Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides

ISME Journal

Volumn 6, Issue 4, 2012, Pages 790-801

  Sharp, Koty H ^a,b   Distel, Dan ^b   Paul, Valerie J ^a  

^a SMITHSONIAN MARINE STATION   (United States)

^b Ocean Genome Legacy   (United States)

Author keywords

bacteria; coral larvae; mucus; Porites astreoides

Indexed keywords

BACTERIUM; CORAL; HYBRIDIZATION; IN SITU MEASUREMENT; JUVENILE; LARVA; LONG-TERM CHANGE; MICROBIAL COMMUNITY; MUCUS; POLYP; SPECIES DIVERSITY; SURVIVAL;

ANIMAL; ANTHOZOA; ARTICLE; BACTERIUM; BIODIVERSITY; CENTRAL AMERICA; CLASSIFICATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LARVA; MICROBIOLOGY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

ANIMALS; ANTHOZOA; BACTERIA; BIODIVERSITY; CARIBBEAN REGION; IN SITU HYBRIDIZATION, FLUORESCENCE; LARVA; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH;

ATLANTIC OCEAN; CARIBBEAN SEA;

ANTHOZOA; BACTERIA (MICROORGANISMS); MARINOBACTER; MARINOBACTER SP.; PORITES ASTREOIDES; ROSEOBACTER;

EID: 84858865609     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.144     Document Type: Article

References (58)

1. Altschul SF, Gish W, Miller W, Wyers EW, Lipman DJ. (1990). Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Apprill A, Marlow HQ, Martindale MQ, Rappe MS. (2009). The onset of microbial associations in the coral Pocillopora meandrina. ISME J 3: 685-699.
3. Barott KL, Rodriguez-Brito B, Janouskovec J, Marhaver KL, Smith JE, Keeling P et al. (2011). Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13: 1192-1204.
4. Ben-Haim Y, Rosenberg E. (2002). A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol (Berlin) 141: 47-55. (Pubitemid 36064879)
5. Biebl H, Allgaier M, Tindall BJ, Koblizek M, Lunsdorf H, Pukall R et al. (2005). Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagellates. Int J Syst Evol Microbiol 55: 1089-1096. (Pubitemid 40731651)
6. Boettcher KJ, Barber BJ, Singer JT. (2000). Additional evidence that juvenile oyster disease is caused by a member of the Roseobacter group and colonization of nonaffected animals by Stappia stellulata-like strains. Appl Environ Microbiol 66: 3924-3930.
7. Bright M, Bulgheresi S. (2010). A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8: 218-230.
8. Cary SC. (1994). Transovarial inheritance of endosymbiotic bacteria in the protobranch bivalve, Solemya reidi. EOS 75: 60.
9. 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: 442-443. (Pubitemid 36150424)
10. Enticknap JJ, Kelly M, Peraud O, Hill RT. (2006). Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72: 3724-3732. (Pubitemid 43728031)
11. Fiala-Medioni A, McKiness ZP, Dando P, Boulegue J, Mariotti A, Alayse-Danet AM et al. (2002). Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge: evidence for a dual symbiosis. Mar Biol (Berlin) 141: 1035-1043. (Pubitemid 36128303)
12. Frias-Lopez J, Bonheyo GT, Jin QS, Fouke BW. (2003). Cyanobacteria associated with coral black band disease in Caribbean and Indo-Pacific Reefs. Appl Environ Microbiol 69: 2409-2413. (Pubitemid 36443668)
13. 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. (Pubitemid 39471841)
14. Garren M, Raymundo L, Guest J, Harvell CD, Azam F. (2009). Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLOS One 4: e7319.
15. Gros O, Duplessis MR, Felbeck H. (1999). Embryonic development and endosymbiont transmission mode in the symbiotic clam Lucinoma aequizonata (Bivalvia: Lucinidae). Invert Reprod Dev 36: 93-103. (Pubitemid 29407570)
16. Haygood MG, Davidson SK. (1997). Small-subunit rRNA genes and in situ hybridization with oligonucleotides specific for the bacterial symbionts in the larvae of the bryozoan Bugula neritina and proposal of 'Candidatus Endobugula sertula'. Appl Environ Microbio 63: 4612-4616. (Pubitemid 27485802)
17. Hirose E. (2000). Plant rake and algal pouch of the larvae in the tropical ascidian Diplosoma similis: an adaptation for vertical transmission of photosynthetic symbionts Prochloron sp. Zoolog Sci 17: 233-240.
18. Kline DI, Kuntz NM, Breitbart M, Knowlton N, Rohwer F. (2006). Role of elevated organic carbon levels and microbial activity in coral mortality. Mar Ecol Prog Ser 314: 119-125. (Pubitemid 43989682)
19. Knowlton N, Rohwer F. (2003). Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162: S51-S62. (Pubitemid 37425177)
20. Krueger DM, Gustafson RG, Cavanaugh CM. (1996). Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia). Biol Bull 190: 195-202. (Pubitemid 126557836)
21. Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson- Williams R, Beach KS. (2006). Inhibition of coral recruitment by macroalgae and cyanobacteria. Marine Ecology Progress Series 323: 107-117. (Pubitemid 44689619)
22. Kushmaro A, Rosenberg E, Fine M, Loya Y. (1997). Bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar Ecol Prog Ser 147: 159-165.
23. Lafay B, Ruimy R, Detraubenberg CR, Breittmayer V, Gauthier MJ, Christen R. (1995). Roseobacter aligicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflagellate Prorocentum lima. Int J Syst Bacteriol 45: 290-296.
24. Lesser MP, Falcon LI, Rodriguez-Roman AR, Enriquez S, Hoegh-Guldberg O, R I-P. (2007). Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346: 143-152. (Pubitemid 350043213)
25. Lesser MP, Farrell JH. (2004). Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23: 367-377. (Pubitemid 39320598)
26. Littman RA, Bourne DG, Willis BL. (2010). Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Mol Ecol 19: 1978-1990.
27. Littman RA, Willis BL, Bourne DG. (2009a). Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389: 45-59.
28. Littman RA, Willis BL, Pfeffer C, Bourne DG. (2009b). 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.
29. Loy A, Horn M, Wagner M. (2003). probeBase - an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res 31: 514-516. (Pubitemid 36157288)
30. McGuire MP. (1998). Timing of larval release by Porites astreoides in the northern Florida Keys. Coral Reefs 17: 369-375.
31. Miller TR, Belas R. (2006). Motility is involved in Silicibacter sp. TM1040 interaction with dinoflagellates. Environ Microbiol 8: 1648-1659. (Pubitemid 44167990)
32. Miller TR, Hnilicka K, Dziedzic A, Desplats P, Belas R. (2004). Chemotaxis of Silicibacter sp. strain TM1040 toward dinoflagellate products. Appl Environ Microbiol 70: 4692-4701. (Pubitemid 39095494)
33. Mouchka ME, Hewson I, Harvell CD. (2010). Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50: 662-674.
34. Negri AP, Webster NS, Hill RT, Heyward AJ. (2001). Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Progr Ser 223: 121-131. (Pubitemid 34067270)
35. Nissimov J, Rosenberg E, Munn CB. (2009). Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292: 210-215.
36. Olson ND, Ainsworth TD, Gates RD, Takabayashi M. (2009). Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J Exp Mar Biol Ecol 371: 140-146.
37. Patterson KL, Porter JW, Ritchie KE, Polson SW, Mueller E, Peters EC et al. (2002). The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc Natl Acad Sci USA 99: 8725-8730. (Pubitemid 34693627)
38. Piekarski T, Buchholz I, Drepper T, Schobert M, Wagner- Doebler I, Tielen P et al. (2009). Genetic tools for the investigation of Roseobacter clade bacteria. BMC Microbiol 9: 265.
39. 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: 6241-6246. (Pubitemid 26230289)
40. Prokic I, Brummer F, Brigge T, Gortz HD, Gerdts G, Schutt C et al. (1998). Bacteria of the genus Roseobacter associated with the toxic dinoflagellate Prorocentrum lima. Protist 149: 347-357. (Pubitemid 29188260)
41. Ritchie KB. (2006). Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1-14. (Pubitemid 44606066)
42. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N. (2001). Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20: 85-91. (Pubitemid 32770406)
43. Rohwer F, Seguritan V, Azam F, Knowlton N. (2002). Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1-10. (Pubitemid 35436643)
44. 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: 355-362. (Pubitemid 46605489)
45. Rypien KL, Ward JR, Azam F. (2010). Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12: 28-39.
46. Schmitt S, Weisz JB, Lindquist N, Hentschel U. (2007). Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73: 2067-2078. (Pubitemid 46649495)
47. Sekar R, Kaczmarsky LT, Richardson LL. (2008). Microbial community composition of black band disease on the coral host Siderastrea siderea from three regions of the wider Caribbean. Mar Ecol Prog Ser 362: 85-98. (Pubitemid 352045314)
48. 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 Microbio 72: 5963-5973. (Pubitemid 44414624)
49. Sharp KH, Eam BE, Faulkner DJ, Haygood MG. (2007). Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73: 622-629. (Pubitemid 46147594)
50. Sharp KH, Ritchie KB, Schupp PJ, Ritson-Williams R, Paul VJ. (2010). Bacterial acquisition in juveniles of several broadcast spawning coral species. PLOS One 5: e10898.
51. Shyu C, Soule T, Bent SJ, Foster JA, Forney LJ. (1997). MiCA: a web-based tool for the analysis of microbial communities based on terminal-restriction fragment length polymorphisms of 16S and 18S rRNA genes. J Microb Ecol 53: 562-570.
52. Storey JD. (2002). A direct approach to false discovery rates. J Roy Statistical Soc, Ser B 64: 490.
53. Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR et al. (2009). Bacterial diversity and White Plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3: 512-521.
54. Sunagawa S, Woodley CM, Medina M. (2010). Threatened corals provide underexplored microbial habitats. PLOS One 5: 7.
55. Sweet M, Croquer A, Bythell J. (2011). Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30: 39-52.
56. Tebben J, Tapiolas DM, Motti CA, Abrego D, Negri AP, Blackall LL et al. (2011). Induction of larval metamorphosis of the coral Acropora millepora by tetrabromopyrrole isolated from a Pseudoalteromonas bacterium. PLOS One 6: e19082.
57. 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. (Pubitemid 47547539)
58. Yoch DC. (2002). Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environ Microbiol 68: 5804-5815. (Pubitemid 36342411)