Microbial Distribution and Abundance in the Digestive System of Five Shipworm Species (Bivalvia: Teredinidae)

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Betcher, Meghan A ^a   Fung, Jennifer M ^b   Han, Andrew W ^a   O'Connor, Roberta ^b   Seronay, Romell ^c   Concepcion, Gisela P ^c   Distel, Daniel L ^b   Haygood, Margo G ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b Ocean Genome Legacy   (United States)

^c University of the Philippines Diliman   (Philippines)

Author keywords

[No Author keywords available]

Indexed keywords

LIGNOCELLULOSE; RNA 16S;

ANIMAL TISSUE; ARCHAEON; ARTICLE; BACTERIAL CELL; BACTERIOCYTE; BACTERIUM; BANKIA SETACEA; BIVALVE; CECUM; CELL TYPE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DIGESTIVE SYSTEM; ENDOSYMBIONT; FLUORESCENCE IN SITU HYBRIDIZATION; GILL; INTESTINE FLORA; LYRODUS MASSA; LYRODUS PEDICELLATUS; MARINE ENVIRONMENT; MICROFLORA; NONHUMAN; OLIGONUCLEOTIDE PROBE; POPULATION ABUNDANCE; POPULATION DENSITY; POPULATION DISTRIBUTION; SHIPWORM; STOMACH; TAXONOMY; TEREDINIDAE; TEREDO TRIANGULARIS; WOOD;

ANIMALS; BACTERIA; BIVALVIA; DIGESTIVE SYSTEM; GILLS; IN SITU HYBRIDIZATION; INTESTINES; RNA, RIBOSOMAL, 16S;

BACTERIA (MICROORGANISMS); BANKIA SETACEA; BIVALVIA; LYRODUS; LYRODUS PEDICELLATUS; TEREDINIDAE; TEREDO;

EID: 84866674202     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045309     Document Type: Article

References (36)

1. Stevens C, Hume I, (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78: 393-427.
2. Hess M, Sczyrba A, Egan R, Kim T-W, Chokhawala H, et al. (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331: 463-467 doi:10.1126/science.1200387.
3. Wallace R, (1994) Ruminal microbiology, biotechnology, and ruminant nutrition- progress and problems. Journal of Animal Science 72: 2992-3003.
4. Brune A, (1998) Termite guts: the world's smallest bioreactors. Trends in Biotechnology 16: 16-21.
5. Ohkuma M, (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biot 61: 1-9 doi: 10.1007/s00253-002-1189-z.
6. Distel DL (2003) The biology of marine wood boring bivalves and their bacterial endosymbionts. In: Goodell B, Nicholas DD, Schultz TP, editors. Wood Deterioration and Preservation. Washington: American Chemical Society Press. 253-271.
7. Greenfield LJ, Lane CE, (1953) Cellulose digestion in Teredo. J Biol Chem 204: 669-672.
8. Distel D, Roberts S, (1997) Bacterial endosymbionts in the gills of the deep-sea wood-boring bivalves Xylophaga atlantica and Xylophaga washingtona. The Biological Bulletin 192: 253.
9. Popham J, Dickson M, (1973) Bacterial associations in the teredo Bankia australis (Lamellibranchia-Mollusca). Mar Biol 19: 338-340.
10. Distel D, Delong E, Waterbury J, (1991) Phylogenetic characterization and in situ localization of the bacterial symbiont of shipworms (Teredinidae, Bivalvia) by using 16s-ribosomal-RNA sequence-analysis and oligodeoxynucleotide probe hybridization. Appl Environ Microb 57: 2376-2382.
11. Distel D, Beaudoin D, Morrill W, (2002) Coexistence of multiple proteobacterial endosymbionts in the gills of the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl Environ Microb 68: 6292-6299 doi: PMID: 12450854.
12. Luyten YA, Thompson JR, Morrill W, Polz MF, Distel DL, (2006) Extensive variation in intracellular symbiont community composition among members of a single population of the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl Environ Microb 72: 412-417 doi: 10.1128/AEM.72.1.412-417.2006.
13. Lechene C, Luyten Y, Mcmahon G, Distel D, (2007) Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science 317: 1563-1566 doi: PMID: 17872448.
14. Waterbury J, Calloway C, Turner R, (1983) A cellulolytic nitrogen-fixing bacterium cultured from the gland of Deshayes in shipworms (Bivalvia, Teredinidae). Science 221: 1401-1403.
15. Ekborg N, Morrill W, Burgoyne A, Li L, Distel D, (2007) CelAB, a multifunctional cellulase encoded by Teredinibacter turnerae T7902T, a culturable symbiont isolated from the wood-boring marine bivalve Lyrodus pedicellatus. Appl Environ Microb 73: 7785-7788 doi: 10.1128/AEM.00876-07 PMID: 17933945.
16. Yang JC, Madupu R, Durkin AS, Ekborg NA, Pedamallu CS, et al. (2009) The complete genome of Teredinibacter turnerae T7901: an intracellular endosymbiont of marine wood-boring bivalves (shipworms). PLoS ONE 4: e6085 doi: 10.1371/journal.pone.0006085.
17. Bazylinski DA, Rosenberg FA (1983) Occurrence of a brush-border in the caecum (appendix) of several Teredo and Bankia species (Teredinidae, Bivalvia, Mollusca). Veliger 25: 251-&.
18. Dean R, (1978) Mechanisms of wood digestion in shipworm Bankia gouldi Bartsch- enzyme degradation of celluloses, hemicelluloses, and wood cell-walls. Biol Bull 155: 297-316.
19. Gallager S, Turner R, Berg C, (1981) Physiological aspects of wood consumption, growth, and reproduction in the shipworm Lyrodus pedicellatus Quatrefages (Bivalvia: Teredinidae). J Exp Mar Biol Ecol 52: 63-77.
20. Turner RD (1966) A survey and illustrated catalogue of the Teredinidae (Mollusca: Bivalvia). Cambridge, Massachusetts: The Museum of Comparative Zoology, Harvard University. pp.
21. Distel DL, Amin M, Burgoyne A, Linton E, Mamangkey G, et al. (2011) Molecular phylogeny of Pholadoidea Lamarck, 1809 supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia. Molecular Phylogenetics and Evolution 61: 245-254 doi: 10.1016/j.ympev.2011.05.019.
22. Rubin EM, (2008) Genomics of cellulosic biofuels. Nature 454: 841-845 doi: 10.1038/nature07190.
23. Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, et al. (2007) Biomass recalcitrance: Engineering plants and enzymes for biofuels production. Science 315: 804-807 doi: 10.1126/science.1137016.
24. Morton B (1970) The functional anatomy of the organs of feeding and digestion of Teredo navalis Linnaeus and Lyrodus pedicellatus (Quatrefages). Proc Malac Soc Lond: 151-167.
25. Lazier E, (1924) Morphology of the digestive tract of Teredo navalis. University of California, Publications in Zoology 22: 455-474.
26. Brune A, Stingl U, (2006) Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis. In: Overmann J, editor. Progress in molecular and subcellular biology: Molecular Basis of Symbiosis. Berlin Heidelberg: Springer-Verlag, Vol. 41: 39-60.
27. Wilson DB, (2011) Microbial diversity of cellulose hydrolysis. Current Opinion in Microbiology 14: 259-263 doi: 10.1016/j.mib.2011.04.004.
28. Watanabe H, Tokuda G, (2010) Cellulolytic systems in insects. Annual Review of Entomology 55: 609-632.
29. Watanabe H, Tokuda G, (2001) Animal cellulases. Cell Mol Life Sci 58: 1167-1178.
30. Warnecke F, Luginbuehl P, Ivanova N, Ghassemian M, Richardson TH, et al. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450: 560-U17 doi: 10.1038/nature06269.
31. King AJ, Cragg SM, Li Y, Dymond J, Guille MJ, et al. (2010) Molecular insight into lignocellulose digestion by a marine isopod in the absence of gut microbes. Proceedings of the National Academy of Sciences 107: 5345-5350 doi: 10.1073/pnas.0914228107.
32. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, et al. (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microb 56: 1919-1925.
33. Zheng D, Alm E, Stahl D, Raskin L, (1996) Characterization of universal small-subunit rRNA hybridization probes for quantitative molecular microbial ecology studies. Appl Environ Microb 62: 4504-4513.
34. Stahl D, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. Chichester, England: John Wiley & Sons Ltd. 205-248.
35. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371 doi: 10.1093/nar/gkh293.
36. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145 doi: 10.1093/nar/gkn879.