Skip to main content
SpringerLink
Log in

Sponge and Coral Microbiomes

  • Chapter
  • First Online:
Symbiotic Microbiomes of Coral Reefs Sponges and Corals

Abstract

Coral/sponge holobiont is the stable assemblage of the host and its symbiotic bionts, e.g., microalgae, bacteria, archaea, virus, fungi, and protists. Coral/sponge microbiome means the entire microbial community and genes that reside within a coral/sponge. Sponges host abundant and diverse microbes including bacteria, archaea, and fungi. Corals form a close mutualistic relationship with photosynthetic, endosymbiotic dinoflagellates of the genus Symbiodinium, along with microorganisms including bacteria, archaea, fungi, and viruses. These microbiota and algae are thought to have various symbiotic relationships with coral/sponge host including mutualism, commensalism, and parasitism.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Lederberg J, McCray AT. Ome sweet omics – a genealogical treasury of words. Scientist. 2001;15:8.

    Google Scholar 

  2. Margulis L, Fester R. Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. Cambridge, MA: MIT Press; 1991.

    Google Scholar 

  3. Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun. 2016;7:11870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Moitinho-Silva L, Nielsen S, Amir A, Gonzalez A, Ackermann GL, Cerrano C, et al. The sponge microbiome project. GigaScience. 2017;6:1–7.

    Article  CAS  PubMed  Google Scholar 

  5. He L, Liu F, Karuppiah V, Ren Y, Li Z. Comparisons of the fungal and protistan communities among different marine sponge holobionts by pyrosequencing. Microb Ecol. 2014;67:951–61.

    Article  PubMed  Google Scholar 

  6. Li Z, Wang Y, Li J, Liu F, He L, He Y, Wang S. Metagenomic analysis of genes encoding nutrient cycling pathways in the microbiota of deep-sea and shallow-water sponges. Mar Biotechnol. 2016;18:659–71.

    Article  CAS  Google Scholar 

  7. Webster NS, Negri AP, Munro MM, Battershill CN. Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol. 2004;6:288–300.

    Article  PubMed  Google Scholar 

  8. Lee OO, Wang Y, Yang J, Lafi FF, Al-Suwailem A, Qian PY. Pyrosequencing reveals highly diverse and species specific microbial communities in sponges from the Red Sea. ISME J. 2011;5:650–64.

    Article  CAS  PubMed  Google Scholar 

  9. Pape T, Hoffmann F, Quéric NV, Juterzenka JR, Michaelis W. Dense populations of Archaea associated with the demosponge Tentorium semisuberites Schmidt, 1870, from Arctic deepwaters. Polar Biol. 2006;29:662–7.

    Article  Google Scholar 

  10. Holmes B, Blanch H. Genus-specific associations of marine sponges with group I crenarchaeotes. Mar Biotechnol. 2007;150:759–72.

    Google Scholar 

  11. Wilkinson CR. Microbial associations in sponges. I. Ecology, physiology and microbial populations of coral reef sponges. Mar Biol. 1978;49:161–7.

    Article  Google Scholar 

  12. Magnino G, Sarà A, Lancioni T, Gaino E. Endobionts of the coral reef sponge Theonella swinhoei (Porifera, Demospongiae). Invertebr Biol. 1999;118:213–20.

    Article  Google Scholar 

  13. Yu Z, Zhang B, Sun W, Zhang F, Li Z. Phylogenetically diverse endozoic fungi in the South China Sea sponges and their potential in synthesizing bioactive natural products suggested by PKS gene and cytotoxic activity analysis. Fungal Divers. 2013;58:127–41.

    Article  Google Scholar 

  14. Zhou K, Zhang X, Zhang F, Li Z. Phylogenetically diverse cultivable fungal community and polyketide synthase (PKS), non-ribosomal peptide synthase (NRPS) genes associated with the South China Sea sponges. Microb Ecol. 2011;62:644–54.

    Article  PubMed  Google Scholar 

  15. Ding B, Yin Y, Zhang F, Li Z. Recovery and phylogenetic diversity of culturable fungi associated with marine sponges Clathrina luteoculcitella and Holoxea sp. in the South China Sea. Mar Biotechnol. 2011;13:713–21.

    Article  CAS  Google Scholar 

  16. Richardson C, Hill M, Marks C, RunyenJanecky L, Hill A. Experimental manipulation of sponge/bacterial symbiont community composition with antibiotics: sponge cell aggregates as a unique tool to study animal/microorganism symbiosis. FEMS Microbiol Ecol. 2012;81:407–18.

    Article  CAS  PubMed  Google Scholar 

  17. Sipkema D, Schippers K, Maalcke WJ, Yang Y, Salim S, Blanch HW. Multiple approaches to enhance the cultivability of bacteria associated with the marine sponge Haliclona (gellius) sp. Appl Environ Microbiol. 2011;77:2130–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Li Z-Y, He L-M, Wu J, Jiang Q. Bacterial community diversity associated with four marine sponges from the South China Sea based on 16S rDNA-DGGE fingerprinting. J Exp Mar Biol Ecol. 2006;329:75–85.

    Article  CAS  Google Scholar 

  19. Ridley CP, Faulkner DJ, Haygood MG. Investigation of Oscillatoria spongeliae-dominated bacterial communities in four dictyoceratid sponges. Appl Environ Microbiol. 2005;71:7366–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA. 2006;103:12115–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Taylor MW, Radax R, Steger D, Wagner M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev. 2007;71:295–347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wilkinson CR. Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges. Proc R Soc. 1984;220:509–17.

    Article  Google Scholar 

  23. Thomas T, Rusch D, Demaere MZ, Yung PY, Lewis M, Halpern A, et al. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 2010;4:1557–67.

    Article  CAS  PubMed  Google Scholar 

  24. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, et al. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol. 2002;68:4431–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 2012;6:564–76.

    Article  CAS  PubMed  Google Scholar 

  26. Sharp KH, Eam B, Faulkner DJ, Haygood MG. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol. 2007;73:622–9.

    Article  CAS  PubMed  Google Scholar 

  27. Preston CM, Wu KY, Molinski TF, Delong EF. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA. 1996;93:6241–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Radax R, Hoffmann F, Rapp TR, Leninger S, Schleper C. Ammonia-oxidising Archaea as main drivers of nitrification in cold-water sponges. Environ Microbiol. 2012;14:909–23.

    Article  CAS  PubMed  Google Scholar 

  29. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M, et al. Diversity and mode of transmission of ammonia oxidising Archaea in marine sponges. Environ Microbiol. 2008;10:1087–94.

    Article  CAS  PubMed  Google Scholar 

  30. Yang Z, Li Z. Spatial distribution of prokaryotic symbionts and ammoxidation, denitrifier bacteria in marine sponge Astrosclera willeyana. Sci Rep. 2012;2:528.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Li Z-Y, Wang Y-Z, He L-M, Zheng H-J. Metabolic profiles of prokaryotic and eukaryotic communities in deep-sea sponge Neamphius huxleyi indicated by metagenomics. Sci Rep. 2014;4:3895.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Jin L, Liu F, Sun W, Zhang F, Karuppiah V, Li Z. Pezizomycotina dominates the fungal communities of South China sea sponges Theonella swinhoei and Xestospongia testudinaria. FEMS Microbiol Ecol. 2014;90:935–45.

    Article  CAS  PubMed  Google Scholar 

  33. Karuppiah V, Li Y, Sun W, Feng G, Li Z. Functional gene-based discovery of phenazines from the Actinobacteria associated with marine sponges in the South China Sea. Appl Microbiol Biotechnol. 2015;99:5939–50.

    Article  CAS  PubMed  Google Scholar 

  34. Sun W, Zhang F, He L, Loganathan K, Li Z. Actinomycetes from the South China Sea sponges: isolation, diversity and potential for aromatic polyketides discovery. Front Microbiol. 2015;6:1048.

    PubMed  PubMed Central  Google Scholar 

  35. Zhao H-Y, Anbuchezhian R, Sun W, Shao C-L, Zhang F-L, Yin Y, et al. Cytotoxic nitrobenzoyloxy-substituted sesquiterpenes from sponge derived endozoic fungus Aspergillus insulicola MD10-2. Curr Pharm Biotechnol. 2016;17:271–4.

    Article  CAS  PubMed  Google Scholar 

  36. Li Z. Advances in marine microbial symbionts in the China Sea and related pharmaceutical metabolites. Mar Drugs. 2009;7:113–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Thomas T, Rusch D, DeMaere MZ, Yun PY, Lewis M, Halpern A, et al. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 2010;4:1557–67.

    Article  CAS  PubMed  Google Scholar 

  38. Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T. Metaproteogenomic analysis of a community of sponge symbionts. ISME J. 2012;6:1515–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, et al. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci USA. 2012;109:E1878–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Trindade-Silva AE, Rua C, Silva GGZ, Dutilh BE, Moreira Ana PB, Edwards RA. Taxonomic and functional microbial signatures of the endemic marine sponge Arenosclera brasiliensis. PLoS One. 2012;7:e39905.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, et al. Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol. 2009;11:2228–43.

    Article  CAS  PubMed  Google Scholar 

  42. Schlappy ML, Schottner SI, Lavik G, Kuypers MMM, de Beer D, Hoffmann F. Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol. 2010;157:593–602.

    Article  PubMed  Google Scholar 

  43. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, et al. Single cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 2011;5:61–70.

    Article  PubMed  Google Scholar 

  44. Mohamed NM, Saito K, Tal Y, Hill RT. Diversity of aerobic and anaerobic ammonia oxidizing bacteria in marine sponges. ISME J. 2010;4:38–48.

    Article  CAS  PubMed  Google Scholar 

  45. Han M, Li Z, Zhang F. The ammonia oxidizing and denitrifying prokaryotes associated with sponges from different sea areas. Microb Ecol. 2013;66:427–36.

    CAS  PubMed  Google Scholar 

  46. Han M, He L, Li Z, Lin H. Bacterial and archaeal symbionts in the South China Sea sponge Phakellia fusca: community structure, relative abundance, and ammonia-oxidizing populations. Mar Biotechnol. 2012;14:701–13.

    CAS  Google Scholar 

  47. Zhang D, Sun W, Feng G, Zhang F, Anbuchezhian R, Li Z, et al. Phylogenetic diversity of sulfate-reducing desulfovibrio associated with three South China Sea sponges. Lett Appl Microbiol. 2015;60:504–12.

    Article  CAS  PubMed  Google Scholar 

  48. López-Legentil S, Erwin PM, Pawlik JR, Song B. Effects of sponge bleaching on ammonia-oxidizing Archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongia muta. Microb Ecol. 2010;60:561–71.

    Article  PubMed  Google Scholar 

  49. Su J, Jin L, Jiang Q, Sun W, Zhang F, Li Z. Phylogenetically diverse ureC genes and their expression suggest the urea utilization by bacterial symbionts in marine sponge Xestospongia testudinaria. PLoS One. 2013;8:e64848.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Feng G, Sun W, Zhang F, Karthik L, Li Z. Inhabitancy of active Nitrosopumilus-like ammonia oxidizing archaea and Nitrospira nitrite-oxidizing bacteria in the sponge Theonella swinhoei. Sci Rep. 2016;6:24966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Engel S, Jensen PR, Fenical W. Chemical ecology of marine microbial defense. J Chem Ecol. 2002;2(8):1971–85.

    Article  Google Scholar 

  52. Walters KD, Pawlik JR. Is there a trade-off between wound-healing and chemical defenses among Caribbean reef sponges? Integr Comp Biol. 2005;45:352–8.

    Article  PubMed  Google Scholar 

  53. Green G. Ecology of toxicity in marine sponges. Mar Biol. 1977;40:207–15.

    Article  Google Scholar 

  54. Thoms C, Ebel R, Proksch P. Activated chemical defense in Aplysina sponges revisited. J Chem Ecol. 2006;32:97–123.

    Article  CAS  PubMed  Google Scholar 

  55. Koopmans M, Martens D, Wijffels RH. Towards commercial production of sponge medicines. Mar Drugs. 2009;7:787–802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Piel J. Metabolites from symbiotic bacteria. Nat Prod Rep. 2009;26:338–62.

    Article  CAS  PubMed  Google Scholar 

  57. Unson MD, Holland ND, Faulkner DJ. A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar Biol. 1994;119:1–11.

    Article  CAS  Google Scholar 

  58. Bewley CA, Holland ND, Faulkner DJ. Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia. 1996;52:716–22.

    Article  CAS  PubMed  Google Scholar 

  59. Piel J, Hui D, Wen G, Butzke D, Platzer M, Fusetani N, et al. Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc Natl Acad Sci U S A. 2004;101:16222–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wilson MC, Mori T, Rückert C, Uria AR, Helf MJ, Takada K, et al. An environmental bacterial taxon with a large and distinct metabolic repertoire. Nature. 2014;506:58–62.

    Article  CAS  PubMed  Google Scholar 

  61. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol. 2007;9:2707–19.

    Article  CAS  PubMed  Google Scholar 

  62. Bourne DG, Morrow KM, Webster NS. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol. 2016;70:317–40.

    Article  CAS  PubMed  Google Scholar 

  63. Roder C, Bayer T, Aranda M, Kruse M, Voolstra CR. Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol Ecol. 2015;24:3501–11.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Wild C, Voolstra CR. Dominance of endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol Evol. 2018;8:2240–52.

    PubMed  PubMed Central  Google Scholar 

  65. Ceh J, Kilburn MR, Cliff JB, Raina J, van Keulen M, Bourne DG. Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol Evol. 2013;3:2393–400.

    Article  Google Scholar 

  66. Raina J-B, Dinsdale E, Willis BL, Bourne DG. Do organic sulphur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol. 2010;18:101–8.

    Article  CAS  PubMed  Google Scholar 

  67. Gilbert JA, Thomas S, Cooley NA, Kulakova A, Field D, et al. Potential for phosphonoacetate utilization by marine bacteria in temperate coastal waters. Environ Microbiol. 2009;11:111–25.

    Article  CAS  PubMed  Google Scholar 

  68. Yang S-H, Lee STM, Huang C-R, Tseng C-H, Chiang P-W, Chen C-P, et al. Prevalence of potential nitrogen-fixing, green sulfur bacteria in the skeleton of reef-building coral Isopora palifera. Limnol Oceanogr. 2016;61:1078–86.

    Article  Google Scholar 

  69. Siboni N, Ben-Dov E, Sivan A, Kushmaro A. Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol. 2008;10:2979–90.

    Article  CAS  PubMed  Google Scholar 

  70. Wood-Charlson EM, Weynberg KD, Suttle CA, Roux S, van Oppen MJH. Metagenomic characterization of viral communities in corals: mining biological signal from methodological noise. Environ Microbiol. 2015;17:3440–9.

    Article  PubMed  Google Scholar 

  71. Sogin EM, Putnam HM, Nelson CE, Anderson P, Gates RD. Correspondence of coral holobiont metabolome with symbiotic bacteria, archaea and Symbiodinium communities. Environ Microbiol Rep. 2017;9:310–5.

    Article  PubMed  Google Scholar 

  72. Glasl B, Herndl GJ, Frade PR. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 2016;10:2280–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Prosser JI, Bohannan BJM, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, et al. The role of ecological theory in microbial ecology. Nat Rev Microbiol. 2007;5:384–92.

    Article  CAS  PubMed  Google Scholar 

  74. Ainsworth TD, Thurber RV, Gates RD. The future of coral reefs: a microbial perspective. Trends Ecol Evol. 2009;25:233–44.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge financial supports from the National Natural Science Foundation of China (NSFC) (31861143020, 41776138, 41742002, U1301131, 41176127, 41076077), the National High-Tech Research and Development Program of China (2013AA092901, 2011AA090702, 2007AA09Z447, 2004AA628060, 2002AA608080), and the National Major Scientific Research Program of China (2013CB956103).

Author information

Authors and Affiliations

  1. Marine Biotechnology Laboratory, State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China

    Zhiyong Li

Authors
  1. Zhiyong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhiyong Li .

Editor information

Editors and Affiliations

  1. Marine Biotechnology Laboratory, State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China

    Zhiyong Li

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature B.V.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Li, Z. (2019). Sponge and Coral Microbiomes. In: Li, Z. (eds) Symbiotic Microbiomes of Coral Reefs Sponges and Corals. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-1612-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation