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Agelas Wasting Syndrome Alters Prokaryotic Symbiont Communities of the Caribbean Brown Tube Sponge, Agelas tubulata

  • Lindsey K. Deignan
  • Joseph R. Pawlik
  • Patrick M. Erwin
Invertebrate Microbiology

Abstract

The brown tube sponge Agelas tubulata (cf. Agelas conifera) is an abundant and long-lived sponge on Caribbean reefs. Recently, a disease-like condition, Agelas wasting syndrome (AWS), was described from A. tubulata in the Florida Keys, where prevalence of the syndrome increased from 7 to 35% of the sponge population between 2010 and 2015. In this study, we characterized the prokaryotic symbiont community of A. tubulata for the first time from individuals collected within the same monitoring plots where AWS was described. We also sampled tissue from A. tubulata exhibiting symptoms of AWS to determine its effect on the diversity and structure of prokaryotic symbiont communities. Bacteria from the phyla Chloroflexi and Proteobacteria, particularly the class Gammaproteobacteria, dominated the sponge microbiome in tissue samples of both healthy sponges and those exhibiting AWS. Prokaryotic community structure differed significantly between the diseased and healthy sponge samples, with greater variability among communities in diseased samples compared to healthy samples. These differences in prokaryotic community structure included a shift in relative abundance of the dominant, ammonia-oxidizing (Thaumarchaeota) symbionts present in diseased and healthy sponge samples. Further research is required to determine the functional consequences of this shift in microbial community structure and the causal relationship of dysbiosis and sponge disease in A. tubulata.

Keywords

Microbiome Porifora Disease Thaumarchaeota Dysbiosis 

Notes

Acknowledgements

The authors thank the staff of the FIU’s Aquarius Reef Base in Key Largo, Florida, for logistical support. Research in the Florida Keys National Marine Sanctuary was performed under permit FKNMS-2012-162.

Funding

This study was funded by grants from the National Science Foundation, Biological Oceanography Program to J.R.P. (OCE-0095724, 0550468, 1029515), and to P.M.E. and J.R.P. (1558580).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

References

  1. 1.
    Hill RT (2004) Microbes from marine sponges: a treasure trove of biodiversity for natural products discovery. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, DC, pp 177–190CrossRefGoogle Scholar
  2. 2.
    Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Webster NS, Taylor M (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346CrossRefPubMedGoogle Scholar
  4. 4.
    Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, Olson JB, Erwin PM, Lopez-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Lopez JV, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Webster NS, Hill RT (2001) The cultural microbial community of the great barrier reef sponge Rhopaloeides odorabile is dominated by an α-proteobacterium. Mar Biol 138:843–851CrossRefGoogle Scholar
  6. 6.
    Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, Heidelberg KB, Egan S, Steinberg PD, Kjelleberg S (2010) Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4:1557–1567CrossRefPubMedGoogle Scholar
  7. 7.
    Rützler K (1988) Mangrove sponge disease induced by cyanobacterial symbionts: failure of a primitive immune system? Dis Aquat Org 5:143–149CrossRefGoogle Scholar
  8. 8.
    Cowart JD, Henkel TP, McMurray SE, Pawlik JR (2006) Sponge orange band (SOB): a pathogenic-like condition of the giant barrel sponge, Xestospongia muta. Coral Reefs 25:513–513CrossRefGoogle Scholar
  9. 9.
    Olson JB, Gochfeld DJ, Slattery M (2006) Aplysina red band syndrome: a new threat to Caribbean sponges. Dis Aquat Org 71:163–168CrossRefPubMedGoogle Scholar
  10. 10.
    Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9:1363–1375CrossRefPubMedGoogle Scholar
  11. 11.
    Maldonado M, Sanchez-Tocino L, Navarro C (2010) Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: epidemic incidence and defense mechanisms. Mar Biol 157:1577–1590CrossRefGoogle Scholar
  12. 12.
    Angermeier H, Glöckner V, Pawlik JR, Lindquist NL, Hentschel U (2012) Sponge white patch disease affecting the Caribbean sponge Amphimedon compressa. Dis Aquat Org 99:95–102CrossRefPubMedGoogle Scholar
  13. 13.
    Sweet M, Bulling M, Cerrano C (2015) A novel sponge disease caused by a consortium of micro-organisms. Coral Reefs 34:871–883CrossRefGoogle Scholar
  14. 14.
    Deignan LK, Pawlik JR (2016) Demographics of the Caribbean brown tube sponge Agelas tubulata on Conch Reef, Florida Keys, and a description of Agelas wasting syndrome (AWS). Proc 13th ICRS, Honolulu, pp 72–4Google Scholar
  15. 15.
    Webster NS, Negri AP, Webb RI, Hill RT (2002) A spongin-boring α-proteobacterium is the etiological agent of disease in the great barrier reef sponge Rhopaloeides odorabile. Mar Ecol Prog Ser 232:305–309CrossRefGoogle Scholar
  16. 16.
    Choudhury JD, Pramanik A, Webster NS, Llewellyn LE, Gachhui R, Mukherjee J (2015) The pathogen of the great barrier reef sponge Rhopaloeides odorabile a new strain of Pseudoalteromonas agarivorans containing abundant and diverse virulence-related genes. Mar Biotechnol 17:463–478CrossRefPubMedGoogle Scholar
  17. 17.
    Angermeier H, Kamke J, Abdelmohsen U, Krohne G, Pawlik J, Lindquist N, Hentschel U (2011) The pathology of sponge orange band disease affecting the Caribbean barrel sponge Xestospongia muta. FEMS Microbiol Ecol 75:218–230CrossRefPubMedGoogle Scholar
  18. 18.
    Olson JB, Thacker RW, Gochfeld DJ (2014) Molecular community profiling reveals impacts of time, space, and disease status on the bacterial community associated with the Caribbean sponge Aplysina cauliformis. FEMS Microbiol Ecol 87:268–279CrossRefPubMedGoogle Scholar
  19. 19.
    Blanquer A, Uriz MJ, Cebrian E, Galand PE (2016) Snapshot of a bacterial microbiome shift during the early symptoms of a massive sponge die-off in the western Mediterranean. Front Microbiol 7.  https://doi.org/10.3389/fmicb.2016.00752
  20. 20.
    Vayssier-Taussat M, Albina E, Citti C, Cosson J-F, Jacques M-A, Lebrun MH, Le Loir Y, Ogliastro M, Petit M-A, Roumagnac P, Candresse T (2014) Shifting the paradigm from pathogens to pathobiome: new concepts in the light of meta-omics. Front Cell Infect Microbiol 4:29.  https://doi.org/10.3389/fcimb.2014.00029CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Sweet M, Bulling M (2017) On the importance of the microbiome and pathobiome in coral health and disease. Front Mar Sci 4:9.  https://doi.org/10.3389/fmars.2017.00009CrossRefGoogle Scholar
  22. 22.
    Loh T-L, Pawlik JR (2014) Chemical defenses and resource trade-offs structure sponge communities on Caribbean coral reefs. Proc Natl Acad Sci USA 111:4151–4156CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish: I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194CrossRefGoogle Scholar
  24. 24.
    Assmann M, Lichte E, Pawlik JR, Köck M (2000) Chemical defenses of the Caribbean sponges Agelas wiedenmayeri and Agelas conifera. Mar Ecol Prog Ser 207:255–262CrossRefGoogle Scholar
  25. 25.
    Richelle-Maurer E, De Kluijver MJ, Feio S, Gaudêncio S, Gaspar H, Gomez R, Tavares R, Van de Vyver G, Van Soest RWM (2003) Localization and ecological significance of oroidin and sceptrin in the Caribbean sponge Agelas conifera. Biochem Syst Ecol 31:1073–1091CrossRefGoogle Scholar
  26. 26.
    Gloeckner V, Wehrl M, Moitinho-Silva L, Gernert C, Schupp P, Pawlik JR, Lindquist NL, Erpenbeck D, Wörheide G, Hentschel U (2014) The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biol Bull 227:78–88CrossRefPubMedGoogle Scholar
  27. 27.
    Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microbiol 74:7694–7708CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522CrossRefPubMedGoogle Scholar
  29. 29.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787CrossRefGoogle Scholar
  32. 32.
    White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5:e1000352CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  34. 34.
    López-Legentil S, Erwin PM, Pawlik JR, Song B (2010) 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 60:561–571CrossRefPubMedGoogle Scholar
  35. 35.
    Gao Z-M, Wang Y, Tian R-M, Lee OO, Wong YH, Batang ZB, Al-Suwailem A, Lafi FF, Bajic VB, Qian P-Y (2015) Pyrosequencing revealed shifts of prokaryotic communities between healthy and disease-like tissues of the Red Sea sponge Crella cyathophora. Peer J 3:e890.  https://doi.org/10.7717/peerj.890CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252CrossRefPubMedGoogle Scholar
  37. 37.
    Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 4:300–306CrossRefGoogle Scholar
  38. 38.
    Radax R, Hoffmann F, Rapp HT, Leininger S, Schleper C (2012) Ammonia-oxidizing Archaea as main drivers of nitrification in cold-water sponges. Environ Microbiol 14:909–923CrossRefPubMedGoogle Scholar
  39. 39.
    Zhang F, Pita L, Erwin PM, Abaid S, López-Legentil S, Hill RT (2014) Symbiotic archaea in marine sponges show stability and host specificity in community structure and ammonia oxidation functionality. FEMS Microbiol Ecol 90:699–707CrossRefPubMedGoogle Scholar
  40. 40.
    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 3:512–521CrossRefPubMedGoogle Scholar
  41. 41.
    Witt V, Wild C, Anthony KR, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the great barrier reef. Environ Microbiol 13:2976–2989CrossRefPubMedGoogle Scholar
  42. 42.
    Olson JB, Gao X (2013) Characterizing the bacterial associates of three Caribbean sponges along a gradient from shallow to mesophotic depths. FEMS Microbiol Ecol 85:74–84CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology and Marine Biology, Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA

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