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Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponges, Dysidea spp.

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Abstract

Marine sponges can host a variety of cyanobacterial and bacterial symbionts, but it is often unclear whether these symbionts are generalists that occur in many host species or specialists that occur only in certain species or populations of sponges. The filamentous cyanobacterium Oscillatoria spongeliae is found in the sponges Dysidea n. sp. aff. herbacea 1A and 1B, and similar cyanobacteria are found in D. n. sp. aff. granulosa. We amplified and sequenced sponge nuclear ribosomal DNA (rDNA) and cyanobacterial 16S rDNA from specimens of these three sponges. We then used these sequences to construct phylogenies for host sponges and their symbiotic cyanobacteria. Each of these three sponge species hosts a distinct cyanobacterial clade, suggesting a high degree of host specificity and potential coevolution between symbiotic cyanobacteria and their host sponges.

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References

  • Althoff K, Schütt, Steffen R, Batel R, Müller WEG (1998) Evidence for a symbiosis between bacteria of the genus Rhodobacter and the marine sponge Halichondria panicea: harbor also for putatively toxic bacteria? Mar Biol 130:529–536

    Article  Google Scholar 

  • Alvarez B, Crisp MD, Driver F, Hooper JNA, Soest RWM van (2000) Phylogenetic relationships of the family Axinellidae (Porifera: Demospongiae) using morphological and molecular data. Zool Scr 29:169–198

    Article  Google Scholar 

  • Bergquist PR (1965) The sponges of Micronesia, part 1. The Palau Archipelago. Pac Sci 19:123–204

    Google Scholar 

  • Borchiellini C, Chombard C, Lafay B, Boury-Esnault N (2000) Molecular systematics of sponges (Porifera). Hydrobiologia 420:15–27

    CAS  Google Scholar 

  • Brooks DR, McLennan DA (1991) Phylogeny, ecology, and behavior. The University of Chicago Press, Chicago

  • Colin PL, Arneson C (1995) Tropical Pacific invertebrates. Coral Reef Press, Beverly Hills, Calif.

  • Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546

    Google Scholar 

  • Engel S, Pawlik JR (2000) Allelopathic activities of sponge extracts. Mar Ecol Prog Ser 207:273–281

    Google Scholar 

  • Erpenbeck D, Breeuwer JAJ, van der Velde HC, van Soest RWM (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar Biol 141:377–386

    Google Scholar 

  • Flowers AE, Garson MJ, Webb RI, Dumdei EJ, Charan RD (1998) Cellular origin of chlorinated diketopiperazines in the dictyoceratid sponge Dysidea herbacea (Keller). Cell Tissue Res 292:597–607

    CAS  PubMed  Google Scholar 

  • Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, Hentschel U (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 

  • Garson MJ (2001) Ecological perspectives on marine natural product biosynthesis. In:McClintock JB, Baker BJ (eds) Marine Chemical Ecology. CRC Press, Boca Raton, Fla., pp 71–114

  • Hinde R, Pironet F, Borowitzka MA (1994) Isolation of Oscillatoria spongeliae, the filamentous cyanobacterial symbiont of the marine sponge Dysidea herbacea. Mar Biol 119:99–104

    Google Scholar 

  • Kelly M, Hooper J, Paul VJ, Paulay G, Soest R van, Weerdt W de (2003) Taxonomic inventory of sponges (Porifera) of the Mariana islands. Micronesica (in press)

  • Lopez JV, Peterson CL, Willoughby R, Wright AE, Enright E, Zoladz S, Reed JK, Pomponi SA (2002) Characterization of genetic markers for in vitro cell line identification of the marine sponge, Axinella corrugata. J Hered 93:27–36

    Article  CAS  PubMed  Google Scholar 

  • Margot H, Acebal C, Toril E, Amils R, Fernandez Puentes JL (2002) Consistent association of crenarchaeal Archaea with sponges of the genus Axinella. Mar Biol 140:739–745

    CAS  Google Scholar 

  • Martínez-Murcia AJ, Acinas SG, Rodriguez-Valera F (1995) Evaluation of prokaryotic diversity by restrictase digestion of 16S rDNA directly amplified from hypersaline environments. FEMS Microbiol Ecol 17:247–256

    Article  Google Scholar 

  • Nelissen B, De Baere R, Wilmotte A, De Wachter R (1996) Phylogenetic relationships of nonaxenic filamentous cyanobacterial strains based on 16S rRNA sequence analysis. J Mol Evol 42:194–200

    CAS  PubMed  Google Scholar 

  • Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332

    PubMed  Google Scholar 

  • Parker MA, Spoerke JM (1998) Geographic structure of lineage associations in a plant–bacterial mutualism. J Evol Biol 11:549–562

    Article  Google Scholar 

  • Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194

    CAS  Google Scholar 

  • Rai AN (1990) CRC Handbook of symbiotic cyanobacteria. CRC Press, Boca Raton, Fla.

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

    Google Scholar 

  • Sarà M, Bavestrello G, Cattaneo-Vietti R, Cerrano C (1998) Endosymbiosis in sponges: relevance for epigenesis and evolution. Symbiosis 25:57–70

    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

    CAS  Google Scholar 

  • Swofford DL (1999) PAUP*:Phylogenetic analysis using parsimony (*and other methods), Version 4.0b3a. Sinauer, Sunderland, Mass.

  • Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In:Hillis DM, Moritz C, Mable BK (eds) Molecular Systematics, 2nd ed. Sinauer, Sunderland, Mass., pp 407–514

  • Thacker RW, Becerro MA, Lumbang WA, Paul VJ (1998) Allelopathic interactions between sponges on a tropical reef. Ecology 79:1740–1750

    Google Scholar 

  • Thompson JN (1994) The coevolutionary process. The University of Chicago Press, Chicago

  • Unson MD, Holland ND, Faulkner DJ (1994) 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 119:1–11

    CAS  Google Scholar 

  • Uriz MJ, Turon X, Galera J, Tur JM (1996) New light on the cell location of avarol within the sponge Dysidea avara (Dendroceratida). Cell Tissue Res 285:519–527

    Article  Google Scholar 

  • Usher KM, Kuo J, Fromont J, Sutton DC (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461:15–23

    Article  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

    Google Scholar 

  • Wilmotte A (1994) Molecular evolution and taxonomy of the cyanobacteria. In:Bryant DA (ed) Molecular biology of Cyanobacteria. Kluwer, Dordrecht,, pp 1–25

  • Zheng WW, Nilsson M, Bergman B, Rasmussen U (1999) Genetic diversity and classification of cyanobacteria in different Azolla species by the use of PCR fingerprinting. Theor Appl Genet 99:1187–1193

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Becerro, F. Camacho, D. Ginsburg, R. Helling, K. Iken, V. Paul, and G. Paulay for helpful suggestions and assistance in the field. K. Bevis, P. Erwin, P. Sammarco and two anonymous reviewers provided comments that improved the manuscript. This work was supported by a Faculty Research Grant from the University of Alabama at Birmingham. The experiments reported in this manuscript comply with the current laws of the United States of America.

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Correspondence to R. W. Thacker.

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Communicated by P.W. Sammarco, Chauvin

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Thacker, R.W., Starnes, S. Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponges, Dysidea spp.. Marine Biology 142, 643–648 (2003). https://doi.org/10.1007/s00227-002-0971-x

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  • DOI: https://doi.org/10.1007/s00227-002-0971-x

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