Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix

Applied and Environmental Microbiology

Volumn 73, Issue 7, 2007, Pages 2067-2078

  Schmitt, Susanne ^a   Weisz, Jeremy B ^b,c   Lindquist, Niels ^b   Hentschel, Ute ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b University of North Carolina at Chapel Hill   (United States)

^c OLD DOMINION UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; ELECTRON MICROSCOPY; ELECTROPHORESIS; GENETIC ENGINEERING; MARINE BIOLOGY;

DENATURING GRADIENT GEL ELECTROPHORESIS (DGGE); EUBACTERIAL LINEAGE; MICROBIAL CONSORTIUM; SPONGE CELLS;

BACTERIA;

ADULT; BACTERIUM; COMPARATIVE STUDY; ELECTROKINESIS; JUVENILE; LARVA; MICROBIAL COMMUNITY; PHYLOGENETICS; SPECIES DIVERSITY; SPONGE; VERTICAL TRANSMISSION; VIVIPARITY;

ACIDOBACTERIUM; ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL TRANSMISSION; BACTERIUM; BACTERIUM IDENTIFICATION; BACTEROIDETES; CHLOROFLEXI; CRENARCHAEOTA; CYANOBACTERIUM; DELTAPROTEOBACTERIA; DENATURING GRADIENT GEL ELECTROPHORESIS; ELECTRON MICROSCOPY; GAMMAPROTEOBACTERIA; GEMMATIMONADETES; GENE SEQUENCE; HOST PARASITE INTERACTION; IMAGE ANALYSIS; LARVA; NITROSPIRA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLUM; PROGENY; SEQUENCE ANALYSIS; SPONGE (PORIFERA); UNINDEXED SEQUENCE;

ANIMALS; BACTERIA; ELECTROPHORESIS; LARVA; MICROSCOPY, ELECTRON, SCANNING; PHYLOGENY; PORIFERA; WATER MICROBIOLOGY;

BACTERIA (MICROORGANISMS); IRCINIA FELIX;

EID: 34247494635     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01944-06     Document Type: Article

References (60)

1. Ashelford, K. E., N. A. Chuzhanova, J. C. Fry, A. J. Jones, and A. J. Weightman. 2005. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71:7724-7736.
2. Baumann, P., L. Baumann, C. Y. Lai, D. Rouhbakhsh, N. A. Moran, and M. A. Clark. 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49:55-94.
3. Brusca, R. C., and G. J. Brusca. 1990. Phylum Porifera: the sponges, p. 181-210. In A. D. Sinauer (ed.), Invertebrates. Sinauer Press, Sunderland, MA.
4. Cary, S., and S. Giovannoni. 1993. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc. Natl. Acad. Sci. USA 90:5695-5699.
5. Duchassaing De Fonbressin, P., and G. Michelotti. 1864. Spongiaires de la mer Caraibe. Natuurk. Verh. Holl. Mij. Venetsch. Haarlem 21:1-124.
6. Enticknap, J. J., M. Kelly, O. Peraud, and R. T. Hill. 2006. Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl. Environ. Microbiol. 72:3724-3732.
7. Ereskovsky, A. V., E. Gonobobleva, and A. Vishnyakov. 2005. Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarca). Mar. Biol. 146:869-875.
8. Ereskovsky, A. V., and D. Tokina. 2004. Morphology and fine structure of the swimming larvae of Ircinia oros (Porifera, Demospongiae, Dictyoceratida). Invertebr. Reprod. Dev. 45:137-150.
9. Fieseler, L., M. Horn, M. Wagner, and U. Hentschel. 2004. Discovery of the novel candidate phylum "Poribacteria" in marine sponges. Appl. Environ. Microbiol. 70:3724-3732.
10. Fieseler, L., A. Quaiser, C. Schleper, and U. Hentschel. 2006. Analysis of the first genome fragment from the marine sponge-associated, novel candidate phylum Poribacteria by environmental genomics. Environ. Microbiol. 8:612-624.
11. Friedrich, A. B., I. Fischer, P. Proksch, J. Hacker, and U. Hentschel. 2001. Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol. Ecol. 38:105-113.
12. Friedrich, A. B., H. Merkert, T. Fendert, J. Hacker, P. Proksch, and U. Hentschel. 1999. Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridisation (FISH). Mar. Biol. 134:461-470.
13. Fuerst, J. A., R. I. Webb, M. J. Garson, L. Hardy, and H. M. Reiswig. 1998. Membrane-bounded nucleoids in microbial symbionts of marine sponges. FEMS Microbiol. Lett. 166:29-34.
14. Gernert, C., F. O. Glöckner, G. Krohne, and U. Hentschel. 2005. Microbial diversity of the freshwater sponge Spongilla lacustris. Microb. Ecol. 50:206-212.
15. Hallam, S. J., T. J. Mincer, C. Schleper, C. M. Preston, K. Roberts, P. M. Richardson, and E. F. DeLong. 2006. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4:520-536.
16. Hentschel, U., L. Fieseler, M. Wehrl, C. Gernert, M. Steinert, M. Horn, and J. Hacker. 2003. Microbial diversity of marine sponges, p. 59-88. In W. E. G. Müller (ed.), Molecular marine biology of sponges. Springer-Verlag, Heidelberg, Germany.
17. Hentschel, U., J. Hopke, M. Horn, A. B. Friedrich, M. Wagner, J. Hacker, and B. S. Moore. 2002. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 68:4431-4440.
18. Hentschel, U., K. M. Usher, and M. W. Taylor. 2006. Marine sponges as microbial fermenters. FEMS Microbiol. Ecol. 55:167-177.
19. Hill, R. T. 2004. Microbes from marine sponges: a treasure trove of biodiversity for natural products discovery, p. 177-190. In A. T. Bull (ed.), Microbial diversity and bioprospecting. ASM Press, Washington, DC.
20. Hooper, J. N. A., and R. W. M. van Soest. 2002. Systema Porifera. A guide to the classification of sponges, volume 1. Plenum Publishers, New York, NY.
21. Imhoff, J. F., and R. Stöhr. 2003. Sponge-associated bacteria: general overview and special aspects of bacteria associated with Halichondria panicea, p. 35-56. In W. E. G. Müller (ed.), Molecular marine biology of sponges. Springer-Verlag, Heidelberg, Germany.
22. Jaeckle, W. 1995. Transport and metabolism of alanine and palmitic acid by field-collected larvae of Tedania ignis (Porifera, Demospongiae): estimated consequences of limited label translocation. Biol. Bull. 189:159-167.
23. Kaye, H. 1991. Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts. Invertebr. Reprod. Dev. 19:13-24.
24. Kaye, H. R., and H. M. Reiswig. 1991. Sexual reproduction in four Caribbean commercial sponges. III. Larval behaviour, settlement and metamorphosis. Invertebr. Reprod. Dev. 19:25-35.
25. Levi, C., and P. Levi. 1976. Embryogenese de Chondrosia reniformis (Nardo), demosponge ovipare, et transmission des bacteries symbiotiques. Ann. Sci. Nat. Zool. 18:367-380.
26. Levi, C., and A. Porte. 1962. Ètude au microscope électronique de l'éponge Oscarella lobularis Schmidt et de sa larve amphiblastula. Cah. Biol. Mar. 3:307-315.
27. Leys, S., and B. Degnan. 2001. Cytological basis of photoresponsive behavior in a sponge larva. Biol. Bull. 201:323-338.
28. Li, C. W., J. Y. Chen, and T. E. Hua. 1998. Precambrian sponges with cellular structures. Science 279:879-882.
29. Lim, G., and M. Haygood. 2004. "Candidatus Endobugula glebosa," a specific bacterial symbiont of the marine bryozoan Bugula simplex. Appl. Environ. Microbiol. 70:4921-4929.
30. Lindquist, N., R. Bolser, and K. Laing. 1997. Timing of larval release by two Caribbean demosponges. Mar. Ecol. Prog. Ser. 155:309-313.
31. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K. H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
32. Maldonado, M., N. Cortadellas, M. I. Trillas, and K. Rutzler. 2005. Endosymbiotic yeast maternally transmitted in a marine sponge. Biol. Bull. 209: 94-106.
33. Muyzer, G., T. Brinkhoff, U. Nübel, C. Santegoeds, H. Schäfer, and C. Wawer. 1998. Denaturing gradient gel electrophoresis (DGGE) in microbial ecology, p. 1-27. In A. D. L. Akkermans, J. D. van Elsas, and F. J. de Bruijn (ed.), Molecular microbial ecology, manual 3.4.4. Kluwer, Dordrecht, The Netherlands.
34. Olson, J. B., and P. J. McCarthy. 2005. Associated bacterial communities of two deep-water sponges. Aquat. Microb. Ecol. 39:47-55.
35. Pawlik, J. R., G. McFall, and S. Zea. 2002. Does the odor from sponges of the genus Ircinia protect them from fish predators? J. Chem. Ecol. 28:1103-1115.
36. Peek, A. S., R. A. Feldman, R. A. Lutz, and R. C. Vrijenhoek. 1998. Cospeciation of chemoautotrophic bacteria and deep sea clams. Proc. Natl. Acad. Sci. USA 95:9962-9966.
37. Pile, A. J. 1997. Finding Reiswig's missing carbon: quantification of sponge feeding using dual-beam flow cytometry, p. 1403-1410. In H. A. Lessios and I. G. Macintyre (ed.), Proceedings of the 8th International Coral Reef Symposium, vol. 2. Smithsonian Tropical Research Institute, Balboa, Panama.
38. Preston, C. M., K. Y. Wu, T. F. Molinski, and E. F. DeLong. 1996. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc. Natl. Acad. Sci. USA 93:6241-6246.
39. Reiswig, H. 1974. Water transport, respiration and energetics of three tropical marine sponges. J. Exp. Mar. Biol. Ecol. 14:231-249.
40. Rützler, K., R. W. M. van Soest, and B. Alvarez. 2003. Swenzea zeai, a Caribbean reef sponge with a giant larva, and Scopalina ruetzleri: a comparative fine-structural approach to classification (Demospongiae, Halichondrida, Dictyonellidae). Invertebr. Biol. 122:203-222.
41. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Sauer, C., D. Dudaczek, B. Holldobler, and R. Gross. 2002. Tissue localization of the endosymbiotic bacterium "Candidatus Blochmannia floridanus" in adults and larvae of the carpenter ant Camponotus floridanus. Appl. Environ. Microbiol. 68:4187-4193.
43. Scheuermayer, M., S. M. Pimentel-Elardo, L. Fieseler, L. Grozdanov, and U. Hentschel. 2006. Microorganisms of sponges: phylogenetic diversity and biotechnological potential, p. 289-312. In P. Proksch and W. E. G. Müller (ed.), Frontiers in marine biotechnology, Horizon Scientific Press, London, United Kingdom.
44. Schirmer, A., R. Gadkari, C. Reeves, F. Ibrahim, E. DeLong, and C. Hutchinson. 2005. Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl. Environ. Microbiol. 71:4840-4849.
45. Sciscioli, M., E. Lepore, M. Gherardi, and L. S. Liaci. 1994. Transfer of symbiotic bacteria in the mature oocyte of Geodia sydonium (Porifera, Demospongiae): an ultrastructural study. Cah. Biol. Mar. 35:471-478.
46. Sharp, K. H., B. Earn, D. J. Faulkner, and M. G. Haygood. 2007. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl. Environ. Microbiol. 73:622-629.
47. Sipe, A., A. Wilbur, and S. Cary. 2000. Bacterial symbiont transmission in the wood-boring shipworm Bankia setacea (Bivalvia: Teredinidae). Appl. Environ. Microbiol. 66:1685-1691.
48. Taylor, M. W., P. J. Schupp, I. Dahllof, S. Kjelleberg, and P. D. Steinberg. 2004. Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ. Microbiol. 6:121-130.
49. Taylor, M. W., P. J. Schupp, R. de Nys, S. Kjelleberg, and P. D. Steinberg. 2005. Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environ. Microbiol. 7:419-433.
50. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Adds Res. 25:4876-4882.
51. Thorns, C., M. Horn, M. Wagner, U. Hentschel, and P. Proksch. 2003. Monitoring microbial diversity and natural products profiles of the sponge Aplysina cavernicola following transplantation. Mar. Biol. 142:685-692.
52. Usher, K. M., J. Kuo, J. Fromont, and D. C. Sutton. 2001. Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461:15-23.
53. Vacelet, J. 1975. Étude en microscopie électronique de l'association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). J. Microsc. Biol. Cell. 23:271-288.
54. Vacelet, J., and C. Donadey. 1977. Electron microscope study of the association between some sponges and bacteria. J. Exp. Mar. Biol. Ecol. 30:301-314.
55. Webster, N., and R. T. Hill. 2001. The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an α-proteobacterium. Mar. Biol. 138:843-851.
56. Webster, N. S., K. J. Wilson, L. L. Blackall, and R. T. Hill. 2001. Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl. Environ. Microbiol. 67:434-444.
57. Wehrl, M., M. Steinert, and U. Hentschel. Bacterial uptake by the marine sponge Aplysina aerophoba. Microb. Ecol., in press.
58. Wilkinson, C. R. 1978. Microbial associations in sponges. III. Ultrastructure of the in situ associations in coral reef sponges. Mar. Biol. 49:169-176.
59. Willenz, P., and W. D. Hartman. 1989. Micromorphology and ultrastructure of Caribbean sclerosponges. I. Ceratoporella nicholsoni and Stromatospongia norae (Ceratoporellidae-Porifera). Mar. Biol. 103:387-402.
60. Zhang, H., Y. Sekiguchi, S. Hanada, P. Hugenholtz, H. Kim, Y. Kamagata, and K. Nakamura. 2003. Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating microorganism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int. J. Syst. Evol. Microbiol. 53:1155-1163.