Diversity and biological activities of the bacterial community associated with the marine sponge Phorbas tenacior (Porifera, Demospongiae)

Letters in Applied Microbiology

Volumn 58, Issue 1, 2014, Pages 42-52

  Dupont, S ^a   Carre Mlouka A ^a   Descarrega, F ^a   Ereskovsky, A ^b   Longeon, A ^a   Mouray, E ^a   Florent, I ^a   Bourguet Kondracki, M L ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b AVIGNON UNIVERSITÉ   (France)

Author keywords

Antimicrobial activity; Antioxidant activity; Antiplasmodial activity; Associated bacteria; Phorbas tenacior; Phylogenetic diversity; RAPD; Sponge

Indexed keywords

ANTIOXIDANTS; BACTERIA; PLANTS (BOTANY); RNA;

ANTI-MICROBIAL ACTIVITY; ANTIOXIDANT ACTIVITIES; ANTIPLASMODIAL ACTIVITY; ASSOCIATED BACTERIA; MARINE SPONGE; PHORBAS TENACIOR; PHYLOGENETIC DIVERSITY; POLYMORPHIC DNA; RANDOM AMPLIFIED POLYMORPHIC DNA; SPONGE;

BIOACTIVITY;

ANTIINFECTIVE AGENT; ANTIMALARIAL AGENT; ANTIOXIDANT; NALIDIXIC ACID; RNA 16S;

ANTIMICROBIAL ACTIVITY; ANTIOXIDANT; DATA ACQUISITION; DNA; GENE; PHYLOGENETICS; SPECIES DIVERSITY; SPONGE;

ACTINOBACTERIA; ANTIBACTERIAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIPROTOZOAL ACTIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM ISOLATION; CITRICOCCUS; CULTURE MEDIUM; ELECTRON MICROSCOPY; EPIBIONT; FLUORESCENCE IN SITU HYBRIDIZATION; GENE SEQUENCE; HOST RESISTANCE; MARINE ENVIRONMENT; MEDITERRANEAN SEA; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MORPHOTYPE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHORBAS TENACIOR; PHOTOBACTERIUM; PHYLOGENETIC TREE; PHYLOGENY; PLASMODIUM FALCIPARUM; PROTEOBACTERIA; PSEUDOMONAS; PSEUDOVIBRIO; RANDOM AMPLIFIED POLYMORPHIC DNA; RUEGERIA; SCANNING ELECTRON MICROSCOPY; SEQUENCE HOMOLOGY; SHEWANELLA; SPECIES CULTIVATION; SPONGE (PORIFERA); TRANSMISSION ELECTRON MICROSCOPY; VERTICAL TRANSMISSION; VIBRIO;

MEDITERRANEAN SEA;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); CITRICOCCUS; DEMOSPONGIAE; PHORBAS TENACIOR; PHOTOBACTERIUM; PORIFERA; PROTEOBACTERIA; PSEUDOMONAS; PSEUDOVIBRIO; RUEGERIA; SHEWANELLA; VIBRIO;

ANTIMICROBIAL ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIPLASMODIAL ACTIVITY; ASSOCIATED BACTERIA; PHORBAS TENACIOR; PHYLOGENETIC DIVERSITY; RAPD; SPONGE;

ACTINOBACTERIA; ANIMALS; ANTIBIOSIS; BIODIVERSITY; GENES, RRNA; MEDITERRANEAN SEA; MICROBIOTA; MICROCOCCACEAE; PHYLOGENY; PLASMODIUM FALCIPARUM; PORIFERA; PROTEOBACTERIA; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; RHODOBACTERACEAE; RNA, RIBOSOMAL, 16S; VIBRIO;

EID: 84890163270     PISSN: 02668254     EISSN: 1472765X     Source Type: Journal    
DOI: 10.1111/lam.12154     Document Type: Article

References (53)

1. Altenburger, P., Kämpfer, P., Schumann, P., Steiner, R., Lubitz, W. and Busse, H.J. (2002) Citricoccus muralis gen. nov., sp nov., a novel actinobacterium isolated from a medieval wall painting. Int J Syst Evol Microbiol 52, 2095-2100.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215, 403-410.
3. Al-Zereini, W., Fusto Fondja Yao, C.B., Laatsh, H. and Anke, H. (2010) Aqabamycins A-G: novel maleimides from a marine Vibrio species: II. Structure elucidation. J Antibiot 63, 297-301.
4. Bhattarai, H.D., Ganti, V.S., Paudel, B., Lee, Y.K. and Lee, H.K. (2007) Isolation of antifouling compounds from the marine bacterium, Shewanella oneidensis SCH0402. World J Microbiol 23, 243-249.
5. Blunt, J.W., Copp, B.R., Keyzers, R.A., Munro, M.H.G. and Prinsep, M.R. (2012) Marine natural products. Nat Prod Rep 29, 144-222.
6. Casapullo, A., Minale, L., Zollo, F. and Lavayre, J. (1994) 4 New dimeric peptide alkaloids, anchinopeptolides-B-D, and cycloanchinopeptolide-C, congeners of anchinopeptolide-a, from the Mediterranean marine sponge Anchinoe tenacior. J Nat Prod 57, 1227-1233.
7. Cole, J.R., Chai, B., Marsh, T.L., Farris, R.J., Wang, Q., Kulam, S.A., Chandra, S., McGarrell, D.M. et al. (2003) The ribosomal database project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31, 442-443.
8. Delong, E.F. (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89, 5685-5689.
9. Enticknap, J.J., Kelly, M., Peraud, O. and Hill, R.T. (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.
10. Ereskovsky, A.V., Gonobobleva, E.L. and Vishnyakov, A. (2005) Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar Biol 146, 869-875.
11. Ereskovsky, A.V., Lavrov, D.V., Boury-Esnault, N. and Vacelet, J. (2011) Molecular and morphological description of a new species of Halisarca (Demospongiae: Halisarcida) from Mediterranean Sea with redescription of the type species Halisarca dujardini. Zootaxa 2768, 5-31.
12. Florent, I., Mouray, E., Ali, F.D., Drobecq, H., Girault, S., Schrevel, J., Sergheraert, C. and Grellier, P. (2001) Cloning of Plasmodium falciparum protein disulfide isomerase homologue by affinity purification using the antiplasmodial inhibitor 1, 4-bis{3-[N-(cyclohexyl methyl)amino]propyl}piperazine. FEBS Lett 484, 246-252.
13. Friedrich, A.B., Fischer, I., Proksch, P., Hacker, J. and Hentschel, U. (2001) Temporal variation of the microbial community associated with the mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38, 105-113.
14. Hentschel, U., Schmid, M., Wagner, M., Fieseler, L., Gernert, C. and Hacker, J. (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol 35, 305-312.
15. Hentschel, U., Piel, J., Degnan, S.M. and Taylor, M.W. (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10, 641-654.
16. Hoffmann, M., Monday, S.R., Allard, M.W., Strain, E.A., Whittaker, P., Naum, M., McCarthy, P.J., Lopez, J.V. et al. (2012) Vibrio caribbeanicus sp. nov., isolated from the marine sponge Scleritoderma cyanea. Int J Syst Evol Microbiol 62, 1736-1743.
17. Jang, K.H., Jeon, J.E., Ryu, S., Lee, H.S., Oh, K.B. and Shin, J. (2008) Polyoxygenated diterpenes from the sponge Phorbas sp. J Nat Prod 71, 1701-1707.
18. Kalinovskaya, N.I., Romanenko, L.A., Irisawa, T., Ermakova, S.P. and Kalinovsky, A.I. (2011) Marine isolate Citricoccus sp KMM 3890 as a source of a cyclic siderophore nocardamine with antitumor activity. Microbiol Res 166, 654-661.
19. Lajnef, R., Snoussi, M., Romalde, J.L., Nozha, C. and Hassen, A. (2012) Comparative study on the antibiotic susceptibility and plasmid profiles of Vibrio alginolyticus strains isolated from four Tunisian marine biotopes. World J Microbiol Biotechnol 28, 3345-3363.
20. Laroche, M., Imperatore, C., Grozdanov, L., Costantino, V., Mangoni, A., Hentschel, U. and Fattorusso, E. (2006) Cellular localization of secondary metabolites isolated from the Caribbean sponge Plakortis simplex. Mar Biol 151, 1365-1373.
21. Li, W.J., Chen, H.H., Zhang, Y.Q., Kim, C.J., Park, D.J., Lee, J.C., Xu, L.H. and Jiang, C.L. (2005) Citricoccus alkalitolerans sp nov., a novel actinobacterium isolated from a desert soil in Egypt. Int J Syst Evol Microbiol 55, 87-90.
22. Mansson, M., Gram, L. and Larsen, T.O. (2011) Production of bioactive secondary metabolites by marine Vibrionaceae. Mar drugs 9, 1440-1468.
23. Margassery, L.M., Kennedy, J., O'Gara, F., Dobson, A.D. and Morrissey, J.P. (2012) Diversity and antibacterial activity of bacteria isolated from the coastal marine sponges Amphilectus fucorum and Eurypon major. Lett Appl Microbiol 55, 2-8.
24. Mayer, A.M., Glaser, K.B., Cuevas, C., Jacobs, R.S., Kem, W., Little, R.D., McIntosh, J.M., Newman, D.J. et al. (2010) The odyssey of marine pharmaceuticals: a current pipeline perspective. Trends Pharmacol Sci 31, 255-265.
25. McNally, M. and Capon, R.J. (2001) Phorbasin B and C: novel diterpenes from a southern Australian marine sponge, Phorbas species. J Nat Prod 64, 645-647.
26. Meng, F.X., Yang, X.C., Yu, P.S., Pan, J.M., Wang, C.S., Xu, X.W. and Wu, M. (2010) Citricoccus zhacaiensis sp nov., isolated from a bioreactor for saline wastewater treatment. Int J Syst Evol Microbiol 60, 495-499.
27. Morinaka, B.I., Masuno, M.N., Pawlik, J.R. and Molinski, T.F. (2007) Amaranzole A, a new N-Imidazolyl steroid from Phorbas amaranthus. Org Lett 9, 5919-2477.
28. Morinaka, B.I., Pawlik, J.R. and Molinski, T.F. (2009) Amaroxocanes A and B: sulfated dimeric sterols defend the Caribbean coral reef sponge Phorbas amaranthus from fish predators. J Nat Prod 72, 259-264.
29. Neulinger, S.C., Stohr, R., Thiel, V., Schmaljohann, R. and Imhoff, J.F. (2010) New phylogenetic lineages of the Spirochaetes phylum associated with Clathrina species (Porifera). J Microbiol 48, 411-418.
30. Nishida, T., Morita, N., Yano, Y., Orikasa, Y. and Okuyama, H. (2007) The antioxidative in a marine bacterium, Shewanella marinintestina IK-1. FEBS Lett 581, 4212-4216.
31. O' Halloran, J.A., Barbosa, T.M., Morrissey, J.P., Kennedy, J., O' Gara, F. and Dobson, A.D.W. (2011) Diversity and antimicrobial activity of Pseudovibrio spp. from Irish marine sponges. J Appl Microbiol 110, 1495-1508.
32. O'Brien, J.A., Daudi, A., Butt, V.S. and Bolwell, G.P. (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 3, 765-779.
33. Olsen, S.M., Pedersen, L.T., Laursen, M.H., Kiil, S. and Dam-Johansen, K. (2007) Enzyme-based antifouling coatings: a review. Biofouling 23, 369-383.
34. Quévrain, E., Domart-Coulon, I., Pernice, M. and Bourguet-Kondracki, M.L. (2009) Novel natural parabens produced by a Microbulbifer bacterium in its calcareous sponge host Leuconia nivea. Environ Microbiol 11, 1527-1539.
35. Rho, J.R., Lee, H.S., Sim, C.J. and Shin, J. (2002) Gagunins, highly oxygenated diterpenoids from the sponge Phorbas sp. Tetrahedron 58, 9585-9591.
36. Roue, M., Domart-Coulon, I., Ereskovsky, A., Djediat, C., Perez, T. and Bourguet-Kondracki, M.L. (2010) Cellular localization of clathridimine, an antimicrobial 2-aminoimidazole alkaloid produced by the Mediterranean calcareous sponge Clathrina clathrus. J Nat Prod 73, 1277-1282.
37. Rudi, A., Stein, Z., Green, S., Goldberg, I., Kashman, Y., Benayahu, Y. and Schleyer, M. (1994) Phorbazoles A-D, novel chlorinated phenylpyrrolyloxazoles from the marine sponge Phorbas Aff Clathrata. Tetrahedron Lett 35, 2589-2592.
38. Schmitt, S., Angermeier, H., Schiller, R., Lindquist, N. and Hentschel, U. (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microbiol 74, 7694-7708.
39. Schmitt, S., Tsai, P., Bell, J., Fromont, J., Ilan, M., Lindquist, N., Perez, T., Rodrigo, A. et al. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. Isme 6, 564-576.
40. Searle, P.A. and Molinski, T.F. (1995) 4-Dehydroecdysterone, a new ecdysteroid from the zoanthid Parazoanthus Sp. J Nat Prod 58, 264-268.
41. Sipkema, D., Schippers, K., Maalcke, W.J., Yang, Y., Salim, S. and Blanch, H.W. (2011) Multiple approaches to enhance the cultivability of bacteria associated with the marine sponge Haliclona (gellius) sp. Appl Environ Microbiol 77, 2130-2140.
42. Taylor, M.W., Radax, R., Steger, D. and Wagner, M. (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71, 295-347.
43. Topsent, E. (1925) Etude de Spongiaires du Golfe de Naples. Arch Zool Exp Gen 63, 623-725.
44. Trager, W. and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193, 673-675.
45. Vacelet, J. (1975) Electron-microscope study of association between bacteria and sponges of genus Verongia (Dictyoceratida). J Microsc Biol Cell 23, 271-288.
46. Vacelet, J. and Donadey, C. (1977) Electron-microscope study of association between some sponges and bacteria. J Exp Mar Biol Ecol 30, 301-314.
47. Vacelet, J. and Perez, T. (2008) Phorbas topsenti and Phorbas tailliezi (Demospongiae, Poecilosclerida), new names for the Mediterranean 'Phorbas paupertas' and 'Phorbas coriaceus'. Zootaxa 1873, 26-38.
48. Van-Soest, R.W.M. (2007) Sponge biodiversity. J Mar Biol Assoc 6, 1345-1348.
49. Webster, N.S. and Taylor, M.W. (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 2, 335-346.
50. Wilkinson, C.R. and Fay, P. (1979) Nitrogen-fixation in coral-reef sponges with symbiotic Cyanobacteria. Nature 279, 527-529.
51. Wilkinson, C.R., Nowak, M., Austin, B. and Colwell, R.R. (1981) Specificity of bacterial symbionts in Mediterranean and great barrier-reef sponges. Microb Ecol 7, 13-21.
52. Yang, S.H., Kwon, K.K., Lee, H.S. and Kim, S.J. (2006) Shewanella spongiae sp nov., isolated from a marine sponge. Int J Syst Evol Microbiol 56, 2879-2882.
53. Zhang, H., Major, J.M., Lewis, R.J. and Capon, R.J. (2008) Phorbasins G-K: new cytotoxic diterpenes from a southern Australian marine sponge, Phorbas sp. Org Biomol Chem 6, 3811-3815.