Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite

Nature

Volumn 450, Issue 7169, 2007, Pages 560-565

  Warnecke, Falk ^a   Luginbühl, Peter ^b   Ivanova, Natalia ^a   Ghassemian, Majid ^b   Richardson, Toby H ^b,g   Stege, Justin T ^b   Cayouette, Michelle ^b   McHardy, Alice C ^c,h   Djordjevic, Gordana ^b   Aboushadi, Nahla ^b   Sorek, Rotem ^a   Tringe, Susannah G ^a   Podar, Mircea ^d   Martin, Hector Garcia ^a   Kunin, Victor ^a   Dalevi, Daniel ^a   Madejska, Julita ^a   Kirton, Edward ^a   Platt, Darren ^a   Szeto, Ernest ^a   Salamov, Asaf ^a   Barry, Kerrie ^a   Mikhailova, Natalia ^a   Kyrpides, Nikos C ^a   Matson, Eric G ^e   Ottesen, Elizabeth A ^e   Zhang, Xinning ^e   Hernández, Myriam ^f   Murillo, Catalina ^f   Acosta, Luis G ^f   Rigoutsos, Isidore ^c   Tamayo, Giselle ^f   Green, Brian D ^b   Chang, Cathy ^b   Rubin, Edward M ^a   Mathur, Eric J ^b,g   Robertson, Dan E ^b   Hugenholtz, Philip ^a   Leadbetter, Jared R ^e   more..

^a DOE JOINT GENOME INSTITUTE   (United States)

^b DIVERSA CORPORATION   (United States)

^c IBM T J WATSON RESEARCH CENTER   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^f INSTITUTO NACIONAL DE BIODIVERSIDAD   (Costa Rica)

^g Synthetic Genomics Inc   (United States)

^h MAX PLANCK INSTITUTE FOR INFORMATICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIGNOCELLULOSE;

BACTERIUM; BIODEGRADATION; BIOTECHNOLOGY; CATALYSIS; DIGESTIVE SYSTEM; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; HYDROLYSIS; MICROBIAL COMMUNITY; SYMBIOSIS; TERMITE;

ANALYTIC METHOD; ARTICLE; BACTERIAL GENE; BIOTECHNOLOGY; GENETIC ANALYSIS; HYDROLYSIS; IN VITRO STUDY; ISOPTERA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); FIBROBACTER; ISOPTERA; NASUTITERMES; PROTOZOA; SPIROCHAETALES; TERMITIDAE;

EID: 36549000721     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature06269     Document Type: Article

References (66)

1. Sugimoto, A., Bignell, D. E. & Macdonald, J. A. in Termites: Evolution, Sociality, Symbioses, Ecology (eds Abe, T. Bignell, D. E. & Higashi, M.) 409-435 (Kluwer Academic, Dordrecht, 2000).
2. Tokuda, G. & Watanabe, H. Hidden cellulases in termites: revision of an old hypothesis. Biol. Lett. 3, 336-339 (2007).
3. Brune, A. in The Prokaryotes Vol. 1 (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) 439-474 (Springer, New York, 2006).
4. Kambhampati, S. & Eggleton, P. in Termites: Evolution, Sociality, Symbioses, Ecology (eds Abe, T. Bignell, D. E. & Higashi, M.) 1-24 (Kluwer Academic, Dordrecht, 2000).
5. Tokuda, G. et al. Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol. Ecol. 13, 3219-3228 (2004).
6. Brennan, Y. et al. Unusual microbial xylanases from insect guts. Appl. Environ. Microbiol. 70, 3609-3617 (2004).
7. McHardy, A. C., Martin, H. G., Tsirigos, A., Hugenholtz, P. & Rigoutsos, I. Accurate phylogenetic classification of variable-length DNA fragments. Nat. Methods 4, 63-72 (2007).
8. Brune, A., Emerson, D. & Breznak, J. A. The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl. Environ. Microbiol. 61, 2681-2687 (1995).
9. Davies, G. J. & Henrissat, B. Structural enzymology of carbohydrate-active enzymes: implications for the post-genomicera. Biochem. Soc. Trans. 30, 291-297 (2002).
10. Breznak, J. A. & Brune, A. Role of microorganisms in the digestion of lignocellulose in termites. Annu. Rev. Entomol. 39, 453-487 (1994).
11. Taylor, L. E. II et al. Complete cellulase system in the marine bacterium Saccharophagus degradans strain 2-40T. J. Bacteriol. 188, 3849-3861 (2006).
12. Xie, G. et al. Genome sequence of the cellulolytic gliding bacterium Cytophaga hutchinsonii. Appl. Environ. Microbiol. 73, 3536-3546 (2007).
13. Tringe, S. G. et al. Comparative metagenomics of microbial communities. Science 308, 554-557 (2005).
14. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66-74 (2004).
15. Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355-1359 (2006).
16. Qi, M. et al. Novel molecular features of the fibrolytic intestinal bacterium Fibrobacter intestinalis not shared with Fibrobacter succinogenes as determined by suppressive subtractive hybridization. J. Bacteriol. 187, 3739-3751 (2005).
17. Odelson, D. A. & Breznak, J. A. Nutrition and growth characteristics of Trichomitopsis termopsidis, a cellulolytic protozoan from termites. Appl. Environ. Microbiol. 49, 614-621 (1985).
18. Vignais, P. M. & Colbeau, A. Molecular biology of microbial hydrogenases. Curr. Issues Mol. Biol. 6, 159-188 (2004).
19. Breznak, J. A. & Switzer, J. M. Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl. Environ. Microbiol. 52, 623-630 (1986).
20. Pester, M. & Brune, A. Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J. 1, 551-565 (2007).
21. Ragsdale, S. W. The eastern and western branches of the Wood/Ljungdahl pathway: how the East and West were won. Biofactors 6, 3-11 (1997).
22. Pester, M. & Brune, A. Expression profiles of fhs (FTHFS) genes support the hypothesis that spirochaetes dominate reductive acetogenesis in the hindgut of lower termites. Environ. Microbiol. 8, 1261-1270 (2006).
23. Prestwich, G. D., Bentley, B. L. & Carpenter, E. J. Nitrogen sources for neotropical nasute termites: Fixation and selective foraging. Oecologia 46, 397-401 (1980).
24. Ohkuma, M., Noda, S. & Kudo, T. Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl. Environ. Microbiol. 65, 4926-4934 (1999).
25. Potrikus, C. J. & Breznak, J. A. Anaerobic degradation of uric acid by gut bacteria of termites. Appl. Environ. Microbiol. 40, 125-132 (1980).
26. Brune, A. & Friedrich, M. Microecology of the termite gut: structure and function on a microscale. Curr. Opin. Microbiol. 3, 263-269 (2000).
27. Beckwith, T. & Light, S. The spirals within the termite gut for class use. Science 66, 656-657 (1927).
28. Robertson, D. E. et al. Exploring nitrilase sequence space for enantioselective catalysis. Appl. Environ. Microbiol. 70, 2429-2436 (2004).
29. Short, J. M., Fernandez, J. M., Sorge, J. A. & Huse, W. D. Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties. Nucleic Acids Res. 16, 7583-7600 (1988).
30. Ewing, B. & Green, P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8, 186-194 (1998).
31. Ewing, B., Hillier, L., Wendl, M. C. & Green, P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8, 175-185 (1998).
32. Markowitz, V. M. et al. An experimental metagenome data management and analysis system. Bioinformatics 22, e359-e367 (2006).
33. Markowitz, V. M. et al. The integrated microbial genomes (IMG) system. Nucleic Acids Res. 34, D344-D348 (2006).
34. Marchler-Bauer, A., Panchenko, A. R., Ariel, N. & Bryant, S. H. Comparison of sequence and structure alignments for protein domains. Proteins 48, 439-446 (2002).
35. Emanuelsson, O., Brunak, S., von Heijne, G. & Nielsen, H. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2, 953-971, doi:10.1038/nprot.2007.131 (2007).
36. Wei, J. et al. Global proteome discovery using an online three-dimensional LC-MS/MS. J. Proteome Res. 4, 801-808 (2005).
37. DeSantis, T. Z. Jr et al. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 34, W394-W399 (2006).
38. DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072 (2006).
39. Stamatakis, A., Ludwig, T. & Meier, H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21, 456-463 (2005).
40. Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502-504 (2002).
41. Schloss, P. D. & Handelsman, J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71, 1501-1506 (2005).
42. Colwell, R. K. & Coddington, J. A. Estimating terrestrial biodiversity through extrapolation. Phil. Trans. R. Soc. Lond. B 345, 101-118 (1994).
43. de Caprariis, P., Lindemann, R. & Collins, C. A method for determining optimum sample size in species diversity studies. J. Int. Assoc. Math. Geol. 8, 575-581 (1976).
44. Smith, E. P. & van Belle, G. Nonparametric estimation of species richness. Biometrics 40, 119-129 (1984).
45. Krebs, C. J. Ecological Methodology (Harper & Row, New York, 1989).
46. Efron, B. & Tibshirani, R. An Introduction to the Bootstrap (Chapman & Hall, New York, 1993).
47. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
48. Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371 (2004).
49. Austin, J. W., Szalanski, A. L. & Cabrera, B. J. Phylogenetic analysis of the subterranean termite family Rhinotermitidae (Isoptera) by using the mitochondrial cytochrome oxidase II gene. Ann. Entomol. Soc. Am. 97, 548-555 (2004).
50. Ohkuma, M. et al. Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences. Mol. Phylogenet. Evol. 31, 701-710 (2004).
51. Henrissat, B. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280, 309-316 (1991).
52. Davies, D. G. & Geesey, G. G. Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continous culture. Appl. Environ. Microbiol. 61, 860-867 (1995).
53. Johnston, D. in Handbook of Food Enzymology (eds Whitaker, J. R., Voragen, A. G. J. & Wong, D. W. S.) 761-769 (Marcel Dekker Inc., New York, 2002).
54. Stahlberg, J., Johansson, G. & Pettersson, G. Trichoderma reesei has no true exocellulase: all intact and truncated cellulases produce new reducing end groups on cellulose. Biochim. Biophys. Acta 1157, 107-113 (1993).
55. Wood, T. Preparation of crystalline, amorphous and dyed cellulase substrate. Methods Enzymol. 160, 19-25 (1988).
56. von Mering, C. et al. STRING 7 - recent developments in the integration and prediction of protein interactions. Nucleic Acids Res. 35, D358-D362 (2007).
57. Marchler-Bauer, A. & Bryant, S. H. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32, W327-W331 (2004).
58. Marchler-Bauer, A. et al. CDD: a conserved domain database for protein classification. Nucleic Acids Res. 33, D192-D196 (2005).
59. Corpet, F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890 (1988).
60. Apweiler, R. et al. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 29, 37-40 (2001).
61. Peters, J. W., Lanzilotta, W. N., Lemon, B. J. & Seefeldt, L. C. X-ray crystal structure of the Fe-only hydrogenase (Cpl) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282, 1853-1858 (1998).
62. Chenna, R. et al. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31, 3497-3500 (2003).
63. Bates, P. A., Kelley, L. A., MacCallum, R. M. & Sternberg, M. J. E. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins Struct. Funct. Genet. 45, 39-46 (2001).
64. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 27-28 (1996).
65. Lilburn, T. G. et al. Nitrogen fixation by symbiotic and free-living spirochetes. Science 292, 2495-2498 (2001).
66. Sturn, A., Quackenbush, J. & Trajanoski, Z. Genesis: cluster analysis of microarray data. Bioinformatics 18, 207-208 (2002).