Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular evidence for metabolic interchange

Frontiers in Microbiology

Volumn 6, Issue APR, 2015, Pages

  Fiore, Cara L ^a,b   Labrie, Micheline ^a,c   Jarett, Jessica K ^a,d   Lesser, Michael P ^a  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^c UNIVERSITY OF MASSACHUSETTS DARTMOUTH   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

Author keywords

Ammonia oxidation; B vitamins; Denitrification; Metatranscriptome; Sponge symbionts

Indexed keywords

TRANSCRIPTOME;

ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; GENE AMPLIFICATION; GENE EXPRESSION; GENE ONTOLOGY; GENE SEQUENCE; GENETIC TRANSCRIPTION; MOLECULAR CLONING; NITROGEN CYCLING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SYMBIONT; XESTOSPONGIA; XESTOSPONGIA MUTA;

ANTHOZOA; ARCHAEA; PROKARYOTA; XESTOSPONGIA MUTA;

EID: 84930936816     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00364     Document Type: Article

References (100)

1. Antal, T. K., and Lindblad, P. (2005). Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. J. Appl. Microbiol. 98, 114-120. doi: 10.1111/j.1365-2672.2004.02431.x.
2. Arillo, A., Bavestrello, G., Burlando, B., and Sarà, M. (1993). Metabolic integration between symbiotic cyanobacteria and sponges: a possible mechanism. Marine Biol. 117, 159-162. doi: 10.1007/BF00346438.
3. Bagwell, C. E., Piskorska, M., Soule, T., Petelos, A., and Yeager, C. M. (2014). A diverse assemblage of indole-3-acetate producing bacteria associate with unicellular green algae. Appl. Biochem. Biotech. 173, 1977-1984. doi: 10.1007/s12010-014-0980-5.
4. Boyer, J. N., Dailey, S. K., Gibson, P. J., Rogers, M. T., and Mir-Gonzalez, D. (2006). The role of dissolved organic matter bioavailability in promoting phytoplankton blooms in Florida Bay. Hydrobiologia 569, 71-85. doi: 10.1007/s10750-006-0123-2.
5. Braker, G., Fesefeldt, A., and Witzel, K.-P. (1998). Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl. Environ. Microbiol. 64, 3769-3775.
6. Braker, G., and Tiedje, J. M. (2003). Nitric Oxide Reductase (norB) genes from pure cultures and environmental samples. Appl. Environ. Microbiol. 69, 3476-3483. doi: 10.1128/AEM.69.6.3476-3483.2003.
7. Calvo, L., Cortey, M., García-Marín, J.-L., and Garcia-Gil, L. J. (2005). Polygenic analysis of ammonia-oxidizing bacteria using 16S rDNA, amoA, and amoB genes. Interntl. Microbiol. 8, 103-110. Available online at: http://www.im.microbios.org/0802/0802103.pdf.
8. Chen, T.-W., Gan, R.-C. R., Wu, T. H., Huang, P.-J., Lee, C.-Y., Chen, Y.-Y. M., et al. (2012). FastAnnotator-an efficient transcript annotation web tool. BMC Genomics 13:S9. doi: 10.1186/1471-2164-13-S7-S9.
9. Chien, Y.-T., and Zinder, S. H. (1996). Cloning, functional organization, transcript studies, and phylogenetic analysis of the complete nitrogenase structural genes (nifHDK2) and associated genes in the archaeon Methanosarcina barkeri 227. J. Bacteriol. 178, 143-148.
10. Chistoserdova, L., Kalyuzhnaya, M. G., and Lidstrom, M. E. (2009). The expanding world of methylotrophic metabolism. Ann. Rev. Microbiol. 63, 477-499. doi: 10.1146/annurev.micro.091208.073600.
11. Conaco, C., Neveu, P., Zhou, H., Arcila, M. L., Degnan, S. M., Degnan, B. M., et al. (2012). Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions. BMC Genomics 13:209. doi: 10.1186/1471-2164-13-209.
12. de Goeij, J. M., van Oevelen, D., Vermeij, M. J. A., Osinga, R., Middelburg, J. J., de Goeij, A. F. P. M., et al. (2013). Surviving in a Marine Desert: the sponge loop retains resources within coral reefs. Science 342, 108-110. doi: 10.1126/science.1241981.
13. D'Elia, C. F., and Wiebe, W. J. (1990). "Biogeochemical nutrient cycles in coral-reef ecosystems," in Coral Reefs Ecosystems of the World, Vol. 25 ed Z. Dubinsky (New York, NY: Elsevier), 49-74.
14. De Wit, P., Pespeni, M. H., Ladner, J. T., Barshis, D. J., Seneca, F., Jaris, H., et al. (2012). The simple fool's guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis. Mol. Ecol. Resour. 12, 1058-1067. doi: 10.1111/1755-0998.12003.
15. Diaz, C. M., and Rutzler, K. (2001). Sponges: an essential component of Caribbean coral reefs. Bull. Mar. Sci. 69, 535-546. doi: 10.3354/dao071163.
16. Diaz, M., and Ward, B. (1997). Sponge-mediated nitrification in tropical benthic communities. Mar. Ecol. Prog. Ser. 156, 97-107. doi: 10.3354/meps156097.
17. Dillon, R. J., and Dillon, V. M. (2004). The gut bacteria of insects: nonpathogenic interactions. Ann. Rev. Entomol. 49, 71-92. doi: 10.1146/annurev.ento.49.061802.123416.
18. Doxey, A. C., Kurtz, D. A., Lynch, M. D. J., Sauder, L. A., and Neufeld, J. D. (2014). Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production. ISME J. 9, 461-471. doi: 10.1038/ismej.2014.142.
19. Erwin, P. M., and Thacker, R. W. (2007). Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge asemblages. J. Marine Biol. Assoc. U.K. 87, 1687-1692. doi: 10.1017/S0025315407058213.
20. Erwin, P. M., and Thacker, R. W. (2008). Phototrophic nutrition and symbiont diversity of two Caribbean spponge-cyanobacteria symbioses. Mar. Ecol. Prog. Ser. 362, 139-147. doi: 10.3354/meps07464.
21. Fan, L., Reynolds, D., Liu, M., Stark, M., Kjelleberg, S., Webster, N. S., et al. (2012). Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc. Natl. Acad. Sci. U.S.A. 109, E1878-E1887. doi: 10.1073/pnas.1203287109.
22. Fiore, C. L., Baker, D. M., and Lesser, M. P. (2013a). Nitrogen biogeochemistry in the Caribbean sponge, Xestospongia muta: a source or sink of dissolved inorganic nitrogen? PLoS ONE 8:e72961. doi: 10.1371/journal.pone.0072961.
23. Fiore, C. L., Jarett, J. K., and Lesser, M. P. (2013b). Symbiotic prokaryotic communities from different populations of the giant barrel sponge, Xestospongia muta. Microbiologyopen 2, 938-952. doi: 10.1002/mbo3.135.
24. Fiore, C. L., Jarett, J. K., Olson, N. D., and Lesser, M. P. (2010). Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 18, 455-463. doi: 10.1016/j.tim.2010.07.001.
25. Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E., and Oakley, B. B. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. U.S.A. 102, 14683-14688. doi: 10.1073/pnas.0506625102.
26. Freeman, C. J., and Thacker, R. W. (2011). Complex interactions between marine sponges and their symbiotic microbial communities. Limnol. Oceangr. 56, 1577-1586. doi: 10.4319/lo.2011.56.5.1577.
27. Frias-Lopez, J., Shi, Y., Tyson, G. W., Coleman, M. L., Schuster, S. C., Chrisholm, S. W., et al. (2008). Microbial community gene expression in ocean surface waters. Proc. Natl. Acad. Sci. U.S.A. 105, 3805-3810. doi: 10.1073/pnas.0708897105.
28. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644-652. doi: 10.1038/nbt.1883.
29. Hallam, S. J., Konstantinidis, K. T., Putnam, N., Schleper, C., Watanabe, Y.-I., Sugahara, J., et al. (2006a). Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. U.S.A. 103, 18296-18301. doi: 10.1073/pnas.0608549103.
30. Hallam, S. J., Mincer, T. J., Schleper, C., Preston, C. M., Roberts, K., Richardson, P. M., et al. (2006b). Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine crenarchaeota. PLoS Biol. 4:e95. doi: 10.1371/journal.pbio.0040095.
31. Hamada, M., Shoguchin, E., Shinzato, C., Kawashima, T., Miller, D. J., and Satoh, N. (2013). The complex NOD-Like receptor repertoire of the coral Acropora digitifera includes novel domain combinations. Mol. Biol. Evol. 30, 167-176. doi: 10.1093/molbev/mss213.
32. Hentschel, U., Fieseler, L., Wehrl, M., Gernert, C., Steinert, M., Horn, M., et al. (2003). "Microbial diversity of marine sponges," in Sponges (Porifera), ed W. E. G. Müller (Heidelberg: Springer), 59-88.
33. 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. doi: 10.1038/nrmicro2839.
34. Hoffmann, F., Radax, R., Woebken, D., Holtappels, M., Lavik, G., Rapp, H. T., et al. (2009). Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11, 2228-2243. doi: 10.1111/j.1462-2920.2009.01944.x.
35. Huson, D. H., Auch, A. F., Qi, J., and Schuster, S. C. (2007). MEGAN analysis of metagenomic data. Gen. Res. 17, 377-386. doi: 10.1101/gr.5969107.
36. Jarett, J. (2012). Effects of Nitrogen-Fixing Symbiotic Bacteria on the Microbial Ecology of the Coral Montastrea Cavernosa. Ph.D. dissertation. University of New Hampshire, Durham, NH.
37. Junier, P., Kim, O.-S., Hadas, O., Imhoff, J. F., and Witzel, K.-P. (2008). Evaluation of PCR primer selectivity and phylogenetic specificity by using amplification of 16S rRNA genes from Betaproteobacterial ammonia-oxidizing bacteria in environmental samples. Appl. Environ. Microbiol. 74, 5231-5236. doi: 10.1128/AEM.00288-08.
38. Kamke, J., Taylor, M. W., and Schmitt, S. (2010). Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. ISME J. 4, 498-508. doi: 10.1038/ismej.2009.143.
39. Kanehisa, M., and Goto, S. (2000). KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucl. Acid. Res. 28, 27-30. doi: 10.1093/nar/28.1.27.
40. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., and Tanabe, M. (2011). KEGG for integration and interpretation of large-scale molecular data sets. Nucl. Acid. Res. 40, D109-D114. doi: 10.1093/nar/gkr988.
41. Kennedy, J., Flemer, B., Jackson, S. A., Morrisssey, J. P., O'Gara, F., and Dobson, A. D. W. (2014). Evidence of putative deep sea specific microbiome in marine sponges. PLoS ONE 9:e91092. doi: 10.1371/journal.pone.0091092.
42. Knapp, A. (2012). The sensitivity of marine N2 fixation to dissolved inorganic nitrogen. Front. Microbiol. 3:374. doi: 10.3389/fmicb.2012.00374.
43. Kvennefors, E. C. E., Leggat, W., Kerr, C. C., Ainsworth, T. D., Hoegh-Guldberg, O., and Barnes, A. C. (2010). Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Devel. Compar. Immunol. 34, 1219-1229. doi: 10.1016/j.dci.2010.06.016.
44. Lee, O. O., Wong, Y. H., and Qian, P. Y. (2009). Inter-and intraspecific variations of bacterial communities associated with marine sponges from San Juan Island, Washington. Appl. Environ. Microbiol. 75, 3513-3521. doi: 10.1128/AEM.00002-09.
45. Lesser, M. P. (2006). Benthic-pelagic coupling on coral reefs: feeding and growth of Caribbean sponges. J. Exper. Mar. Biol. Ecol. 328, 277-288. doi: 10.1016/j.jembe.2005.07.010.
46. Lesser, M. P., Stat, M., and Gates, R. D. (2013). The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32, 603-611. doi: 10.1007/s00338-013-1051-z.
47. Li, Z.-Y., Wang, Y.-Z., He, L.-M., and Zheng, H.-J. (2014). Metabolic profiles of prokaryotic and eukaryotic communities in deep-sea sponge Lamellomorpha sp. indicated by metagenomics. Sci. Rep. 4:3895. doi: 10.1038/srep03895.
48. Lopez-Legentil, S., Erwin, P. M., Pawlik, J. R., and Song, B. (2010). Effects of sponge bleaching on ammonia-oxidizing Archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongia muta. Micro. Ecol. 60, 561-571. doi: 10.1007/s00248-010-9662-1.
49. McCutcheon, J. P., and Moran, N. A. (2007). Parellel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl. Acad. Sci. U.S.A. 104, 19392-19397. doi: 10.1073/pnas.0708855104.
50. McMurray, S. E., Blum, J. E., and Pawlik, J. R. (2008). Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. Mar. Biol. 155, 159-171. doi: 10.1007/s00227-008-1014-z.
51. McMurray, S. E., Henkel, T. P., and Pawlik, J. R. (2010). Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology 91, 560-570. doi: 10.1890/08-2060.1.
52. Meyer, O., and Schlegel, H. G. (1983). Biology of aerobic carbon monoxide oxidizing bacteria. Ann. Rev. Microbiol. 37, 277-310. doi: 10.1146/annurev.mi.37.100183.001425.
53. Miller, C. S., Baker, B. J., Thomas, B. C., Singer, S. W., and Banfield, J. F. (2011). EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Gen. Biol. 12:R44. doi: 10.1186/gb-2011-12-5-r44.
54. Mohamed, N. M., Colman, A. S., Tai, Y., and Hill, R. T. (2008). Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environ. Microbiol. 10, 2910-2921. doi: 10.1111/j.1462-2920.2008.01704.x.
55. Moitinho-Silva, L., Seridi, L., Ryu, T., Voolstra, C. R., Ravasi, T., and Hentschel, U. (2014). Revealing microbial functional activities in the Red Sea sponge Stylissa carteriby metatranscriptomics. Environ. Microbiol. 16, 3683-3698. doi: 10.1111/1462-2920.12533.
56. Montalvo, N. F., Davis, J., Vicente, J., Pittiglio, R., Ravel, J., and Hill, R. T. (2014). Integration of culture-based and molecular analysis of a complex sponge-associated bacterial community. PLOS ONE 9:e90517. doi: 10.1371/journal.pone.0090517.
57. Montalvo, N. F., and Hill, R. T. (2011). Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl. Environ. Microbiol. 77, 7207-7216. doi: 10.1128/AEM.05285-11.
58. Muscatine, L., and Porter, J. W. (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454-460. doi: 10.2307/1297526.
59. Nichols, S. A., Dirks, W., Pearse, J. S., and King, N. (2006). Early evolution of animal cell signalling and adhesion genes. Proc. Natl. Acad. Sci. U.S.A. 103, 12451-12456. doi: 10.1073/pnas.0604065103.
60. Noyer-Weidner, M., and Trautner, T. A. (1993). "Methylation of DNA in prokaryotes," in DNA Methylation Molecular Biology and Biological Significance, eds J. P. Jost and H. P. Saluz (Basel: Birkhäuser), 39-108.
61. O'Brien, R. G. (1981). A simple test for variance effects in experimental designs. Psychol. Bull. 89, 570-574. doi: 10.1037/0033-2909.89.3.570.
62. Oelgeschläger, E., and Rother, M. (2008). Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea. Arch. Microbiol. 190, 257-269. doi: 10.1007/s00203-008-0382-6.
63. Ohkuma, M., and Kudo, T. (1996). Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl. Environ. Microbiol. 62:461-468.
64. Olson, J. B., Steppe, T. F., Litaker, R. W., and Paerl, H. W. (1998). N2-fixing microbial consortia associated with the ice cover of Lake Bonney, Antarctica. Micro. Ecol. 36, 231-238. doi: 10.1007/s002489900110.
65. Olson, N. D., Ainsworth, T. D., Gates, R. D., and Takabayashi, M. (2009). Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J. Exp. Mar. Biol. Ecol. 371, 140-146. doi: 10.1016/j.jembe.2009.01.012.
66. Olson, N. D., and Lesser, M. P. (2013). Diazotrophic diversity in the Caribbean coral, Montastraea cavernosa. Arch. Microbiol. 195, 853-859. doi: 10.1007/s00203-013-0937-z.
67. Parsek, M. R., and Greenberg, E. P. (2000). Acyl-homoserine lactone quorum sensing in Gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. U.S.A. 97, 8789-8793. doi: 10.1073/pnas.97.16.8789.
68. Prasanna, R., Kumar, V., Kumar, S., Yadav, A. K., Tripathi, U., et al. (2002). Methane production in rice soil is inhibited by cyanobacteria. Microbiol. Res. 157, 1-6. doi: 10.1078/0944-5013-00124.
69. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl. Acid. Res. 41, D590-D596. doi: 10.1093/nar/gks1219.
70. Radax, R., Rattei, T., Lanzen, A., Bayer, C., Rapp, H. T., Urich, T., et al. (2012). Metatranscriptomics of the marine sponge Geodia barretti: tackling phylogeny and function of its microbial community. Environ. Microbiol. 14, 1308-1324. doi: 10.1111/j.1462-2920.2012.02714.x.
71. Reiswig, H. M. (1971). In situ pumping activities of tropical Demospongiae. Mar. Biol. 9, 38-50. doi: 10.1007/BF00348816.
72. Riesgo, A., Farrar, N., Windsor, P. J., Giribet, G., and Leys, S. P. (2014). The analysis of eight transcriptomes from all Porifera classes reveals surprising genetic complexity in sponges. Mol. Biol. Evol. 31, 1102-1120. doi: 10.1093/molbev/msu057.
73. Roberts, K. L., Kessler, A. J., Grace, M. R., and Cook, P. L. M. (2014). Increased rates of dissimilatory nitrate reduction to ammonium (DNRA) under oxic conditions in a periodically hypoxic estuary. Geochim. Cosmo. Acta. 133, 313-324. doi: 10.1016/j.gca.2014.02.042.
74. Rotthauwe, J.-H., Witzel, K.-P., and Liesack, W. (1997). The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63, 4704-4712.
75. Royston, P. (1995). A remark on Algorithm AS 181: the W test for normality. Appl. Stat. 44, 547-551. doi: 10.2307/2986146.
76. Sañudo-Wilhelmy, S. A., Gómez-Consarnau, L., Suffridge, C., and Webb, E. A. (2014). The role of B vitamins in marine biogeochemistry. Ann. Rev. Mar. Sci. 6, 339-367. doi: 10.1146/annurev-marine-120710-100912.
77. Sayers, E. W., Barrett, T., Benson, D. A., Bolton, E., Bryant, S. H., Canese, K., et al. (2010). Database resources of the National Center for Biotechnology Information. Nucl. Acid. Res. 38, D5-D16. doi: 10.1093/nar/gkp967.
78. Schmid, M. C., Maas, M., Dapena, A., van de Pas-Schoonen, K., van de Vossenber, J., Kartal, B., et al. (2005). Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl. Environ. Microbiol. 71, 1677-1684. doi: 10.1128/AEM.71.4.1677-1684.2005.
79. Schmieder, R., and Edwards, R. (2011). Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863-864. doi: 10.1093/bioinformatics/btr026.
80. Schmitt, S., Tsai, P., Bell, J., Fromont, J., Ilan, M., Lindquist, N., et al. (2011). Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6, 564-576. doi: 10.1038/ismej.2011.116.
81. Seutin, G., White, B. N., and Boag, P. T. (1991). Preservation of avian blood and tissue samples for DNA analysis. Can. J. Zoo. 69, 82-90. doi: 10.1139/z91-013.
82. Shu, Q., and Jiao, N. (2008). New primers for amplification of the Planctomycetes 16S rRNA gene from environmental samples. J. Rap. Meth. Auto. Microbiol. 16, 330-336. doi: 10.1111/j.1745-4581.2008.00139.x.
83. Siegl, A., Kamke, J., Hochmuth, T., Piel, J. O. R., Richter, M., Liang, C., et al. (2011). Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 5, 61-70. doi: 10.1038/ismej.2010.95.
84. Simister, R. L., Deines, P., Botté, E. S., Webster, N. S., and Taylor, M. W. (2012). Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ. Microbiol. 14, 517-524. doi: 10.1111/j.1462-2920.2011.02664.x.
85. Southwell, M. W., Weisz, J. B., Martens, C. S., and Lindquist, N. (2008). In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnol. Oceangr. 53, 986-996. doi: 10.4319/lo.2008.53.3.0986.
86. Spaepen, S., Vanderleyden, J., and Remans, R. (2007). Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. 31, 425-448. doi: 10.1111/j.1574-6976.2007.00072.x.
87. Steger, D., Ettinger-Epstein, P., Whalan, S., Hentschel, U., De Nys, R., Wagner, M., et al. (2008). Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ. Microbiol. 10, 1087-1094. doi: 10.1111/j.1462-2920.2007.01515.x.
88. Steindler, L., Huchon, D., Avni, A., and Ilan, M. (2005). 16S rRNA phylogeny of sponge-associated cyanobacteria. Appl. Environ. Microbiol. 71, 4127-4131. doi: 10.1128/AEM.71.7.4127-4131.2005.
89. Sun, S., Chen, J., Li, W., Altintas, I., Lin, A., Peltier, S., et al. (2010). Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucl. Acid. Res. 39, D546-D551. doi: 10.1093/nar/gkq1102.
90. Taprab, Y., Johjima, T., Maeda, Y., Moriya, S., Trakulnaleamsai, S., Noparatnaraporn, N., et al. (2005). Symbiotic fungi produce laccases potentially involved in phenol degradation in fungus combs of fungus-growing termites in Thailand. Appl. Environ. Microbiol. 71, 7696-7704. doi: 10.1128/AEM.71.12.7696-7704.2005.
91. Taylor, M. W., Radax, R., Stegor, D., and Wagner, M. (2007). Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71, 1-53. doi: 10.1128/MMBR.00040-06.
92. Thomas, T., Rusch, D., DeMaere, M. Z., Yung, P. Y., Lewis, M., Halpern, A., et al. (2010). Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 3, 74. doi: 10.1038/ismej.2010.74.
93. Ulrich, T., Lanzén, A., Qi, J., Huson, D. H., Schleper, C., and Schuster, S. C. (2008). Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3:e2527. doi: 10.1371/journal.pone.0002527.
94. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267. doi: 10.1128/AEM.00062-07.
95. Webster, N. S., Taylor, M. W., Behnam, F., Lucker, S., Rattei, T., Whalen, S., et al. (2010). Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12, 2070-2082. doi: 10.1111/j.1462-2920.2009.02065.x.
96. Weisz, J. B., Lindquist, N., and Martens, C. S. (2008). Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 155, 367-376. doi: 10.1007/s00442-007-0910-0.
97. Wilkinson, C. (1979). Nutrient translocation from symbiotic cyanobacteria to coral reef sponges. Biol. spong. 291, 373-378.
98. Wilkinson, C., and Fay, P. (1979). Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature. 279, 527-529. doi: 10.1038/279527a0.
99. Zehr, J. P., and McReynolds, L. A. (1989). Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl. Environ. Microbiol. 55, 2522-2526.
100. Zhang, F., Vicente, J., and Hill, R. T. (2014). Temporal changes in the diazotrophic bacterial communities associated with Caribbean sponges Ircinia stroblina and Mycale laxissima. Front. Microbiol. 5:561. doi: 10.3389/fmicb.2014.00561.