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A novel sponge disease caused by a consortium of micro-organisms

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Abstract

In healthy sponges, microbes have been shown to account for up to 40 % of tissues. The majority of these are thought to originate from survivors evading digestion and immune responses of the sponge and growing and residing in the microenvironments of the mesophyll. Although a large percentage of these microbes are likely commensals, they may also include potentially pathogenic agents, which under specific conditions, such as temperature stress, may cause disease. Here we report a novel disease (sponge necrosis syndrome) that is severely affecting populations of the sponge Callyspongia (Euplacella) aff biru. Both ITS fungal and 16S rDNA bacterial diversities were assessed in healthy and diseased individuals, highlighting six potential primary causal agents for this new disease: two bacteria, a Rhodobacteraceae sp. and a cyanobacterium, Hormoscilla spongeliae (formally identified as Oscillatoria spongeliae), and four fungi, a Ascomycota sp., a Pleosporales sp., a Rhabdocline sp., and a Clasosporium sp. Furthermore, histological analysis showed the dominance of fungal hyphae rather than bacteria throughout the disease lesion, which was absent or rare in healthy tissues. Inoculation trails showed that only a combination of one bacterium and one fungus could replicate the disease, fulfilling Henle–Koch’s postulates and showing that this sponge disease is caused by a poly-microbial consortium.

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References

  • Aly AH, Debbad A, Proksch P (2011) Fifty years of drug discovery from fungi. Fungal Divers 50:3–19

    Article  Google Scholar 

  • Angermeier H, Glöckner V, Pawlik J, Lindquist N, Hentschel U (2012) Sponge white patch disease affecting the Caribbean sponge Amphimedon compressa. Dis Aquat Organ 99:95

    Article  CAS  PubMed  Google Scholar 

  • Bjorndahl L, Soderlund I, Kvist U (2003) Evaluation of the one-step eosin-nigrosin staining technique for human sperm vitality assessment. Hum Reprod 18:813–816

    Article  CAS  PubMed  Google Scholar 

  • Bungni BD, Ireland CM (2004) Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat Prod Rep 21:143–163

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

  • Cerrano C, Bavestrello G (2009) Massive mortalities and extinctions. In: Wahl M (ed) Marine hard bottom communities. Springer-Verlag, Berlin Heidelberg, pp 295–307

    Chapter  Google Scholar 

  • Cervino JM, Winiarski-Cervino K, Polson SW, Goreau T, Smith GW (2006) Identification of bacteria associated with a disease affecting the marine sponge Ianthella basta. New Britain, Papua New Guinea. Mar Ecol Prog Ser 324:139–150

  • 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

  • Debbab A, Aly AH, Proksch P (2011) Bioactive secondary metabolites from endophytes and associated marine derived fungi. Fungal Divers 49:1–12

    Article  Google Scholar 

  • 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. J Appl Environ Microbiol 72:3724–3732

    Article  CAS  Google Scholar 

  • Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum “Poribacteria” in marine sponges. J Appl Envion Microbiol 70:3724–3732

    Article  CAS  Google Scholar 

  • Gaino E, Pronzato R, Corriero G, Buffa P (1992) Mortality of commercial sponges: incidence in two Mediterranean areas. Ital J Zool 59:79–85

    Google Scholar 

  • Galstoff PS (1942) Wasting disease causing mortality of sponges in the West Indies and Gulf of Mexico. Proceeding of the 8th American Scientific Congress 3:411-421

  • Hinde R, Pironet F, Borowitzka MA (1994) Isolation of Oscillatoria spongeliae, the filamentous cyanobacterial symbiont of the marine sponge Dysidea herbacea. Mar Biol 1:99–104

    Article  Google Scholar 

  • Hoegh-Guldberg O (2004) Coral reefs in a century of rapid environmental change symbiosis. Symbiosis 37:1–31

    Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Huang A, Li J-W, Shen Z-Q, Wang X-W, Jin M (2006) High-throughput identification of clinical pathogenic fungi by hybridization to an oligonucleotide microarray. J Clin Microbiol 44:3299–3305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Imhoff JF, Truper HG (1976) Marine sponges as habitats of anaerobic phototrophic bacteria. Microb Ecol 3:1–9

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Wang G (2009) Diversity of fungal isolates from three Hawaiian marine sponges. Microbiol Res 164:233–241

    Article  CAS  PubMed  Google Scholar 

  • Luter HM, Whalan S, Webster NS (2012) The marine sponge Ianthella basta can recover from stress-induced tissue regression. Hydrobiologia 687(1):227–235

  • Miller AW, Richardson LL (2014) Emerging coral diseases: a temperature-driven process? Mar Ecol. doi:10.1111/maec.12142

    Google Scholar 

  • Olson JB, Gochfeld DJ, Slattery M (2006) Aplysina red band syndrome: a new threat to Caribbean sponges. Dis Aquat Org 71:163–168

    Article  CAS  PubMed  Google Scholar 

  • Osinga R, Armstrong E, Burgess JG, Hoffmann F, Reitner J, Schumann-Kindel G (2001) Sponge-microbe associations and their importance for sponge bioprocess engineering. Hydrobiologia 461:55–62

    Article  Google Scholar 

  • Oksanen J (2013) Vegan: ecological diversity. Available at http://cran.rproject.org/web/packages/vegan/vignettes/diversity-vegan.pdf

  • Penesyan A, Tebben J, Lee M, Thomas T, Kjelleberg S, Harder T, Egan S (2011) Identification of the antibacterial compound produced by the marine epiphytic bacterium Pseudovibrio sp. D323 and related sponge-associated bacteria. Mar Drugs 9:1391–1402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peters EC (1997) Diseases of coral reef organisms. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp 114–139

  • R Core Team (2014) R: A language and environment for statistical computing. (3.0.3) [Computer software].Vienna, Austria: Foundation for Statistical Computing. Available at http://www.R-project.org/

  • Rüetzler K (1988) Mangrove sponge disease induced by cyanobacterial symbionts: failure of a primitive immune system? Dis Aquat Org 5:143–149

    Article  Google Scholar 

  • Sanchez O, Gasol JM, Massana R, Mas J, Pedros-Alio C (2007) Comparison of different denaturing gradient gel electrophoresis primer sets for the study of marine bacterioplankton communities. Appl Environ Microbiol 73:5962–5967

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schippers A, Neretin LN, Kallmeyer J, Ferdelman TG, Cragg BA, Parkes RJ, Jørgensen BB (2005) Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433:861–864

    Article  CAS  PubMed  Google Scholar 

  • Smith FW (1941) Sponge disease in British Honduras, and its transmission by water currents. Ecology 22:415–421

    Article  Google Scholar 

  • Sweet MJ, Bythell J (2012) Ciliate and bacterial communities associated with White Syndrome and Brown Band Disease in reef building corals. Environ Microbiol 14:2184–2199

    Article  PubMed Central  PubMed  Google Scholar 

  • Sweet MJ, Croquer A, Bythell JC (2010) Temporal and spatial patterns in waterborne bacterial communities of an island reef system. Aquat Microb Ecol 61:1–11

    Article  Google Scholar 

  • Sweet MJ, Croquer A, Bythell JC (2011) Development of bacterial biofilms on artificial corals in comparison to surface-associated microbes of hard corals. PLoS One 6:e21195

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sweet M, Croquer A, Bythell J (2014) Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis. Proc Roy Soc B Biol Sci 281:20140094

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thirunavukkarasu N, Suryanarayanan TS, Girivasan KP, Venkatachalam A, Geetha V, Ravishankar JP, Doble M (2012) Fungal symbionts of marine sponges from Rameswaram, southern India: species composition and bioactive metabolites. Fungal Divers 55:37–46

    Article  Google Scholar 

  • Vacelet J (1975) Electron microscope study of the association between bacteria and sponges of the genus Verongia (Dictyoceratida). J Exp Mar Bio Ecol 23:271–288

    Google Scholar 

  • Vacelet J, Vacelet E, Gaino E, Gallissian M-F (1994) Bacterial attack of spongin skeleton during the 1986–1990 Mediterranean sponge disease. In: van Kempen TMG, Braekman JC (eds) van Soest RWM. Sponges in time and space Balkema, Rotterdam, pp 355–362

    Google Scholar 

  • Voogd NJD (2004) Callyspongia (Euplacella) biru spec. nov. (Porifera: Demospongiae: Haplosclerida) from Indonesia. Zool Meded 78:477–483

    Google Scholar 

  • Wang G, Li Q, Zhu P (2008) Phylogenetic diversity of culturable fungi associated with the Hawaiian sponges Suberites zeteki and Gelliodes fibrosa. Antonie Leeuwenhoek 93:163–174

    Article  PubMed  Google Scholar 

  • Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9:1363–1375

    Article  CAS  PubMed  Google Scholar 

  • Webster NS, Blackall LL (2009) What do we really know about sponge-microbial symbioses? ISME J 3:1–3

    Article  CAS  PubMed  Google Scholar 

  • Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346

    Article  CAS  PubMed  Google Scholar 

  • Webster NS, Cobb RE, Negri AP (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2:830–842

    Article  CAS  PubMed  Google Scholar 

  • Webster NS, Negri AP, Webb RI, Hill RT (2002) A spongin-boring alpha proteobacterium is the etiological agent of disease in the Great Barrier Reef sponge, Rhopaloeides odorabile. Mar Ecol Prog Ser 232:305–309

    Article  Google Scholar 

  • Weisz JB, Lindquist N, Martens CS (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 155:367–376

    Article  PubMed  Google Scholar 

  • Wulff JL (2006) Ecological interactions of marine sponges. Can J Zool 84:146–166

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Korallion Lab for allowing us to conduct the work at the research station. Field activities were partially funded by an Internationalization Grant from Polytechnic University of Marche. We also wish to thank Barbara Calcinai and Azzurra Bastari for their assistance in sponge identification.

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Authors and Affiliations

  1. Molecular Health and Disease Laboratory, College of Life and Natural Sciences, University of Derby, Derby, DE22 1GB, UK

    Michael Sweet & Mark Bulling

  2. Dipartimento di Scienze della Vita e dell’Ambiente - DiSVA, Università Politecnica delle Marche, Via Brecce Bianche, 60131, Ancona, Italy

    Carlo Cerrano

Authors
  1. Michael Sweet
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  2. Mark Bulling
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  3. Carlo Cerrano
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Correspondence to Michael Sweet.

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Communicated by Biology Editor Dr. Mark Vermeij

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Sweet, M., Bulling, M. & Cerrano, C. A novel sponge disease caused by a consortium of micro-organisms. Coral Reefs 34, 871–883 (2015). https://doi.org/10.1007/s00338-015-1284-0

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