16S rDNA-based metagenomic analysis of bacterial diversity associated with two populations of the kleptoplastic sea slug Elysia chlorotica and its algal prey vaucheria litorea

Biological Bulletin

Volumn 223, Issue 1, 2012, Pages 138-154

  Devine, Susan P ^a,b   Pelletreau, Karen N ^a,b   Rumpho, Mary E ^a  

^a UNIVERSITY OF MAINE   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; ALGA; BACTERIUM; CHLOROPLAST; DNA; ENDOSYMBIONT; GENOMICS; MICROBIAL COMMUNITY; NITROGEN FIXATION; PHOTOAUTOTROPHY; PREDATOR-PREY INTERACTION; SLUG;

ACTINOBACTERIA; ALGAE; ANIMALIA; BACILLI (CLASS); BACTERIA (MICROORGANISMS); ELYSIA CHLOROTICA; FLAVOBACTERIA; GAMMAPROTEOBACTERIA; OPISTHOBRANCHIA; SPHINGOBACTERIA; VAUCHERIA LITOREA;

EID: 84866411687     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/BBLv223n1p138     Document Type: Article

References (127)

1. Ashour, M., R. Edrada, R. Ebel, V. Wray, W. Wätjen, K. Padmakumar, W. E. G. Mü ller, W. H. Lin, and P. Proksch. 2006. Kahalalide derivatives from the Indian sacoglossan mollusk Elysia grandifolia. J. Nat. Prod. 69: 1547-1553.
2. Bent, S. J., and L. J. Forney. 2008. The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J. 2: 689-695.
3. Bernardet, J.-F., and Y. Nakagawa. 2006. An introduction to the family Flavobacteriaceae. Pp. 455-480 in The Prokaryotes, M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt, eds. Springer, New York.
4. Blunt, J. W., B. R. Copp, W-P. Hu, M. H. G. Munro, P. T. Northcote, and M. R. Prinsep. 2009. Marine natural products. Nat. Prod. Rep. 26: 170-244.
5. Bowman, J. P. 2006. The marine clade of the family Flavobacteriaceae: the genera Aequorivita, Arenibacter, Cellulophaga, Croceibacter, Formosa, Gelidibacter, Gillisia, Maribacter, Mesonia, Muricauda, Polaribacter, Psychroflexus, Psychroserpens, Robiginitalea, Salegentibacter, Tenacibaculum, Ulvibacter, Vitellibacter and Zobellia. Pp. 677-694 in The Prokaryotes, M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt, eds. Springer, New York.
6. Brandes, J. A., A. H. Devol, and C. Deutsch. 2007. New developments in the marine nitrogen cycle. Chem. Rev. 107: 577-589.
7. Bright, M., and O. Giere. 2005. Microbial symbiosis in Annelida. Symbiosis 38: 1-45.
8. Brinkhoff, T., H.-A. Giebel, and M. Simon. 2008. Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch. Microbiol. 189: 531-539.
9. Brune, A., and M. Ohkuma. 2011. Role of the termite gut microbiota in symbiotic digestion. Pp. 439-475 in Biology of Termites: A Modern Synthesis, D. E. Bignell, Y. Roisin, and N. Lo, eds. Springer, The Netherlands.
10. Burja, A. M., B. Banaigs, E. Abou-Mansour, J. G. Burgess, and P. C. Wright. 2001. Marine cyanobacteria-a prolific source of natural products. Tetrahedron 57: 9347-9377.
11. Capone, D. G. 2008. The marine nitrogen cycle. Microbe 3: 186-192.
12. Carman, M. R., J. A. Morris, Jr., R. C. Karney, and D. W. Grunden. 2010. An initial assessment of native and invasive tunicates in shellfish aquaculture of the North American east coast. J. Appl. Ichthyol. 26: 8-11.
13. Chakraborty, C., C.-H. Hsu, Z.-H. Wen, and C.-S. Lin. 2009. Anticancer drugs discovery and development from marine organisms. Curr. Top. Med. Chem. 9: 1536-1545.
14. Chelius, M. K., and E. W. Triplett. 2001. The diversity of Archaea and bacteria in association with the roots of Zea mays L. Microb. Ecol. 41: 252-263.
15. Chimetto, L. A., M. Brocchi, C. C. Thompson, R. C. R. Martins, H. R. Ramos, and F. L. Thompson. 2008. Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazillian coral Mussismilia hispida. Syst. Appl. Microbiol. 31: 312-319.
16. Chou, Y.-J., J.-H. Chou, K.-Y. Lin, M.-C. Lin, Y.-H. Wei, A. B. Arun, C.-C. Young, and W.-M. Chen. 2008. Rothia terrae sp. nov. isolated from soil in Taiwan. Int. J. Syst. Evol. Microbiol. 58: 84-88.
17. Cohan, F. M. 2002. What are bacterial species? Annu. Rev. Microbiol. 56: 457-487.
18. Cole, J. 1996. Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol. Lett. 136: 1-11.
19. Cole, J. R., Q. Wang, E. Cardenas, J. Fish, B. Chai, R. J. Farris, A. S. Kulam-Syed-Mohideen, D. M. McGarrell, T. Marsh, G. M. Garrity, and J. M. Tiedje. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37: D141-D145.
20. Cottrell, M. T., and D. L. Kirchman. 2000. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low-and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66: 1692-1697.
21. Crosby, L. D., and C. S. Criddle. 2003. Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques 34: 2-9.
22. Crump, B. C., E. V. Armbrust, and J. A. Baross. 1999. Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl. Environ. Microbiol. 65: 3192-3204.
23. Dethlefsen, L., S. Huse, M. L. Sogin, and D. A. Relman. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6: e280.
24. Dillon, J. G., L. M. McMath, and A. L. Trout. 2009. Seasonal changes in bacterial diversity in the Salton Sea. Hydrobiologia 632: 49-64.
25. Distel, D. L, W. Morrill, N. MacLaren-Toussaint, D. Franks, and J. Waterbury. 2002. Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic gamma-proteobacterium isolated from the gills of wood-boring molluscs (Bivalvia: Teredinidae). Int. J. Syst. Evol. Microbiol. 52: 2261-2269.
26. Dowd, S. E., T. R. Callaway, R. D. Wolcott, Y. Sun, T. McKeehan, R. G. Hagevoort, and T. S. Edrington. 2008. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 8: 125.
27. Dubilier, N., C. Bergin, and C. Lott. 2008. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6: 725-740.
28. Erasmus, J. H., P. A. Cook, and V. E. Coyne. 1997. The role of bacteria in the digestion of seaweed by the abalone Haliotis midae. Aquaculture 155: 377-386.
29. Farrelly, V., F. A. Rainey, and E. Stackebrandt. 1995. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl. Environ. Microbiol. 61: 2798-2801.
30. Fiore, C. L., J. K. Jarett, N. D. Olson, and M. P. Lesser. 2010. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 18: 455-463.
31. Gao, J., and M. T. Hamann. 2011. Chemistry and biology of kahalalides. Chem. Rev. 111: 3208-3235.
32. Gill, S. R., M. Pop, R. T. DeBoy, P. B. Eckburg, P. J. Turnbaugh, B. S. Samuel, J. I. Gordon, D. A. Relman, C. M. Fraser-Liggett, and K. E. Nelson. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312: 1355-1359.
33. Glöckner, F. O., B. M. Fuchs, and R. Amann. 1999. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 65: 3721-3726.
34. Goldberg, S. M. D., J. Johnson, D. Busam, T. Feldblyum, S. Ferriera, R. Friedman, A. Halpern, H. Khouri, S. A. Kravitz, F. M. Lauro et al. 2006. A Sanger/pyrosequencing hybrid approach for the generation of high-quality draft assemblies of marine microbial genomes. Proc. Natl. Acad. Sci. USA 103: 11240-11245.
35. Hamady, M., C. Lozupone, and R. Knight. 2010. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 4: 17-27.
36. Hamann, M. T., and P. J. Scheuer. 1993. Kahalalide F: a bioactive depsipeptide from the sacoglossan mollusk Elysia rufescens and the green alga Bryopsis sp. J. Am. Chem. Soc. 115: 5825-5826.
37. Handelsman, J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68: 669-685.
38. Hay, M. E. 2009. Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annu. Rev. Mar. Sci. 1: 193-212.
39. Hentschel, U., M. Schmid, M. Wagner, L. Fieseler, C. Gernert, and J. Hacker. 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.
40. Hill, R. T., J. Enticknap, K. V. Rao, and M. T. Hamann. 2007 August 23. Kahalalide-producing bacteria. U.S. patent 2007/0196901 A1.
41. Hoffmann, F., R. Radax, D. Woebken, M. Holtappels, G. Lavik, H. T. Rapp, M.-L. Schläppy, C. Schleper, and M. M. M. Kuypers. 2009. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11: 2228-2243.
42. Ivanova, E. P., and V. V. Mikhailov. 2001. A new family, Alteromonadaceae fam. nov., including marine proteobacteria of the genera Alteromonas, Pseudoalteromonas, Idiomarina, and Colwellia. Microbiology 70: 10-17.
43. Jaeckle, W. B., and D. T. Manahan. 1989. Feeding by a "nonfeeding" larva: uptake of dissolved amino acids from seawater by lecithotrophic larvae of the gastropod Haliotis rufescens. Mar. Biol. 103: 87-94.
44. Jannasch, H. W., and M. J. Mottl. 1985. Geomicrobiology of deep-sea hydrothermal vents. Science 229: 717-725.
45. Jenni, B., C. Isch, and M. Aragno. 1989. Nitrogen fixation by new strains of Pseudomonas pseudoflava and related bacteria. Microbiology 135: 461-467.
46. Kennedy, J., J. R. Marchesi, and A. D. W. Dobson. 2007. Metagenomic approaches to exploit the biotechnological potential of the microbial consortia of marine sponges. Appl. Microbiol. Biotechnol. 75: 11-20.
47. Kennedy, J., B. Flemer, S. A. Jackson, D. P. H. Lejon, J. P. Morrissey, F. O'Gara, and A. D. W. Dobson. 2010. Marine metagenomics: new tools for the study and exploitation of marine microbial metabolism. Mar. Drugs 8: 608-628.
48. Kersters, K., P. De Vos, M. Gillis, J. Swings, P. Vandamme, and E. Stackebrandt. 2006. Introduction to the Proteobacteria. Pp. 3-37 in The Prokaryotes, M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt, eds. Springer, New York.
49. Kirchman, D. L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39: 91-100.
50. Kirchman, D. L., A. I. Ditteh, S. E. G. Findlay, and D. Fischer. 2004. Changes in bacterial activity and community structure in response to dissolved organic matter in the Hudson River, New York. Aquat. Microb. Ecol. 35: 243-257.
51. Kirchman, D. L., A. I. Dittel, R. R. Malmstrom, and M. T. Cottrell. 2005. Biogeography of major bacterial groups in the Delaware estuary. Limnol. Oceanogr. 50: 1697-1706.
52. Klappenbach, J. A., P. R. Saxman, J. R. Cole, and T. M. Schmidt. 2001. rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res. 29: 181-184.
53. Klein, D. A. 2011. Bulk extraction-based microbial ecology: three critical questions. Microbe 6: 377.
54. Kooperman, N., E. Ben-Dov, E. Kramarsky-Winter, Z. Barak, and A. Kushmaro. 2007. Coral mucus-associated bacterial communities from natural and aquarium environments. FEMS Microbiol. Lett. 276: 106-113.
55. Kraft, B., M. Strous, and H. E. Tegetmeyer. 2011. Microbial nitrate respiration-genes, enzymes and environmental distribution. J. Biotechnol. 155: 104-117.
56. Kurahashi, M., and A. Yokota. 2007. Endozoicomonas elysicola gen. nov., sp. nov., a gamma-proteobacterium isolated from the sea slug Elysia ornata. Syst. Appl. Microbiol. 30: 202-206.
57. Lane, D. J. 1991. 16S/23S rRNA sequencing. Pp. 115-175 in Nucleic Acid Techniques in Bacterial Systematics, E. Stackebrandt, and M. Goodfellow, eds., John Wiley, New York.
58. Lesser, M. P., L. I. Falcón, A. Rodriguez-Román, S. Enriquez, O. Hoegh-Guldberg, and R. Iglesias-Prieto. 2007. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346: 143-152.
59. Ley, R. E., C. A. Lozupone, M. Hamady, R. Knight, and J. I. Gordon. 2008. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6: 776-788.
60. Liu, Z., T. Z. DeSantis, G. L. Andersen, and R. Knight. 2008. Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequencers Nucleic Acids Res. 36: e120.
61. Luyten, Y. A., J. R. Thompson, W. Morrill, M. F. Polz, and D. L. Distel. 2006. Extensive variation in intracellular symbiont community composition among members of a single population of the woodboring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl. Environ. Microbiol. 72: 412-417.
62. Mansson, M., L. Gram, and T. O. Larsen. 2011. Production of bioactive secondary metabolites by marine Vibrionaceae. Mar. Drugs 9: 1440-1468.
63. Marchesi, J. R., T. Sato, A. J. Weightman, T. A. Martin, J. C. Fry, S. J. Hiom, and W. G. Wade. 1998. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl. Environ. Microbiol. 64: 795-799.
64. 12. Appl. Microbiol. Biotechnol. 58: 275-285.
65. Martens, T., L. Gram, H.-P. Grossart, D. Kessler, R. Mü ller, M. Simon, S. Wenzel, and T. Brinkhoff. 2007. Bacteria of the Roseobacter clade show potential for secondary metabolite production. Microb. Ecol. 54: 31-42.
66. McInerney, J. O., J. A. Cotton, and D. Pisani. 2008. The prokaryotic tree of life: past present. and future? Trends Ecol. Evol. 23: 276-281.
67. Mesbah, N. M., S. H. Abou-El-Ela, and J. Wiegel. 2007. Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb. Ecol. 54: 598-617.
68. Metzker, M. L. 2010. Sequencing technologies-the next generation. Nat. Rev. Genet. 11: 31-46.
69. Mikhailov, V., L. Romanenko, and E. Ivanova. 2006. The genus Alteromonas and related proteobacteria. Pp. 597-645 in The Prokaryotes, M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt, eds. Springer, New York.
70. Mohamed, N. M., A. S. Colman, Y. Tal, and R. T. Hill. 2008. Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environ. Microbiol. 10: 2910-2921.
71. Monks, N. R., C. Lerner, A. T. Henriques, F. M. Farias, E. E. S. Schapoval, E. S. Suyenaga, A. B. da Rocha, G. Schwartsmann, and B. Mothes. 2002. Anticancer, antichemotactic and antimicrobial activities of marine sponges collected off the coast of Santa Catarina, southern Brazil. J. Exp. Mar. Biol. Ecol. 281: 1-12.
72. Nawrocki, E. P., and S. R. Eddy. 2007. Query-dependent banding (QDB) for faster RNA similarity searches. PLoS Comput. Biol. 3: e56.
73. Oren, A. 2008. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst. 4: 2.
74. Ott, D. W. 1979. Endosymbiotic bacteria in Vaucheria (Xanthophyceae): association with cytoplasmic microtubules in Vaucheria sessilis. Cytobios 24: 185-194.
75. Paerl, H. W., R. L. Dennis, and D. R. Whitall. 2002. Atmospheric deposition of nitrogen: implications for nutrient over-enrichment of coastal waters. Estuaries 25: 677-693.
76. Pawlik, J. R. 1993. Marine invertebrate chemical defenses. Chem. Rev. 93: 1911-1922.
77. Pelletreau, K. N., D. Bhattacharya, D. C. Price, J. M. Worful, A. Moustafa, and M. E. Rumpho. 2011. Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiol. 155: 1561-1565.
78. Piel, J., D. Hui, G. Wen, D. Butzke, M. Platzer, N. Fusetani, and S. Matsunaga. 2004. Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc. Natl. Acad. Sci. USA 101: 16222-16227.
79. Pierce, S. K., R. W. Biron, and M. E. Rumpho. 1996. Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J. Exp. Biol. 199: 2323-2330.
80. Proksch, P., R. A. Edrada, and R. Ebel. 2002. Drugs from the sea-current status and microbiological implications. Appl. Microbiol. Biotechnol. 59: 25-34.
81. Rabalais, N. N., R. E. Turner, R. J. Díaz, and D. Justíc. 2009. Global change and eutrophication of coastal waters. ICES J. Mar. Sci. 66: 1528-1537.
82. Rajakumar, S., P. M. Ayyasamy, K. Shanthi, P. Thavamani, P. Velmurugan, Y. C. Song, and P. Lakshmanaperumalsamy. 2008. Nitrate removal efficiency of bacterial consortium (Pseudomonas sp. KW1 and Bacillus sp. YW4) in synthetic nitrate-rich water. J. Hazard. Mater. 157: 553-563.
83. Ramaiah, N., R. T. Hill, J. Chun, J. Ravel, M. H. Matte, W. L. Straube, and R. R. Colwell. 2000. Use of a chiA probe for detection of chitinase genes in bacteria from the Chesapeake Bay. FEMS Microbiol. Ecol. 34: 63-71.
84. Rappé, M. S., K. Vergin, and S. J. Giovannoni. 2000. Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiol. Ecol. 33: 219-232.
85. Reshef, L., O. Koren, Y. Loya, I. Zilber-Rosenberg, and E. Rosenberg. 2006. The coral probiotic hypothesis. Environ. Microbiol. 8: 2068-2073.
86. Ritchie, K. B. 2006. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322: 1-14.
87. Ritchie, K. B., and G. W. Smith. 1995. Preferential carbon utilization by surface bacterial communities from water mass, normal, and whiteband diseased Acropora cervicornis. Mol. Mar. Biol. Biotechnol. 4: 345-352.
88. Rumpho, M. E., E. J. Summer, and J. R. Manhart. 2000. Solarpowered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol. 123: 29-38.
89. Rumpho, M. E., J. M. Worful, J. Lee, K. Kannan, M. S. Tyler, D. Bhattacharya, A. Moustafa, and J. R. Manhart. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc. Natl. Acad. Sci. USA 105: 17867-17871.
90. Rumpho, M. E., K. N. Pelletreau, A. Moustafa, and D. Bhattacharya. 2011. The making of a photosynthetic animal. J. Exp. Biol. 214: 303-311.
91. Sacristán-Soriano, O., B. Banaigs, E. O. Casamayor, and M. A. Becerro. 2011. Exploring the links between natural products and bacterial assemblages in the sponge Aplysina aerophoba. Appl. Environ. Microbiol. 77: 862-870.
92. Satyanarayana, T., C. Raghukumar, and S. Shivaji. 2005. Extremophilic microbes: diversity and perspectives. Curr. Sci. 89: 78-90.
93. Savage, D. C. 1986. Gastrointestinal microflora in mammalian nutrition. Annu. Rev. Nutr. 6: 155-178.
94. Sawabe, T., Y. Oda, Y. Shiomi, and Y. Ezura. 1995. Alginate degradation by bacteria isolated from the gut of sea urchins and abalones. Microb. Ecol. 30: 193-202.
95. Schramm, A., S. K. Davidson, J. A. Dodsworth, H. L. Drake, D. A. Stahl, and N. Dubilier. 2003. Acidovorax-like symbionts in the nephridia of earthworms. Environ. Microbiol. 5: 804-809.
96. Schweitzer, B., I. Huber, R. Amann, W. Ludwig, and M. Simon. 2001. Proteobacteria control the consumption and release of amino acids on lake snow aggregates. Appl. Environ. Microbiol. 67: 632-645.
97. Scott, D. B. 1977. Physiographic and oceanographic characteristics of Chezzetcook Inlet, Nova Scotia. Atlantic Geol. 13: 73-78.
98. Sharon, G., and E. Rosenberg. 2008. Bacterial growth on coral mucus. Curr. Microbiol. 56: 481-488.
99. Shnit-Orland, M., and A. Kushmaro. 2009. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol. Ecol. 67: 371-380.
100. Simon, C., and R. Daniel. 2011. Metagenomic analyses: past and future trends. Appl. Environ. Microbiol. 77: 1153-1161.
101. Simon, C., A. Wiezer, A. W. Strittmatter, and R. Daniel. 2009. Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl. Environ. Microbiol. 75: 7519-7526.
102. Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. Arrieta, and G. J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere." Proc. Natl. Acad. Sci. USA 103: 12115-12120.
103. Söylemez, S. C., K. Murakami, C. A. Strüssmann, M. Yokota, and S. Watanabe. 2010. Uptake of dissolved free amino acids by spiny lobster Panulirus japonicus phyllosoma larvae. Fish. Sci. 76: 437-444.
104. Stackebrandt, E., C. S. Cummins, and J. L. Johnson. 2006. Family Propionibacteriaceae: the genus Propionibacterium. Pp. 400-418 in The Prokaryotes, M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt, eds. Springer, New York.
105. Stal, L. J., and J. P. Zehr. 2008. Cyanobacterial nitrogen fixation in the ocean: diversity, regulation, and ecology. Pp. 423-446 in The Cyanobacteria. Molecular Biology, Genetics, and Evolution, A. Herrero, and E. Flores, eds. Caister Academic Press, Norwich, United Kingdom.
106. Stephens, G. C. 1981. The trophic role of dissolved organic material. Pp. 271-291 in Analysis of Marine Ecosystems, A. R. Longhurst, ed. Academic Press, London.
107. Sun, Y., R. D. Wolcott, and S. E. Dowd. 2011. Tag-encoded FLX amplicon pyrosequencing for the elucidation of microbial and functional gene diversity in any environment. Pp. 129-141 in High-Throughput Next Generation Sequencing: Methods and Applications, Y. M. Kwon and S. C. Ricke, eds. Humana Press, New York.
108. Sunagawa, S., T. Z. DeSantis, Y. M. Piceno, E. L. Brodie, M. K. DeSalvo, C. R. Voolstra, E. Weil, G. L. Andersen, and M. Medina. 2009. Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3: 512-521.
109. Tamames, J., J. J. Abellan, M. Pignatelli, A. Camacho, and A. Moya. 2010. Environmental distribution of prokaryotic taxa. BMC Microbiol. 10: 85.
110. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
111. Taylor, J. D., and E. A. Glover. 2006. Lucinidae (Bivalvia)-the most diverse group of chemosymbiotic molluscs. Zool. J. Linn. Soc. 148: 421-438.
112. Thakur, N. L., A. N. Thakur, and W. E. G. Mü ller. 2005. Marine natural products in drug discovery. Nat. Prod. Radiance 4: 471-477.
113. Trench, R. K. 1975. Of "leaves that crawl": functional chloroplasts in animal cells. Symp. Soc. Exp. Biol. 29: 229-265.
114. Tringe, S. G., and P. Hugenholtz. 2008. A renaissance for the pioneering 16S rRNA gene. Curr. Opin. Microbiol. 11: 442-446.
115. Usher, K. M. 2008. The ecology and phylogeny of cyanobacterial symbionts in sponges. Mar. Ecol. 29: 178-192.
116. Vacelet, J., and N. Boury-Esnault. 2002. A new species of carnivorous deep-sea sponge (Demospongiae: Cladorhizidae) associated with methanotrophic bacteria. Cah. Biol. Mar. 43: 141-148.
117. Wagner-Döbler, I., W. Beil, S. Lang, M. Meiners, and H. Laatsch. 2002. Integrated approach to explore the potential of marine microorganisms for the production of bioactive metabolites. Adv. Biochem. Eng. Biotechnol. 74: 207-238.
118. Webster, N. S., M. W. Taylor, F. Behnam, S. Lü cker, T. Rattei, S. Whalan, M. Horn, and M. Wagner. 2010. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12: 2070-2082.
119. West, H. H. 1979. Chloroplast symbiosis and development of the sacoglossan opisthobranch Elysia chlorotica. Ph.D. dissertation, Northeastern University, Boston.
120. Whitman, W. B., D. C. Coleman, and W. J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95: 6578-6583.
121. Wietz, M., M. Mansson, C. H. Gotfredsen, T. O. Larsen, and L. Gram. 2010. Antibacterial compounds from marine Vibrionaceae isolated on a global expedition. Mar. Drugs 8: 2946-2960.
122. Willems, A., J. De Ley, M. Gillis, and K. Kersters. 1991. Comamonadaceae, a new family encompassing the Acidovorans rRNA complex, including Variovorax paradoxus gen. nov., comb. nov., for Alcaligenes paradoxus (Davis 1969). Int. J. Syst. Evol. Microbiol. 41: 445-450.
123. Woese, C. R., and G. E. Fox. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. USA 74: 5088-5090.
124. Woese, C. R., O. Kandler, and M. L. Wheelis. 1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA 87: 4576-4579.
125. Wooley, J. C., A. Godzik, and I. Friedberg. 2010. A primer on metagenomics. PLoS Comput. Biol. 6: e1000667.
126. Wu, G. D., J. D. Lewis, C. Hoffmann, Y.-Y. Chen, R. Knight, K. Bittinger, J. Hwang, J. Chen, R. Berkowsky, L. Nessel, H. Li, and F. D. Bushman. 2010. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiol. 10: 206.
127. Zheng, L., H. Chen, X. Han, W. Lin, and X. Yan. 2005. Antimicrobial screening and active compound isolation from marine bacterium NJ6-3-1 associated with the sponge Hymeniacidon perleve. World J. Microbiol. Biotechnol. 21: 201-206.