Stable and sporadic symbiotic communities of coral and algal holobionts

ISME Journal

Volumn 10, Issue 5, 2016, Pages 1157-1169

  Hester, Eric R ^a   Barott, Katie L ^b   Nulton, Jim ^c   Vermeij, Mark J A ^d,e   Rohwer, Forest L ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d Caribbean Research and Management of Biodiversity (CARMABI)   (Netherlands)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE ESTIMATION; CORAL; EVOLUTION; GENOME; GUILD; HOST-SYMBIONT INTERACTION; MICROBIAL COMMUNITY; MICROORGANISM; SAMPLING; SYMBIONT;

ACROPORA HYACINTHUS; ACROPORA ROSARIA; ALGAE; ANTHOZOA; BACTERIA (MICROORGANISMS); FUNGI; PORITES LUTEA; PROTISTA;

RIBOSOME DNA;

ALGORITHM; ANIMAL; ANTHOZOA; ARCHAEON; BACTERIUM; CLASSIFICATION; DNA BARCODING; DNA SEQUENCE; ENVIRONMENT; FUNGUS; MICROBIOLOGY; MICROFLORA; MOLECULAR EVOLUTION; POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE; SYMBIOSIS; VIRUS;

ALGORITHMS; ANIMALS; ANTHOZOA; ARCHAEA; BACTERIA; DNA BARCODING, TAXONOMIC; DNA, RIBOSOMAL; ENVIRONMENT; EVOLUTION, MOLECULAR; FUNGI; MICROBIOTA; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS; VIRUSES;

EID: 84946771694     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.190     Document Type: Article

References (90)

1. Ainsworth T, Krause L, Bridge T, Torda G, Raina J-B, Zakrzewski M et al. (2015). The coral core microbiome identifies rare bacterial taxa as ubiquitous endosym-bionts. ISME J 9: 2261-2274.
2. Aires T, Moalic Y, Serrao EA, Arnaud-Haond S. (2015). Hologenome theory supported by cooccurrence networks of species-specific bacterial communities in siphonous algae (Caulerpa). FEMS Microbiol Ecol 91.
3. Barr JJ, Youle M, Rohwer F. (2013a). Innate and acquired bacteriophage-mediated immunity. Bacteriophage 3: 10771-10776.
4. Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML, Pogliano J et al. (2013b). Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc Natl Acad Sci 110: 10771-10776.
5. Barott KL, Caselle JE, Dinsdale EA, Friedlander AM, Maragos JE, Obura D et al. (2010). The lagoon at Caroline/Millennium Atoll, Republic of Kiribati: natural history of a nearly pristine ecosystem. PLoS One 5: e10950.
6. Barott KL, Rodriguez-Brito B, Janoukovec 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.
7. Barott KL, Williams GJ, Vermeij MJ, Harris J, Smith JE, Rohwer FL et al. (2012). Natural history of coral-algae competition across a gradient of human activity in the Line Islands. Institute for Biodiversity and Ecosystem Dynamics (IBED).
8. 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.
9. 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: 5642-5647.
10. Berkelmans R, Van Oppen MJ. (2006). The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proc R Soc London B Biol Sci 273: 2305-2312.
11. Birkeland C. (1997). Life and Death of Coral Reefs. Springer Science & Business Media.
12. Bourne D, Iida Y, Uthicke S, Smith-Keune C. (2008). Changes in coral-associated microbial communities during a bleaching event. ISME J 2: 350-363.
13. Bourne DG, Munn CB. (2005). Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7: 1162-1174.
14. Bordenstein SR, Theis KR. (2015). Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13: e1002226.
15. Brucker RM, Bordenstein SR. (2013). The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus. Nasonia Sci 341: 667-669.
16. Buddemeier RW, Fautin DG. (1993). Coral bleaching as an adaptive mechanism. Bioscience 43: 320-326.
17. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
18. Carlos C, Torres TT, Ottoboni LM. (2013). Bacterial communities and species-specific associations with the mucus of Brazilian coral species. Sci Rep 3: 1624.
19. Case RJ, Longford SR, Campbell AH, Low A, Tujula N, Steinberg PD et al. (2011). Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environ Microbiol 13: 529-537.
20. Ceh J, Van Keulen M, Bourne DG. (2011). Coral-associated bacterial communities on Ningaloo Reef, Western Australia. FEMS Microbiol Ecol 75: 134-144.
21. Chen CP, Tseng CH, Chen CA, Tang SL. (2011). The dynamics of microbial partnerships in the coral Isopora palifera. ISME J 5: 728-740.
22. Chiu JM, Li S, Li A, Po B, Zhang R, Shin PK et al. (2012). Bacteria associated with skeletal tissue growth anomalies in the coral Platygyra carnosus. FEMS Microbiol Ecol 79: 380-391.
23. Daniels CA, Zeifman A, Heym K, Ritchie KB, Watson CA, Berzins I et al. (2011). Spatial heterogeneity of bacterial communities in the mucus of Montastraea annularis. Ma. Ecol Prog Ser 426: 29-40.
24. DeMartini EE, Friedlander AM, Sandin SA, Sala E. (2008). Differences in fish-assemblage structure between fished and unfished atolls in the northern Line Islands, central Pacific. Mar Ecol Progr Ser 365: 199-215.
25. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L et al. (2008). Microbial ecology of four coral atolls in the Northern Line Islands. PloS One 3: e1584.
26. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
27. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T. (2013). The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Micro-biol Rev 37: 462-476.
28. Fiore CL, Jarett JK, Olson ND, Lesser MP. (2010). Nitrogen fixation and nitrogen transformations in marine sym-bioses. Trends Microbiol 18: 455-463.
29. Frank DN. (2009). BARCRAWL and BARTAB: software tools for the design and implementation of barcoded primers for highly multiplexed DNA sequencing. BMC Bioinform 10: 362.
30. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW. (2002). Partitioning of bacterial communities between sea-water and healthy, black band diseased and dead coral surfaces. Appl Environ Microbiol 68: 2214-2228.
31. Gordon J, Knowlton N, Relman DA, Rohwer F, Youle M. (2013). Superorganisms and holobionts. Microbe 8: 152-153.
32. Grafen A, Ridley M. (2007). Richard Dawkins: How a Scientist Changed the way we Think: Reflections by Scientists, Writers, and Philosophers. Oxford University Press.
33. Guppy R, Bythell JC. (2006). Environmental effects on bacterial diversity in the surface mucus layer of the reef coral Montastraea faveolata. Mar Ecol Prog Ser 328: 133-142.
34. Hong MJ, Yu YT, Chen CA, Chiang PW, Tang SL. (2009). Influence of species specificity and other factors on bacteria associated with the coral Stylophora pistillata in Taiwan. Appl Environ Microbiol 75: 7797-7806.
35. Human Microbiome Project Consortium (2012). Structure, function and diversity of the healthy human micro-biome. Nature 486: 207-214.
36. Kellogg C. (2004). Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273: 81-88.
37. 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.
38. Kimes NE, Johnson WR, Torralba M, Nelson KE, Weil E, Morris PJ. (2013). The Montastraea faveolata micro-biome: ecological and temporal influences on a Caribbean reef-building coral in decline. Environ Microbiol 15: 2082-2094.
39. Kimes NE, Van NostrKimes NE, Van Nostrand JD, Weil E, Zhou J, Morris PJ. (2010). Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ Microbiol 12: 541-556.
40. Klaus JS, Frias-Lopez J, Bonheyo GT, Heikoop JM, Fouke BW. (2005). Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation. Coral Reefs 24: 129-137.
41. Klaus JS, Janse I, Heikoop JM, Sanford RA, Fouke BW. (2007). Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ Microbiol 9: 1291-1305.
42. 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 Progr Ser 314: 119-125.
43. Knowlton N, Rohwer F. (2003). Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162: S51-S62.
44. Kvennefors ECE, 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.
45. Lachnit T, Meske D, Wahl M, Harder T, Schmitz R. (2011). Epibacterial community patterns on marine macro-algae are host-specific but temporally variable. Environ Microbiol 13: 655-665.
46. Lachnit T, Wahl M, Harder T. (2009). Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling 26: 247-255.
47. Lee OO, Yang J, Bougouffa S, Wang Y, Batang Z, Tian R et al. (2012). Spatial and species variations in bacterial communities associated with corals from the Red Sea as revealed by pyrosequencing. Appl Environ Micro-biol 78: 7173-7184.
48. 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.
49. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG. (2004). Discovery of symbiotic nitrogen-fixing cyano-bacteria in corals. Science 305: 997-1000.
50. Li J, Chen Q, Zhang S, Huang H, Yang J, Tian XP et al. (2013). Highly heterogeneous bacterial communities associated with the South China Sea reef corals Porites lutea, Galaxea fascicularis and Acropora millepora. PLoS One 8: e71301.
51. Lins-de-Barros MM, Vieira RP, Cardoso AM, Monteiro VA, Turque AS, Silveira CB et al. (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.
52. Littman RA, Willis BL, 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.
53. Margulis L, Fester R. (1991). Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. MIT Press.
54. Marhaver KL, Edwards RA, Rohwer F. (2008). Viral communities associated with healthy and bleaching corals. Environ Microbiol 10: 2277-2286.
55. McDole T, Nulton J, Barott KL, Felts B, Hand C, Hatay M et al. (2012). Assessing coral reefs on a Pacific-wide scale using the microbialization score. PloS One 7: e43233.
56. McKew BA, Dumbrell AJ, Daud SD, Hepburn L, Thorpe E, Mogensen L et al. (2012). Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp. Appl Environ Microbiol 78: 5229-5237.
57. Moran NA, McCutcheon JP, Nakabachi A. (2008). Geno-mics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
58. 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.
59. Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332: 970-974.
60. 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.
61. Nissimov J, Rosenberg E, Munn CB. (2009). Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292: 210-215.
62. Ochman H, Moran NA. (2001). Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292: 1096-1099.
63. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
64. Raina JB, Tapiolas D, Willis BL, Bourne DG. (2009). Coral-associated bacteria and their role in the biogeochem-ical cycling of sulfur. Appl Environ Microbiol 75: 3492-3501.
65. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E. (2006). The coral probiotic hypothesis. Environ Microbiol 8: 2068-2073.
66. Ritchie KB. (2006). Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Progr Ser 322: 1-14.
67. Rohwer F, Seguritan V, Azam F, Knowlton N. (2002). Diversity and distribution of coral-associated bacteria. Mar Ecol Progr Ser 243: 1-10.
68. 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.
69. Rosenberg E, Zilber-Rosenberg I. (2013). The Hologenome Concept: Human, Animal and Plant Microbiota. Springer: Berlin, Heidelberg, Germany.
70. Rowan R, Knowlton N. (1995). Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci 92: 2850-2853.
71. Rypien KL, Ward JR, Azam F. (2010). Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12: 28-39.
72. Sandin SA, Smith JE, Demartini EE, Dinsdale EA, Donner SD, Friedlander AM et al. (2008). Baselines and degradation of coral reefs in the Northern Line Islands. PloS One 3: e1548.
73. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N et al. (2012). Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6: 564-576.
74. Schöttner S, Wild C, Hoffmann F, Boetius A, Ramette A. (2012). Spatial scales of bacterial diversity in cold-water coral reef ecosystems. PloS One 7: e32093.
75. 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.
76. Siboni N, Ben-Dov E, Sivan A, Kushmaro A. (2012). Geographic specific coral-associated ammonia-oxidizing archaea in the northern Gulf of Eilat (Red Sea). Microb Ecol 64: 18-24.
77. Sunagawa S, Woodley CM, Medina M. (2010). Threatened corals provide underexplored microbial habitats. PLoS One 5: e9554.
78. Sweet MJ, Croquer A, Bythell JC. (2011). Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30: 39-52.
79. Takabayashi M, Carter DA, Loh WKW, Hoegh-Guldberg O. (1998). A coral-specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Mol Ecol 7: 928-930.
80. Taylor MW, Schupp PJ, Dahllöf I, Kjelleberg S, Steinberg PD. (2004). Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6: 121-130.
81. Toller WW, Rowan R, Knowlton N. (2001). Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201: 348-359.
82. Tout J, Jeffries TC, Webster NS, Stocker R, Ralph PJ, Seymour JR. (2014). Variability in microbial community composition and function between different niches within a coral reef. Microb Ecol 67: 540-552.
83. Timmis JN, Ayliffe MA, Huang CY, Martin W. (2004). Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5: 123-135.
84. Tremblay P, Weinbauer MG, Rottier C, Guérardel Y, Nozais C, Ferrier-Pagès C. (2011). Mucus composition and bacterial communities associated with the tissue and skeleton of three scleractinian corals maintained under culture conditions. Mar Biol Assoc UK 91: 649.
85. Vega Thurber RL, 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.
86. Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F et al. (2009). Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148-2163.
87. 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.
88. Yachi S, Loreau M. (1999). Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci 96: 1463-1468.
89. Yang S, Sun W, Zhang F, Li Z. (2013). Phylogenetically diverse denitrifying and ammonia-oxidizing bacteria in corals Alcyonium gracillimum and Tubastraea coccinea. Mar Biotechnol 15: 540-551.
90. Zilber-Rosenberg I, Rosenberg E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32: 723-735.