Skip to main content
SpringerLink
Log in

Florida reef sponges harbor coral disease-associated microbes

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Sponges can filter large volumes of seawater and accumulate highly diverse and abundant microbial communities within their tissue. Culture-independent techniques such as fluorescent in situ hybridization (FISH), 16S small subunit (SSU) rRNA gene analyses, and transmission electron microscopy (TEM) were applied to characterize the presence and distribution of microbes within sponges abundant on south Florida reefs. This study found that coral disease-associated bacteria (CDAB) are harbored within Agelas tubulata and Amphimedon compressa. FISH probes detected several potential bacterial pathogens such as Aurantimonas coralicida, Cytophaga sp., Desulfovibrio spp, Serratia marcescans, and Vibrio mediterranei within A. compressa and A. tubulata host sponges. Spatial differences in the distribution of targeted bacteria were seen within sponge hosts. Transmission electron microscopy of A. compressa indicated there was a higher concentration of bacteria in the choanosome compared to the ectosome. These observed spatial distributions support the presence of internal sponge niches, which could play a role in the location of the CDAB within the sponges.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acropora Coral Conservation/Restoration Workshop (2009) National Zoo, Washington DC, November 11–13

  • Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770

    Google Scholar 

  • Boury-Esnault N, Rützler K (1997) Thesaurus of terms for sponge morphology. Smithson. Contributions to Zool. 596: Smithsonian Press, Washington, pp 1–55

  • Cole J, Chai B, Farris R, Wang Q, Kulam-Syed-Mohideen A, McGarrell D, Bandela A, Cardenas E, Garrity G, Tiedje J (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. doi:10.1093/nar/gkl889

    Google Scholar 

  • Cooney R, Pantos O, Le Tissler M, Barer M, O’Donnell A, Bythell J (2002) Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ Microbiol 4:401–413

    Article  PubMed  Google Scholar 

  • Cottrell M, Kirchman D (2000) Community composition of marine bacterioplankton determined by 16s rRNA gene clone libraries and fluorescence in situ hybridization. Appl Environ Microbiol 66(12):5116–5122

    Article  PubMed  CAS  Google Scholar 

  • Cypionka H (2000) Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54:837–848

    Article  Google Scholar 

  • Dar SA, Yao L, van Dongen U, Kuenen JG, Muyzer G (2007) Analysis of diversity and activity of sulfate-reducing bacterial communities in sulfidogenic bioreactors using 16S rRNA and dsrB genes as molecular markers. Appl Environ Microbiol 73:594–604

    Google Scholar 

  • Denner EBM, Smith GW, Busse HJ, Schumann P, Narzt T, Polson SW, Lubitz W, Richardson LL (2003) Aurantimonas coralicida gen. nov., sp. nov., the causative agent of white plague type II on Caribbean scleractinian corals. Int J Syst Evol Microbiol 53:1115–1122

    Article  PubMed  CAS  Google Scholar 

  • Fieseler L, Horn M, Wagner M, Hentschel U (2006) Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Appl Environ Microbiol 70:3724–3732

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Friedrich AB, Merkert H, Fendert T, Hacker J et al (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol 134:461–470

    Article  Google Scholar 

  • Galeano E, Martínez A (2009) Antimicrobial activity of marine sponges from Urabá Gulf, Colombian Caribbean region. Eur J Org Chem 13:2112–2119

    Google Scholar 

  • Hanley JA, Negassa A, Edwardes MD, Forrester JE (2003) Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 157:364–375

    Article  PubMed  Google Scholar 

  • Harvell CD, Kim K, Colwell BJM, RR EPR et al (1999) Emerging marine diseases-climate links and anthropogenic factors. Sci 285:1505–1510

    Article  CAS  Google Scholar 

  • Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440

    Article  PubMed  CAS  Google Scholar 

  • Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. In: Müller WEG (ed) Molecular marine biology of sponges. Springer Verlag, Heidelberg, pp 60–88

    Google Scholar 

  • Hill M, Hill A, Lopez N, Harriott O (2006) Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Mar Biol 148:1221–1230

    Article  Google Scholar 

  • Hoffman T, Larsen O, Thiel V, Rapp HT, Pape T, Michaelis W, Reitner J (2005) An anaerobic world in sponges. Geomicrobiol J 22:1–10

    Article  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg Hoegh-Guldberg RO, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Pandolfi PSR, JM RB, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Sci 301:929–933

    Article  CAS  Google Scholar 

  • Israely T, Banin E, Rosenberg E (2001) Growth, differentiation and death of Vibrio shiloi. Coral tissue as a function of seawater temperature. Aquat Microb Ecol 24:1–8

    Article  Google Scholar 

  • Kaczmarsky LT, Draudi M, Williams EH (2005) Is there a relationship between proximity of sewage effluent and the prevalence of coral diseases? Caribb J Sci 41:124–137

    Google Scholar 

  • Kefalas E, Castritsi-Catharios J, Miliou H (2003) Bacteria associated with the sponge Spongia officinalis as indicators of contamination. Ecol Indic 2:339–343

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Krekeler D, Teske A, Cypionka H (1997) Strategies of sulfate-reducing bacteria to escape oxygen stress in a cyanobacterial mat. FEMS Microbiol Ecol 25:89–96

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Li CW, Chen JY, Hua TA (1998) Precambrian sponges with cellular structures. Sci 143:739–748

    Google Scholar 

  • Lopez JV, McCarthy PJ, Janda KE, Willoughby R, Pomponi SA (1999) Molecular techniques reveal wide phyletic diversity of heterotrophic microbes associated with the sponge genus Discodermia (Porifera:Demospongiae). Proc 5th International Sponge Symposium. Mem Queensl Mus 44:329–341

    Google Scholar 

  • Lopez JV, Ranzer L, Ledger A, Schoch B, Duckworth A, McCarthy PJ, Kerr RG (2010) Comparison of bacterial diversity within the coral reef sponge, Axinella corrugata, and the encrusting coral Erythropodium caribaeorum and adjacent environmental samples. Proc. 11th ICRS 1355–1359

  • Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP, Bradley AS, Kelly AE, Bhatia M, Meredith W, Snape CE, Bowring SA, Condon DJ, Summons RE (2009) Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457:718–722

    Article  PubMed  CAS  Google Scholar 

  • Loy A, Maixner F, Wagner M, Horn M (2007) probeBase--an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res 35(Database issue):D800–D804

    Google Scholar 

  • Maldonado M (2007) Intergenerational transmission of symbiotic bacteria in oviparous and viviparous demosponges, with emphasis on intracytoplasmically compartmented bacterial types. J Mar Biol Assoc UK 87:1701–1713

    Article  Google Scholar 

  • Meier H, Amann R, Ludwig W, Schleifer K-H (1999) Specific oligonucleotide probes for in situ detection of a major group of gram-positive bacteria with low DNA G+C content. Syst Appl Microbiol 22:186–196

    Google Scholar 

  • Meyer B, Kuever J (2008) Phylogenetic diversity and spatial distribution of the microbial community associated with the Caribbean deep-water sponge Polymastia cf. corticata by 16S rRNA, aprA, and amoA gene analysis. Microbiol Ecol 56:306–321

    Article  CAS  Google Scholar 

  • Mohamed NM, Saito K, Tal Y, Hill RT (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4(1):38–48

    Article  PubMed  CAS  Google Scholar 

  • Monier JM, Lindow SE (2003) Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. PNAS 100:15977–15982

    Article  PubMed  CAS  Google Scholar 

  • Nugues MM, Smith GW, Van Hooidonk RJ, Seabra MI, Bak RPM (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923

    Article  Google Scholar 

  • Olson JB, McCarthy PJ (2005) Associated bacterial communities of two deep-water sponges. Aquat Microb Ecol 39:47–55

    Article  Google Scholar 

  • Pace NR (2009) Mapping the tree of life: progress and prospects microbiology and molecular biology reviews 73:565–576

  • Patten NL, Harrison PL, Mitchell JG (2008) Prevalence of virus-like particles within a staghorn scleractinian coral (Acropora muricata) from the Great Barrier Reef. Coral Reefs 27:569–580

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:17–18

    Article  Google Scholar 

  • Radwan M, Hanora A, Zan J, Mohamed NM, Abo-Elmatty DM, Abou-El-Ela SH, Hill RT (2010) Bacterial community analyses of two red sea sponge Mar Biotechnol (NY). 2009 Dec 3. [Epub ahead of print]

  • Rappe’ MS, Giovannoni SJ (2003) The uncultured microbial majority. Ann Rev Microbiol 57:369–394

    Article  CAS  Google Scholar 

  • Reiswig HM (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14:231–249

    Article  Google Scholar 

  • Remily ER, Richardson LL (2006) Ecological physiology of a coral path-ogen and the coral reef environment. Microb Ecol 51:345–352

    Article  PubMed  Google Scholar 

  • Renegar DA, Harrison GF, Blackwelder PL, Thurmond JE, Ritchie KB, Vargas-Angel B (2008) Occurrence of epidermal bacteria in the scleractinian coral Montastraea cavernosa, 11th International Coral Reef Symposium Ft. Lauderdale, Florida, July 7–11, 2008

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron- opaque stain in electron microscopy. J Cel Biol 17:208–212

    Article  CAS  Google Scholar 

  • Richardson LL (1996) Horizontal and vertical migration patterns of Phorrnidium corallyticum and Beggiatoa spp. associated with black-band disease of corals. Microb Ecol 32:323–335

    Article  PubMed  Google Scholar 

  • Richardson LL (1997) Occurrence of the black band disease cyanobacterium on healthy corals of the Florida Keys. Bull Mar Sci 61:485–490

    Google Scholar 

  • Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14

    Article  CAS  Google Scholar 

  • Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers YH, Falcón LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e7

    Article  CAS  Google Scholar 

  • Sara M (1971) Ultrastructual aspects of the symbiosis between two species of the genus Aphanocapsa (Cyanophyceae) and Ircinia variabilis (Demospongiae). Mar Biol 11:214–221

    Article  Google Scholar 

  • Santavy DL, Willenz P, Colwell RR (1990) Phenotypic study of bacteria associated with the Caribbean sclerosponge, Ceratoporella nicholsoni. Appl Environ Microbiol 56:1750–1762

    PubMed  CAS  Google Scholar 

  • Schmidt EW, Obraztsova AY, Davidson SK, Faulkner DJ, Haygood MG (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel δ-proteobacterium, “Candidatus Entotheonella palauensis”. Mar Biol 136:969–977

    Article  CAS  Google Scholar 

  • Schmitt S, Wehrl M, Bayer K, Siegl A, Hentschel U (2007) Marine sponges as models for commensal microbe–host interactions. Symbiosis 44:43–50

    Google Scholar 

  • Sfanos KAS, Harmody DK, McCarthy PJ, Dang P, Pomponi SA, Lopez JV (2005) A molecular systematic survey of cultured microbial associates of deep water marine invertebrates. Syst Appl Microbiol 28:242–264

    Article  PubMed  CAS  Google Scholar 

  • Sharp K, Eam B, Faulkner DJ, Haygood MG (2007) Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73(2):622–629

    Google Scholar 

  • SPSS for Windows, Rel. 17.0 (2008) Chicago: SPSS Inc

  • Stabili L, Licciano M, Longo C, Corriero G, Mercurio M (2008) Evaluation of microbiological accumulation capability of the commercial sponge Spongia officinalis var. adriatica (Schmidt) (Porifera, Demospongiae). Water Res 42:2499–2506

    Article  PubMed  CAS  Google Scholar 

  • Subramaniam S (1998) The biology workbench—a seamless database and analysis environment for the biologist. Proteins 32:1–2

    Article  PubMed  CAS  Google Scholar 

  • Sussman M, Loya Y, Fine M, Rosenberg E (2003) The marine fireworm Hermodice carunculata is a winter reservoir and spring-summer vector for the coral-bleaching pathogen Vibrio shiloi. Environ Microbiol 5:250–255

    Article  PubMed  Google Scholar 

  • Sutherland KP, Porte JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302

    Article  Google Scholar 

  • Swofford D (2001) PAUP* Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer, Sunderland

    Google Scholar 

  • 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. Env Microbiol 6:121–130

    Article  Google Scholar 

  • Taylor MW, Schupp PJ, Nys RD, Kjelleberg S, Steinberg PD (2005) Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Env Microbiol 7:419–433

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Ritchie K (2009) How feasible is the biological control of coral diseases? Trends Ecol Evol 24:378–385

    Article  PubMed  Google Scholar 

  • Thompson FL, Hoste B, Thompson CC, Huys G, Swings J (2001) The coral bleaching Vibrio shiloi Kushmaro et al. 2001 is a later synonym of Vibrio mediterranei Pujalte and Garay 1986. Syst Appl Microbiol 24:516–519

    Article  PubMed  CAS  Google Scholar 

  • Thurber RLV, Barott KL, Hall D, Liu H, Rodrigueq-Mueller B, Desnues C, Edwards RA, Haynes M, Angley FE, Wegley L, Rohwer FL (2008) Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. PNAS 105(47):18413–18418

    Google Scholar 

  • Turon X, Galera J, Uriz MJ (1997) Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. J Exp Zool 278:22–36

    Article  Google Scholar 

  • Unson MD, Holland ND, Faulkner DJ (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbionts of a marine sponge and accumilation of the crystalline metabolite in the sponge tissue. Mar Biol 119:1–11

    Article  CAS  Google Scholar 

  • Vacelet J (1970) Description de cellules a bactéries intranucléaires chez des éponges Verongia. Journal de Microscopie (Paris) 9:333–346

    Google Scholar 

  • Vacelet J (1975) Etude en microscopie électronique de l’association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). J Microsc Biol Cell 23:271–288

    Google Scholar 

  • Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exper Mar Biol Ecol 30:301–314

    Article  Google Scholar 

  • Vacelet J, Boury-Esnault N, Fiala-Medioni A, Fisher CR (1995) A methanotrophic carnivorous sponge. Nature 377:296

    Article  CAS  Google Scholar 

  • Vishnyakov AE, Ereskovsky AV (2009) Bacterial symbionts as an additional cytological marker for identification of sponges without a skeleton. Mar Biol 156:1625–1632

    Article  Google Scholar 

  • Voss JD, Richardson LL (2006) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25:569–576

    Article  Google Scholar 

  • Webster NS, Hill RT (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an alpha-proteobacterium. Mar Biol 138:843–851

    Article  CAS  Google Scholar 

  • Webster NS, Wislon KJ, Blackall LL, Hill RT (2001) Phlogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444

    Article  PubMed  CAS  Google Scholar 

  • Webster NS, Negri AP, Munro MMHG, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300

    Article  PubMed  Google Scholar 

  • Wilkinson CR, Fay P (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279:527–529

    Article  CAS  Google Scholar 

  • Wilson WH, Dale AL, Davy JE, Davy SK (2005) An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145–148

    Google Scholar 

  • Wintzingerode FV, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental sample: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Article  Google Scholar 

  • Yu Y, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: A web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinform 7:57

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This publication is a result of funding from the National Oceanic and Atmospheric Administration, Center for Sponsored Coastal Ocean Science, under awards NA07NOS4000200 to Nova Southeastern University for the National Coral Reef Institute. The authors wish to thank Husain Alsayegh from the University of Miami Center for Advanced Microscopy (UMCAM) for his expertise in electron microscopy, and Abby Renegar for assistance with histological sectioning for FISH analyses. Jeffrey Prince was kind enough to permit use of the TEM in his lab at the Biology Department at the University of Miami. This work was in part supported from a President’s Faculty Research and Development Grant (PB and JL) from Nova Southeastern University. The authors also are grateful to Dr. Kim Ritchie and Dr. Steve Monday for helpful comments on earlier versions of the manuscript.

Author information

Authors and Affiliations

  1. Nova Southeastern University Oceanographic Center, 8000 North Ocean Drive, Dania Beach, FL, 33004, USA

    Karita Negandhi, Patricia L. Blackwelder & Jose V. Lopez

  2. University of Miami Rosenstiel School of Marine and Atmospheric Science (RSMAS), 4600 Rickenbacker Causeway, Miami, FL, 33149, USA

    Patricia L. Blackwelder

  3. Saint-Petersburg State University, 7/9 Universitetskaya nab., St-Petersburg, 199034, Russia

    Alexander V. Ereskovsky

  4. Institut National de la Recherche Scientifique, Centre Eau,Terre et Environnement, 490 rue de la Couronne, Quebec, Quebec, G1K 0B6, Canada

    Karita Negandhi

Authors
  1. Karita Negandhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia L. Blackwelder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander V. Ereskovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jose V. Lopez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jose V. Lopez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Negandhi, K., Blackwelder, P.L., Ereskovsky, A.V. et al. Florida reef sponges harbor coral disease-associated microbes. Symbiosis 51, 117–129 (2010). https://doi.org/10.1007/s13199-010-0059-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-010-0059-1

Keywords

Search

Navigation