The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance

ISME Journal

Volumn 10, Issue 9, 2016, Pages 2280-2292

  Glasl, Bettina ^a   Herndl, Gerhard J ^a   Frade, Pedro R ^a,b,c  

^a UNIVERSITY OF VIENNA   (Austria)

^b ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^c CARMABI FOUNDATION   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; ANTIBIOTICS; BLEACHING; COMMUNITY COMPOSITION; CORAL; HEALTH STATUS; HOST-PATHOGEN INTERACTION; MICROBIAL COMMUNITY; MORTALITY; MUCUS; PROKARYOTE; SURVIVAL;

ANTHOZOA; OXALOBACTERACEAE; PORITES ASTREOIDES; PROKARYOTA; VERRUCOMICROBIACEAE; VIBRIONACEAE;

RIBOSOME DNA;

ANIMAL; ANTHOZOA; BACTERIUM; BIODIVERSITY; CHEMISTRY; CORAL REEF; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY;

ANIMALS; ANTHOZOA; BACTERIA; BIODIVERSITY; CORAL REEFS; DNA, RIBOSOMAL; MICROBIOTA; SEQUENCE ANALYSIS, DNA;

EID: 84960157936     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2016.9     Document Type: Article

References (60)

1. Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B, Zakrzewski M et al. (2015). The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9: 2261-2274.
2. Anderson MJ, Ellingsen KE, McArdle BH. (2006). Multivariate dispersion as a measure of beta diversity. Ecol Lett 9: 683-693.
3. Apprill A, Hughen K, Mincer T. (2013). Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ Microbiol 15: 2063-2072.
4. Bak RPM. (1975). Ecological aspects of the distribution of reef corals in the Netherlands Antilles. Bijdragen tot de Dierkunde 45: 181-190.
5. Bayer T, Neave MJ, Alsheikh-Hussain A, Aranda M, Yum LK, Mincer T et al. (2013). The Microbiome of the Red Sea coral stylophora pistillata is dominated by tissue-associated endozoicomonas bacteria. Appl Environ Microbiol 79: 4759-4762.
6. Ben-Haim Y, Thompson F, Thompson C, Cnockaert M, Hoste B, Swings J et al. (2003). Vibrio coralliilyticus sp nov, a temperature-dependent pathogen of the coral Pocillopora damicornis. Int J Syst Evol Microbiol 53: 309-315.
7. Bourne D, Iida Y, Uthicke S, Smith-Keune C. (2007). Changes in coral-associated microbial communities during a bleaching event. ISME J 2: 350-363.
8. Bragg L, Stone G, Imelfort M, Hugenholtz P, Tyson GW. (2012). Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat Methods 9: 425-426.
9. Brown BE, Bythell JC. (2005). Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296: 291-309.
10. Bythell JC, Wild C. (2011). Biology and ecology of coral mucus release. J Exp Mar Biol Ecol 408: 88-93.
11. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. (2010b). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267.
12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010a). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
13. Carlos C, Torres TT, Ottoboni LMM. (2013). Bacterial communities and species-specific associations with the mucus of Brazilian coral species. Sci Rep 3: 1624.
14. Coffroth MA. (1991). Cyclical mucus sheet formation on poritid corals in the San Blas Islands, Panama. Mar Biol 109: 35-40.
15. De Cáceres M, Legendre P. (2009). Associations between species and groups of sites: indices and statistical inference. Ecology 90: 3566-3574.
16. Frade PR, De Jongh F, Vermeulen F, Van Bleijswijk J, Bak RPM. (2008). Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17: 691-703.
17. Frade PR, Schwaninger V, Glasl B, Sintes E, Hill RW, Simó R et al. (2015). Dimethylsulfoniopropionate in corals and its interrelations with bacterial assemblages in coral surface mucus. Envir Chem; e-pub ahead of print 27 August 2015; doi:10. 1071/EN15023.
18. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW. (2002). Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68: 2214-2228.
19. Garren M, Azam F. (2010). New method for counting bacteria associated with coral mucus. Appl Environ Microbiol 76: 6128-6133.
20. Garren M, Son K, Raina J-B, Rusconi R, Menolascina F, Shapiro OH et al. (2014). A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heatstressed corals. ISME J 8: 999-1007.
21. Gates RD, Ainsworth TD. (2011). The nature and taxonomic composition of coral symbiomes as drivers of performance limits in scleractinian corals. J Exp Mar Biol Ecol 408: 94-101.
22. Gilbert J, Hill R, Doblin M, Ralph P. (2012). Microbial consortia increase thermal tolerance of corals. Mar Biol 159: 1763-1771.
23. Herndl GJ, Velimirov B. (1985). Bacteria in the coelenteron of Anthozoa: control of coelomic bacterial density by the coelenteric fluid. J Exp Mar Biol Ecol 93: 115-130.
24. Kelly LW, Williams GJ, Barott KL, Carlson CA, Dinsdale EA, Edwards RA et al. (2014). Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc Natl Acad Sci USA 111: 10227-10232.
25. Kooperman N, Ben-Dov E, Kramarsky-Winter E, Barak Z, Kushmaro A. (2007). Coral mucus-associated bacterial communities from natural and aquarium environments. FEMS Microbiol 276: 106-113.
26. Koren O, Rosenberg E. (2006). Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72: 5254-5259.
27. 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.
28. Lema KA, Willis BL, Bourne DG. (2014). Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ Microbiol 16: 3345-3359.
29. Lesser M, Mazel C, Gorbunov M, Falkowski P. (2004). Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305: 997-1000.
30. Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O. (2007). Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346: 36-44.
31. Li J, Chen Q, Long L-J, Dong J-D, Yang J, Zhang S. (2014). Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Sci Rep 4: 7320.
32. Mackey D, McFall AJ. (2006). MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol Microbiol 61: 1365-1371.
33. Mao-Jones J, Ritchie KB, Jones LE, Ellner SP. (2010). How microbial community composition regulates coral disease development. PLoS Biol 8: e1000345.
34. Meyer JL, Paul VJ, Teplitski M. (2014). Community shifts in the surface microbiomes of the coral Porites astreoides with unusual lesions. PLoS One 9: e100316.
35. Muscatine L. (1990). The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reefs 25: 1-29.
36. Naumann MS, Richter C, el-Zibdah M, Wild C. (2009). Coral mucus as an efficient trap for picoplanktonic cyanobacteria: implications for pelagic-benthic coupling in the reef ecosystem. Mar Ecol Prog Ser 385: 65-76.
37. Nelson CE, Goldberg SJ, Kelly LW, Haas AF, Smith JE, Rohwer F et al. (2013). Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 7: 962-979.
38. O'Toole G, Kaplan HB, Kolter R. (2000). Biofilm formation as microbial development. Annu Rev Microbiol 54: 49-79.
39. R Development Core Team (2008). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria. Available from http://www. R-project. org/.
40. Reid G, Howard J, Gan BS. (2001). Can bacterial interference prevent infection? Trend Microbiol 9: 424-428.
41. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E. (2006). The coral probiotic hypothesis. Environ Microbiol 8: 2068-2073.
42. Ritchie KB, Smith GW. (1997). Physiological comparison of bacterial communities from various species of scleractinian corals. Proc 8th Int Coral Reef Sym 1: 521-526.
43. Roder C, Arif C, Bayer T, Aranda M, Daniels C, Shibl A et al. (2014). Bacterial profiling of white plague disease in a comparative coral species framework. ISME J 8: 31-39.
44. 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.
45. Rohwer F, Seguritan V, Azam F, Knowlton N. (2002). Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1-10.
46. 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.
47. Round JL, Mazmanian SK. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9: 313-323.
48. Rowan R. (2004). Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430: 742-742.
49. Séré MG, Tortosa P, Chabanet P, Turquet J, Quod J-P, Schleyer MH. (2013). Bacterial communities associated with Porites White Patch Syndrome (PWPS) on three Western Indian Ocean (WIO) coral reefs. PLoS One 8: e83746.
50. Sharshar N, Banaszak AT, Lesser MP, Amrami D. (1997). Coral endolithic algae: life in a protected environment. Pac Sci 51: 167-173.
51. Shin SC, Kim S-H, You H, Kim B, Kim AC, Lee K-A et al. (2011). Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334: 670-674.
52. Shnit-Orland M, Kushmaro A. (2009). Coral mucusassociated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67: 371-380.
53. Sunagawa S, Woodley CM, Medina M. (2010). Threatened corals provide underexplored microbial habitats. PloS One 5: e9554.
54. Sweet MJ, Croquer A, Bythell JC. (2011a). Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30: 39-52.
55. Sweet MJ, Croquer A, Bythell JC. (2011b). Development of bacterial biofilms on artifical corals in comparison to surface-associated microbes of hard corals. PLoS One 6: e21195.
56. Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM et al. (2012). Substratecontrolled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336: 608-611.
57. Thurber RLV, Barott KL, Hall D, Liu H, Rodriguez-Mueller B, Desnues C et al. (2008). Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc Natl Acad Sci USA 105: 18413-18418.
58. Wang Q, Garrity GM, Tiedje JM, Cole JR. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
59. 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: 2807-2719.
60. Wild C, Rasheed M, Werner U, Franke U, Johnstone R, Huettel M. (2004). Degradation and mineralization of coral mucus in reef environments. Mar Ecol Prog Ser 267: 159-171.