Microbial communities and bioactive compounds in marine sponges of the family irciniidae-A review

Marine Drugs

Volumn 12, Issue 10, 2014, Pages 5089-5122

  Hardoim, Cristiane C P ^a   Costa, Rodrigo ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Host microbe interactions; Microbial diversity; Polyketide synthases; Secondary metabolites; Symbiosis

Indexed keywords

BISVERTINOLONE; CHEMICAL COMPOUND; CYCLO(LEVO PROLYL LEVO TYROSINE); OXOSORBICILLINOL; POLYKETIDE; RNA 16S; SORBICILLIN; TERPENOID; UNCLASSIFIED DRUG;

ARCHAEON; BACTERIUM CULTURE; BIOCHEMICAL COMPOSITION; BIOLOGICAL ACTIVITY; CLIMATE CHANGE; COMMUNITY ECOLOGY; DENATURING GRADIENT GEL ELECTROPHORESIS; FUNGUS; GENE CLUSTER; IRCINIIDAE; MARICULTURE; MARINE SPECIES; METABOLITE; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; POPULATION ABUNDANCE; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION; SPECIES CULTIVATION; SPONGE (PORIFERA); STRUCTURE ANALYSIS; SYMBIONT; TRANSMISSION ELECTRON MICROSCOPY; VERTICAL TRANSMISSION; ANIMAL; BACTERIUM; HUMAN; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; ARCHAEA; BACTERIA; FUNGI; HUMANS; PORIFERA; QUORUM SENSING; SYMBIOSIS;

EID: 84908161340     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12105089     Document Type: Review

References (141)

1. Li, C.W.; Chen, J.Y.; Hua, T.E. Precambrian sponges with cellular structures. Science 1998, 279, 879-882.
2. Van Soest, R.W.M.; Boury-Esnault, N.; Vacelet, J.; Dohrmann, M.; Erpenbeck, D.; de Voogd, N.J.; Santodomingo, N.; Vanhoorne, B.; Kelly, M.; Hooper, J.N.A. Global diversity of sponges (Porifera). PLoS One 2012, 7, e35105.
3. Love, G.D.; Grosjean, E.; Stalvies, C.; Fike, D.A.; Grotzinger, J.P.; Bradley, A.S.; Kelly, A.E.; Bhatia, M.; Meredith, W.; Snape, C.E.; et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 2009, 457, 718-722.
4. Vacelet, J.; Donadey, C. Electron-microscope study of association between some sponges and Bacteria. J. Exp. Mar. Biol. Ecol. 1977, 30, 301-314.
5. Hentschel, U.; Piel, J.; Degnan, S.M.; Taylor, M.W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 2012, 10, 641-675.
6. Taylor, M.W.; Radax, R.; Steger, D.; Wagner, M. Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 2007, 71, 295-347.
7. Spalding, M.D.; Fox, H.E.; Halpern, B.S.; McManus, M.A.; Molnar, J.; Allen, G.R.; Davidson, N.; Jorge, Z.A.; Lombana, A.L.; Lourie, S.A.; et al. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. Bioscience 2007, 57, 573-583.
8. Webster, N.S.; Taylor, M.W. Marine sponges and their microbial symbionts: Love and other relationships. Environ. Microbiol. 2012, 14, 335-346.
9. Thomas, T.R.A.; Kavlekar, D.P.; LokaBharathi, P.A. Marine drugs from sponge-microbe association: A review. Mar. Drugs 2010, 8, 1417-1468.
10. Taylor, M.W.; Hill, R.T.; Hentschel, U. Meeting report: 1st International Symposium on Sponge Microbiology. Mar. Biotechnol. 2011, 13, 1057-1061.
11. Bayer, K.; Scheuermayer, M.; Fieseler, L.; Hentschel, U. Genomic mining for novel FADH2-dependent halogenases in marine sponge-associated microbial consortia. Mar. Biotechnol. 2013, 15, 63-72.
12. Fieseler, L.; Horn, M.; Wagner, M.; Hentschel, U. Discovery of the novel candidate phylum "Poribacteria" in marine sponges. Appl. Environ. Microbiol. 2004, 70, 3724-3732.
13. Hentschel, U.; Hopke, J.; Horn, M.; Friedrich, A.B.; Wagner, M.; Hacker, J.; Moore, B.S. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 2002, 68, 4431-4440.
14. Schmitt, S.; Tsai, P.; Bell, J.; Fromont, J.; Ilan, M.; Lindquist, N.; Perez, T.; Rodrigo, A.; Schupp, P.J.; Vacelet, J.; et al. Assessing the complex sponge microbiota: Core, variable and species-specific bacterial communities in marine sponges. ISME J. 2012, 6, 564-576.
15. Siegl, A.; Hentschel, U. PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ. Microbiol. Rep. 2010, 2, 507-513.
16. Fan, L.; Liu, M.; Simister, R.; Webster, N.S.; Thomas, T. Marine microbial symbiosis heats up: The phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J. 2013, 7, 991-1002.
17. Pantile, R.; Webster, N. Strict thermal threshold identified by quantitative PCR in the sponge Rhopaloeides odorabile. Mar. Ecol. Prog. Ser. 2011, 431, 97-105.
18. Simister, R.; Taylor, M.W.; Tsai, P.; Webster, N. Sponge-microbe associations survive high nutrients and temperatures. PLoS One 2012, 7, e52220.
19. Webster, N.S.; Cobb, R.E.; Negri, A.P. Temperature thresholds for bacterial symbiosis with a sponge. ISME J. 2008, 2, 830-842.
20. Webster, N.S.; Taylor, M.W.; Behnam, F.; Lucker, S.; Rattei, T.; Whalan, S.; Horn, M.; Wagner, M. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 2010, 12, 2070-2082.
21. Mohamed, N.M.; Colman, A.S.; Tal, Y.; Hill, R.T. Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environ. Microbiol. 2008, 10, 2910-2921.
22. Mohamed, N.; Cicirelli, E.; Kan, J.; Chen, F.; Fuqua, C.; Hill, R. Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ. Microbiol. 2008, 10, 75-86.
23. Mohamed, N.; Rao, V.; Hamann, M.; Kelly, M.; Hill, R. Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl. Environ. Microbiol. 2008, 74, 4133-4143.
24. Mohamed, N.M.; Saito, K.; Tal, Y.; Hill, R.T. Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J. 2010, 4, 38-48.
25. Zan, J.D.; Fuqua, C.; Hill, R.T. Diversity and functional analysis of luxS genes in vibrios from marine sponges Mycale laxissima and Ircinia strobilina. ISME J. 2011, 5, 1505-1516.
26. Van Soest, R.W.M.; Boury-Esnault, N.; Hooper, J.N.A.; Rützler, K.; de Voogd, N.J.; Alvarez de Glasby, B.; Hajdu, E.; Pisera, A.B.; Manconi, R.; Schoenberg, C.; et al. World Porifera Database. Available online: http://www.marinespecies.org/porifera (accessed on 20 December 2013).
27. Cook, S.C.; Bergquist, P.R. Family Irciniidae Gray, 1867. In System Porifera: A Guide to the Classification of Sponges; Hooper, J.N.A., van Soest R.W.M., Eds.; Kluwer Academic/Plenum Publishers: New York, NY, USA, 2002; pp. 1022-1027.
28. Cook, S.; Bergquist, P. New species of dictyoceratid sponges from New Zealand: Genus Ircinia (Porifera: Demospongiae: Dictyoceratida). N. Z. J. Mar. Freshw. Res. 1999, 33, 545-563.
29. Wörheide, G.; Dohrmann, M.; Erpenbeck, D.; Larroux, C.; Maldonado, M.; Voigt, O.; Borchiellini, C.; Lavrov, D.V. Deep phylogeny and evolution of sponges (Phylum Porifera). In Advances in Marine Biology; Becerro, M.A., Uriz, M.J., Maldonado, M., Turon, X., Eds.; Academic Press: Amsterdam, The Netherlands. 2012; pp. 1-18.
30. Schmitt, S.; Weisz, J.; Lindquist, N.; Hentschel, U. Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl. Environ. Microbiol. 2007, 73, 2067-2078.
31. Weisz, J.; Hentschel, U.; Lindquist, N.; Martens, C. Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar. Biol. 2007, 152, 475-483.
32. Yang, J.K.; Sun, J.; Lee, O.O.; Wong, Y.H.; Qian, P.Y. Phylogenetic diversity and community structure of sponge-associated bacteria from mangroves of the Caribbean Sea. Aquat. Microb. Ecol. 2011, 62, 231-240.
33. Pita, L.; López-Legentil, S.; Erwin, P.M. Biogeography and host fidelity of bacterial communities in Ircinia spp. from the Bahamas. Microb. Ecol. 2013, 66, 437-447.
34. Erwin, P.M.; López-Legentil, S.; González-Pech, R.; Turon, X. A specific mix of generalists: Bacterial symbionts in Mediterranean Ircinia spp. FEMS Microbiol. Ecol. 2012, 79, 619-637.
35. Erwin, P.M.; Pita, L.; López-Legentil, S.; Turon, X. Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl. Environ. Microbiol. 2012, 78, 7358-7368.
36. Erwin, P.M.; López-Legentil, S.; Turon, X. Ultrastructure, molecular phylogenetics, and chlorophyll a content of novel cyanobacterial symbionts in temperate sponges. Microb. Ecol. 2012, 64, 771-783.
37. Esteves, A.I.S.; Hardoim, C.C.P.; Xavier, J.R.; Gonçalves, J.M.S.; Costa, R. Molecular richness and biotechnological potential of bacteria cultured from Irciniidae sponges in the north-east Atlantic. FEMS Microbiol. Ecol. 2013, 85, 519-536.
38. Hardoim, C.C.P.; Esteves, A.I.S.; Pires, F.R.; Gonçalves, J.M.S.; Cox, C.J.; Xavier, J.R.; Costa, R. Phylogenetically and spatially close marine sponges harbour divergent bacterial communities. PLoS One 2012, 7, e53029.
39. Pita, L.; Turon, X.; López-Legentil, S.; Erwin, P.M. Host rules: Spatial stability of bacterial communities associated with marine sponges (Ircinia spp.) in the western Mediterranean Sea. FEMS Microbiol. Ecol. 2013, 86, 268-276.
40. Usher, K.; Kuo, J.; Fromont, J.; Toze, S.; Sutton, D. Comparative morphology of five species of symbiotic and non-symbiotic coccoid Cyanobacteria. Eur. J. Phycol. 2006, 41, 179-188.
41. Wilkinson, C.R. Microbial associations in sponges. III. Ultrastructure of in situ associations in coral-reef sponges. Mar. Biol. 1978, 49, 177-185.
42. Webster, N.S.; Hill, R.T. The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an alpha-proteobacterium. Mar. Biol. 2001, 138, 843-851.
43. Hentschel, U.; Usher, K.M.; Taylor, M.W. Marine sponges as microbial fermenters. FEMS Microbiol. Ecol. 2006, 55, 167-177.
44. Hardoim, C.C.P.; Costa, R.; Araújo, F.V.; Hajdu, E.; Peixoto, R.; Lins, U.; Rosado, A.S.; van Elsas, J.D. Diversity of bacteria in the marine sponge Aplysina fulva in Brazilian coastal waters. Appl. Environ. Microbiol. 2009, 75, 3331-3343.
45. Kamke, J.; Taylor, M.W.; Schmitt, S. Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs. 16S rRNA gene comparisons. ISME J. 2010, 4, 498-508.
46. Sara, M. Ultrastructural aspects of symbiosis between two species of genus Aphanocapsa (Cyanophyceae) and Ircinia variabilis (Demospongiae). Mar. Biol. 1971, 11, 214-221.
47. Wilkinson, C.R. Microbial associations in sponges. I. Ecology, physiology and microbial-populations of coral-reef sponges. Mar. Biol. 1978, 49, 161-167.
48. Wilkinson, C.R. Microbial associations in sponges. II. Numerical-analysis of sponge and water bacterial populations. Mar. Biol. 1978, 49, 169-176.
49. Hentschel, U.; Schmid, M.; Wagner, M.; Fieseler, L.; Gernert, C.; Hacker, J. Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol. Ecol. 2001, 35, 305-312.
50. Muscholl-Silberhorn, A.; Thiel, V.; Imhoff, J.F. Abundance and bioactivity of cultured sponge-associated bacteria from the Mediterranean Sea. Microb. Ecol. 2008, 55, 94-106.
51. Thiel, V.; Imhoff, J.F. Phylogenetic identification of bacteria with antimicrobial activities isolated from Mediterranean sponges. Biomol. Eng. 2003, 20, 421-423.
52. Enticknap, J.J.; Kelly, M.; Peraud, O.; Hill, R.T. Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl. Environ. Microbiol. 2006, 72, 3724-3732.
53. O'Halloran, J.A.; Barbosa, T.M.; Morrissey, J.P.; Kennedy, J.; O'Gara, F.; Dobson, A.D.W. Diversity and antimicrobial activity of Pseudovibrio spp. from Irish marine sponges. J. Appl. Microbiol. 2011, 110, 1495-1508.
54. Tabares, P.; Pimentel-Elardo, S.M.; Schirmeister, T.; Huenig, T.; Hentschel, U. Anti-protease and immunomodulatory activities of bacteria associated with Caribbean sponges. Mar. Biotechnol. 2011, 13, 883-892.
55. Friedrich, A.B.; Fischer, I.; Proksch, P.; Hacker, J.; Hentschel, U. Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol. Ecol. 2001, 38, 105-113.
56. Hugenholtz, P. Exploring prokaryotic diversity in the genomic era. Genome Biol. 2002, 3, doi:10.1186/gb-2002-3-2-reviews0003.
57. Usher, K.; Fromont, J.; Sutton, D.; Toze, S. The biogeography and phylogeny of unicellular cyanobacterial symbionts in sponges from Australia and the Mediterranean. Microb. Ecol. 2004, 48, 167-177.
58. Schmitt, S.; Angermeier, H.; Schiller, R.; Lindquist, N.; Hentschel, U. Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl. Environ. Microbiol. 2008, 74, 7694-7708.
59. Stabili, L.; Cardone, F.; Alifano, P.; Tredici, S.M.; Piraino, S.; Corriero, G.; Gaino, E. Epidemic mortality of the sponge Ircinia variabilis (Schmidt, 1862) associated to proliferation of a Vibrio bacterium. Microb. Ecol. 2012, 64, 802-813.
60. Lee, O.O.; Wang, Y.; Yang, J.K.; Lafi, F.F.; Al-Suwailem, A.; Qian, P.Y. Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J. 2011, 5, 650-664.
61. Hardoim, C.C.P.; Cardinale, M.; Cúcio, A.; Esteves, A.I.S.; Berg, G.; Xavier, J.R.; Cox, C.; Costa, R. Bacterial cultivation bias examined for keratose marine sponges. Unpublised work, 2014.
62. Hardoim, C.C.P.; Costa, R. Temporal dynamics of prokaryotic communities in the marine sponge Sarcotragus spinosulus. Mol. Ecol. 2014. 23, 3097-3112.
63. Fiore, C.L.; Jarett, J.K.; Olson, N.D.; Lesser, M.P. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 2010, 18, 455-463.
64. Zehr, J.P.; Mellon, M.T.; Zani, S. New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl. Environ. Microbiol. 1998, 64, 3444-3450.
65. Zehr, J.P.; Jenkins, B.D.; Short, S.M.; Steward, G.F. Nitrogenase gene diversity and microbial community structure: A cross-system comparison. Environ. Microbiol. 2003, 5, 539-554.
66. Man-Aharonovich, D.; Kress, N.; Bar Zeev, E.; Berman-Frank, I.; Beja, O. Molecular ecology of nifH genes and transcripts in the eastern Mediterranean Sea. Environ. Microbiol. 2007, 9, 2354-2363.
67. Thakur, N.; Anil, A. Antibacterial activity of the sponge Ircinia ramosa: Importance of its surface-associated bacteria. J. Chem. Ecol. 2000, 26, 57-71.
68. Thakur, N.; Anil, A.; Müller, W. Culturable epibacteria of the marine sponge Ircinia fusca: Temporal variations and their possible role in the epibacterial defense of the host. Aquat. Microb. Ecol. 2004, 37, 295-304.
69. Pandey, S.; Sree, A.; Dash, S.S.; Sethi, D.P.; Chowdhury, L. Diversity of marine bacteria producing beta-glucosidase inhibitors. Microb. Cell. Fact. 2013, 12, doi:10.1186/1475-2859-12-35.
70. Asano, N. Glycosidase inhibitors: Update and perspectives on practical use. Glycobiology 2003, 13, 93R-104R.
71. De Rosa, S.; Mitova, M.; Tommonaro, G. Marine bacteria associated with sponge as source of cyclic peptides. Biomol. Eng. 2003, 20, 311-316.
72. Holden, M.T.G.; Chhabra, S.R.; de Nys, R.; Stead, P.; Bainton, N.J.; Hill, P.J.; Manefield, M.; Kumar, N.; Labatte, M.; England, D.; et al. Quorum-sensing cross talk: Isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol. Microbiol. 1999, 33, 1254-1266.
73. Degrassi, G.; Aguilar, C.; Bosco, M.; Zahariev, S.; Pongor, S.; Venturi, V. Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: Cross-talk with quorum sensing bacterial sensors. Curr. Microbiol. 2002, 45, 250-254.
74. Kalinovskaya, N.; Kuznetsova, T.; Rashkes, Y.; Milgrom, Y.; Milgrom, E.; Willis, R.; Wood, A.; Kurtz, H.; Carabedian, C.; Murphy, P.; et al. Surfactin-like structures of five cyclic depsipeptides from the marine isolate of Bacillus pumilus. Russ. Chem. Bull. 1995, 44, 951-955.
75. Prokof'eva, N.; Kalinovskaya, N.; Luk'yanov, P.; Shentsova, E.; Kuznetsova, T. The membranotropic activity of cyclic acyldepsipeptides from bacterium Bacillus pumilus, associated with the marine sponge Ircinia sp. Toxicon 1999, 37, 801-813.
76. Simister, R.L.; Deines, P.; Botte, E.S.; Webster, N.S.; Taylor, M.W. Sponge-specific clusters revisited: A comprehensive phylogeny of sponge-associated microorganisms. Environ. Microbiol. 2012, 14, 517-524.
77. Brochier-Armanet, C.; Boussau, B.; Gribaldo, S.; Forterre, P. Mesophilic crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 2008, 6, 245-252.
78. Spang, A.; Hatzenpichler, R.; Brochier-Armanet, C.; Rattei, T.; Tischler, P.; Spieck, E.; Streit, W.; Stahl, D.A.; Wagner, M.; Schleper, C. Distinct gene set in two different lineages of ammonia-oxidizing Archaea supports the phylum Thaumarchaeota. Trends Microbiol. 2010, 18, 331-340.
79. Pester, M.; Schleper, C.; Wagner, M. The Thaumarchaeota: An emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 2011, 14, 300-306.
80. Lee, E.Y.; Lee, H.K.; Lee, Y.K.; Sim, C.J.; Lee, J.H. Diversity of symbiotic archaeal communities in marine sponges from Korea. Biomol. Eng. 2003, 20, 299-304.
81. Webster, N.S.; Watts, J.E.M.; Hill, R.T. Detection and phylogenetic analysis of novel crenarchaeote and euryarchaeote 16S ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar. Biotechnol. 2001, 3, 600-608.
82. Webster, N.S.; Negri, A.P.; Munro, M.; Battershill, C.N. Diverse microbial communities inhabit Antarctic sponges. Environ. Microbiol. 2004, 6, 288-300.
83. Hoffmann, F.; Radax, R.; Woebken, D.; Holtappels, M.; Lavik, G.; Rapp, H.T.; Schlappy, M.L.; Schleper, C.; Kuypers, M.M.M. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 2009, 11, 2228-2243.
84. Han, M.Q.; Liu, F.; Zhang, F.L.; Li, Z.Y.; Lin, H.W. Bacterial and archaeal symbionts in the south China Sea sponge Phakellia fusca: Community structure, relative abundance, and ammonia-oxidizing populations. Mar. Biotechnol. 2012, 14, 701-713.
85. Cardoso, J.; van Bleijswijk, J.D.L.; Witte, H.; van Duyl, F.C. Diversity and abundance of ammonia-oxidizing Archaea and Bacteria in tropical and cold-water coral reef sponges. Aquat. Microb. Ecol. 2013, 68, 215-230.
86. Höller, U.; Wright, A.D.; Matthee, G.F.; Konig, G.M.; Draeger, S.; Aust, H.J.; Schulz, B. Fungi from marine sponges: Diversity, biological activity and secondary metabolites. Mycol. Res. 2000, 104, 1354-1365.
87. Paz, Z.; Komon-Zelazowska, M.; Druzhinina, I.S.; Aveskamp, M.M.; Shnaiderman, A.; Aluma, Y.; Carmeli, S.; Ilan, M.; Yarden, O. Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge. Fungal Divers. 2010, 42, 17-26.
88. Bringmann, G.; Lang, G.; Gulder, T.; Tsuruta, H.; Muhlbacher, J.; Maksimenka, K.; Steffens, S.; Schaumann, K.; Stohr, R.; Wiese, J.; et al. The first sorbicillinoid alkaloids, the antileukemic sorbicillactones A and B, from a sponge-derived Penicillium chrysogenum strain. Tetrahedron 2005, 61, 7252-7265.
89. Ereskovsky, A.V.; Gonobobleva, E.; Vishnyakov, A. Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar. Biol. 2005, 146, 869-875.
90. Sharp, K.H.; Eam, B.; Faulkner, D.J.; Haygood, M.G. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl. Environ. Microbiol. 2007, 73, 622-629.
91. Lee, O.O.; Chui, P.Y.; Wong, Y.H.; Pawlik, J.R.; Qian, P.Y. Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl. Environ. Microbiol. 2009, 75, 6147-6156.
92. Lindquist, N.; Bolser, R.; Laing, K. Timing of larval release by two Caribbean demosponges. Mar. Ecol. 1997, 155, 309-313.
93. Lopanik, N.; Lindquist, N.; Targett, N. Potent cytotoxins produced by a microbial symbiont protect host larvae from predation. Oecologia 2004, 139, 131-139.
94. Lopanik, N.; Gustafson, K.R.; Lindquist, N. Structure of bryostatin 20: A symbiont-produced chemical defense for larvae of the host bryozoan, Bugula neritina. J. Nat. Prod. 2004, 67, 1412-1414.
95. Lopanik, N.B.; Targett, N.M.; Lindquist, N. Isolation of two polyketide synthase gene fragments from the uncultured microbial symbiont of the marine bryozoan Bugula neritina. Appl. Environ. Microbiol. 2006, 72, 7941-7944.
96. Lopanik, N.B.; Shields, J.A.; Buchholz, T.J.; Rath, C.M.; Hothersall, J.; Haygood, M.G.; Hakansson, K.; Thomas, C.M.; Sherman, D.H. In vivo and in vitro trans-acylation by BryP, the putative bryostatin pathway acyltransferase derived from an uncultured marine symbiont. Chem. Biol. 2008, 15, 1175-1186.
97. Sudek, S.; Lopanik, N.B.; Waggoner, L.E.; Hildebrand, M.; Anderson, C.; Liu, H.B.; Patel, A.; Sherman, D.H.; Haygood, M.G. Identification of the putative bryostatin polyketide synthase gene cluster from "Candidatus Endobugula sertula", the uncultivated microbial symbiont of the marine bryozoan Bugula neritina. J. Nat. Prod. 2007, 70, 67-74.
98. Jaeckle, W.B. 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. 1995, 189, 159-167.
99. Bandara, H.; Lam, O.L.T.; Jin, L.J.; Samaranayake, L. Microbial chemical signaling: A current perspective. Crit. Rev. Microbiol. 2012, 38, 217-249.
100. Kalia, V.C. Quorum sensing inhibitors: An overview. Biotechnol. Adv. 2013, 31, 224-245.
101. Skindersoe, M.E.; Ettinger-Epstein, P.; Rasmussen, T.B.; Bjarnsholt, T.; de Nys, R.; Givskov, M. Quorum sensing antagonism from marine organisms. Mar. Biotechnol. 2008, 10, 56-63.
102. Dobretsov, S.; Teplitski, M.; Bayer, M.; Gunasekera, S.; Proksch, P.; Paul, V.J. Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling 2011, 27, 893-905.
103. Dieckmann, R.; Graeber, I.; Kaesler, I.; Szewzyk, U.; von Dohren, H. Rapid screening and dereplication of bacterial isolates from marine sponges of the Sula Ridge by Intact-Cell-MALDI-TOF mass spectrometry (ICM-MS). Appl. Microbiol. Biotechnol. 2005, 67, 539-548.
104. Anand, T.P.; Bhat, A.W.; Shouche, Y.S.; Roy, U.; Siddharth, J.; Sarma, S.P. Antimicrobial activity of marine bacteria associated with sponges from the waters off the coast of south east India. Microbiol. Res. 2006, 161, 252-262.
105. Hoffmann, M.; Fischer, M.; Ottesen, A.; McCarthy, P.J.; Lopez, J.V.; Brown, E.W.; Monday, S.R. Population dynamics of Vibrio spp. associated with marine sponge microcosms. ISME J. 2010, 4, 1608-1612.
106. Flemer, B.; Kennedy, J.; Margassery, L.M.; Morrissey, J.P.; O'Gara, F.; Dobson, A.D.W. Diversity and antimicrobial activities of microbes from two Irish marine sponges, Suberites carnosus and Leucosolenia sp. J. Appl. Microbiol. 2012, 112, 289-301.
107. Webster, N.S. Sponge disease: A global threat? Environ. Microbiol. 2007, 9, 1363-1375.
108. Gaino, E.; Pronzato, R.; Corriero, G.; Buffa, P. Mortality of commercial sponges-Incidence in two Mediterranean areas. Boll. Zool. 1992, 59, 79-85.
109. Wulff, J.L. Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biol. Conserv. 2006, 127, 167-176.
110. Maldonado, M.; Sanchez-Tocino, L.; Navarro, C. Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: Epidemic incidence and defense mechanisms. Mar. Biol. 2010, 157, 1577-1590.
111. Cebrian, E.; Uriz, M.J.; Garrabou, J.; Ballesteros, E. Sponge mass mortalities in a warming Mediterranean sea: Are Cyanobacteria-harboring species worse off? PLoS One 2011, 6, e20211.
112. di Camillo, C.G.; Bartolucci, I.; Cerrano, C.; Bavestrello, G. Sponge disease in the Adriatic Sea. Mar. Ecol. 2013, 34, 62-71.
113. Pita, L.; Erwin, P.M.; Turon, X.; López-Legentil, S. Till death do us part: Stable sponge-bacteria associations under thermal and food shortage stresses. PLoS One 2013, 8, e80307.
114. Luter, H.M.; Whalan, S.; Webster, N.S. Prevalence of tissue necrosis and brown spot lesions in a common marine sponge. Mar. Freshw. Res. 2010, 61, 484-489.
115. Mohamed, N.M.; Enticknap, J.J.; Lohr, J.E.; McIntosh, S.M.; Hill, R.T. Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl. Environ. Microbiol. 2008, 74, 1209-1222.
116. Isaacs, L.T.; Kan, J.J.; Nguyen, L.; Videau, P.; Anderson, M.A.; Wright, T.L.; Hill, R.T. Comparison of the bacterial communities of wild and captive sponge Clathria prolifera from the Chesapeake Bay. Mar. Biotechnol. 2009, 11, 758-770.
117. Thomas, T.; Rusch, D.; DeMaere, M.Z.; Yung, P.Y.; Lewis, M.; Halpern, A.; Heidelberg, K.B.; Egan, S.; Steinberg, P.D.; Kjelleberg, S. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 2010, 4, 1557-1567.
118. Fan, L.; Reynolds, D.; Liu, M.; Stark, M.; Kjelleberg, S.; Webster, N.S.; Thomas, T. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc. Natl. Acad. Sci. USA 2012, 109, E1878-E1887.
119. Simister, R.; Taylor, M.W.; Tsai, P.; Fan, L.; Bruxner, T.J.; Crowe, M.L.; Webster, N. Thermal stress responses in the bacterial biosphere of the Great Barrier Reef sponge Rhopaloeides odorabile. Environ. Microbiol. 2012, 14, 3232-3246.
120. Webster, N.; Pantile, R.; Botte, E.; Abdo, D.; Andreakis, N.; Whalan, S. A complex life cycle in a warming planet: Gene expression in thermally stressed sponges. Mol. Ecol. 2013, 22, 1854-1868.
121. Duckworth, A.R.; Peterson, B.J. Effects of seawater temperature and pH on the boring rates of the sponge Cliona celata in scallop shells. Mar. Biol. 2013, 160, 27-35.
122. Staunton, J.; Weissman, K.J. Polyketide biosynthesis: A millennium review. Nat. Prod. Rep. 2001, 18, 380-416.
123. Piel, J.; Butzke, D.; Fusetani, N.; Hui, D.Q.; Platzer, M.; Wen, G.P.; Matsunaga, S. Exploring the chemistry of uncultivated bacterial symbionts: Antitumor polyketides of the pederin family. J. Nat. Prod. 2005, 68, 472-479.
124. Schirmer, A.; Gadkari, R.; Reeves, C.D.; Ibrahim, F.; DeLong, E.F.; Hutchinson, C.R. Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl. Environ. Microbiol. 2005, 71, 4840-4849.
125. Siegl, A.; Kamke, J.; Hochmuth, T.; Piel, J.; Richter, M.; Liang, C.G.; Dandekar, T.; Hentschel, U. Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 2011, 5, 61-70.
126. Fisch, K.; Gurgui, C.; Heycke, N.; van der Sar, S.; Anderson, S.; Webb, V.; Taudien, S.; Platzer, M.; Rubio, B.; Robinson, S.; et al. Polyketide assembly lines of uncultivated sponge symbionts from structure-based gene targeting. Nat. Chem. Biol. 2009, 5, 494-501.
127. Hochmuth, T.; Niederkruger, H.; Gernert, C.; Siegl, A.; Taudien, S.; Platzer, M.; Crews, P.; Hentschel, U.; Piel, J. Linking chemical and microbial diversity in marine sponges: Possible role for Poribacteria as producers of methyl-branched fatty acids. Chembiochem 2010, 11, 2572-2578.
128. Osinga, R.; Tramper, J.; Wijffels, R.H. Cultivation of marine sponges. Mar. Biotechnol. 1999, 1, 509-532.
129. Rinkevich, B. Marine invertebrate cell cultures: New millennium trends. Mar. Biotechnol. 2005, 7, 429-439.
130. Sipkema, D.; Osinga, R.; Schatton, W.; Mendola, D.; Tramper, J.; Wijffels, R.H. Large-scale production of pharmaceuticals by marine sponges: Sea, cell, or synthesis? Biotechnol. Bioeng. 2005, 90, 201-222.
131. Wilkinson, C.R.; Vacelet, J. Transplantation of marine sponges to different conditions of light and current. J. Exp. Mar. Biol. Ecol. 1979, 37, 91-104.
132. Duckworth, A.; Battershill, C.; Bergquist, P. Influence of explant procedures and environmental factors on culture success of three sponges. Aquaculture 1997, 156, 251-267.
133. Van Treeck, P.; Eisinger, M.; Müller, J.; Paster, M.; Schuhmacher, H. Mariculture trials with Mediterranean sponge species-The exploitation of an old natural resource with sustainable and novel methods. Aquaculture 2003, 218, 439-455.
134. De Voogd, N. An assessment of sponge mariculture potential in the Spermonde Archipelago, Indonesia. J. Mar. Biol. Assoc. UK 2007, 396, 1777-1784.
135. De Rosa, S.; de Caro, S.; Tommonaro, G.; Slantchev, K.; Stefanov, K.; Popov, S. Development in a primary cell culture of the marine sponge Ircinia muscarum and analysis of the polar compounds. Mar. Biotechnol. 2001, 3, 281-286.
136. De Rosa, S.; Tommonaro, G.; Slantchev, K.; Stefanov, K.; Popov, S. Lipophylic metabolites from the marine sponge Ircinia muscarum and its cell cultures. Mar. Biol. 2002, 140, 465-470.
137. De Rosa, S.; de Caro, S.; Iodice, C.; Tommonaro, G.; Stefanov, K.; Popov, S. Development in primary cell culture of demosponges. J. Biotechnol. 2003, 100, 119-125.
138. De Caralt, S.; Uriz, M.J.; Wijffels, R.H. Cell culture from sponges: Pluripotency and immortality. Trends Biotechnol. 2007, 25, 467-471.
139. Piel, J.; Hui, D.Q.; Wen, G.P.; Butzke, D.; Platzer, M.; Fusetani, N.; Matsunaga, S. Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc. Natl. Acad. Sci. USA 2004, 101, 16222-16227.
140. Liu, M.; Fan, L.; Zhong, L.; Kjelleberg, S.; Thomas, T. Metaproteogenomic analysis of a community of sponge symbionts. ISME J. 2012, 6, 1515-1525.
141. Kamke, J.; Sczyrba, A.; Ivanova, N.; Schwientek, P.; Rinke, C.; Mavromatis, K.; Woyke, T.; Hentschel, U. Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges. ISME J. 2013, 7, 2287-2300.