  CAS  Google Scholar 

  69. Kim A, Terzian C, Santamaria P, Pelisson A, Purd’homme N, Bucheton A (1994) Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci U S A 91:1285–1289

    Article  PubMed  CAS  Google Scholar 

  70. Springer MS, Davidson EH, Britten RJ (1991) Retroviral-like element in a marine invertebrate. Proc Natl Acad Sci U S A 88:8401–8404

    Article  PubMed  CAS  Google Scholar 

  71. Gladyshev EA, Meselson M, Arkhipova IR (2007) A deep-branching clade of retrovirus-like retrotransposons in bdelloid rotifers. Gene 390:136–145

    Article  PubMed  CAS  Google Scholar 

  72. Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341

    Article  PubMed  CAS  Google Scholar 

  73. Faulkner GJ, Kimura Y, Daub CO, Wani S, Plessy C, Irvine KM, Schroder K, Cloonan N, Steptoe AL, Lassmann T, Waki K, Hornig N, Arakawa T, Takahashi H, Kawai J, Forrest AR, Suzuki H, Hayashizaki Y, Hume DA, Orlando V, Grimmond SM, Carninci P (2009) The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41:563–571

    Article  PubMed  CAS  Google Scholar 

  74. Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM, Bonanomi D, Firth A, Singer O, Trono D, Pfaff SL (2012) Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487:57–63

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge JST-CNPq, FAPERJ, and CAPES for funding. We also thank the project for the International Research Center for Infectious Diseases, Research Institute for Microbial Diseases, Osaka University, from the Ministry of Education, Science, Sports, Culture, and Technology, Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabiano L. Thompson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table 1

Coral Database composition and references (XLSX 11 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garcia, G.D., Gregoracci, G.B., de O. Santos, E. et al. Metagenomic Analysis of Healthy and White Plague-Affected Mussismilia braziliensis Corals. Microb Ecol 65, 1076–1086 (2013). https://doi.org/10.1007/s00248-012-0161-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0161-4

Keywords

Navigation