Microbiome of fungus-growing termites: A new reservoir for lignocellulase genes

Applied and Environmental Microbiology

Volumn 77, Issue 1, 2011, Pages 48-56

  Liu, Ning ^a   Yan, Xing ^a   Zhang, Meiling ^b   Xie, Lei ^a   Wang, Qian ^a   Huang, Yongping ^a   Zhou, Xuguo ^c   Wang, Shengyue ^d   Zhou, Zhihua ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b EAST CHINA NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF KENTUCKY   (United States)

^d CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTEROIDES; CARBON MINERALIZATION; CATALYTIC DOMAINS; CELLOBIOHYDROLASES; DISPLACEMENT AMPLIFICATION; DNA EXTRACTION; ENDOGLUCANASES; FUNCTIONAL SCREENING; FUNGUS-GROWING TERMITES; GLUCOSIDASE; HIGH QUALITY; LIGNOCELLULOSE DEGRADATION; MICROBIOTAS; MULTI DOMAINS; N-TERMINALS; OPEN READING FRAME; SUBTROPICAL REGIONS; XYLANASES;

CELLULOSE; CLONING; DEGRADATION; DNA; GENES;

NUCLEIC ACIDS;

CELLULASE; LIGNIN; LIGNOCELLULOSE;

AMPLIFICATION; BIODEGRADATION; BIOME; CARBON; CELLULOSE; CLIMATIC REGION; ENZYME ACTIVITY; FUNCTIONAL MORPHOLOGY; FUNGUS; GENE EXPRESSION; GENETIC ANALYSIS; LIGNIN; MICROBIAL ACTIVITY; MINERALIZATION; PH; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RESERVOIR; TEMPERATURE EFFECT; TERMITE; TOLERANCE;

ANIMAL; ARTICLE; DNA SEQUENCE; GENE LIBRARY; GENETICS; ISOPTERA; METABOLISM; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY;

ANIMALS; CELLULASES; GENE LIBRARY; ISOPTERA; LIGNIN; METAGENOME; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

BACTEROIDES; FUNGI; ISOPTERA; LISTERIA; MACROTERMITINAE;

EID: 79251624712     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01521-10     Document Type: Article

References (58)

1. Abulencia, C. B., D. L. Wyborski, J. A. Garcia, M. Podar, W. Q. Chen, S. H. Chang, H. W. Chang, D. Watson, E. L. Brodie, T. C. Hazen, and M. Keller. 2006. Environmental whole-genome amplification to access microbial populations in contaminated sediments. Appl. Environ. Microbiol. 72:3291-3301.
2. Bignell, D. E., P. Eggleton, L. Nunes, and K. L. Thomas. 1997. Termites as mediators of carbon fluxes in tropical forests: budgets for carbon dioxide and methane emissions, p. 109-134. In A. D. Watt, N. E. Stork, and M. D. Hunter (ed.), Forests and insects. Chapman and Hall, London, United Kingdom.
3. Bourgois, T. M., D. V. Nguyen, S. Sansen, S. Rombouts, T. Belien, K. Fierens, G. Raedschelders, A. Rabijns, C. M. Courtin, J. A. Delcour, S. Van Campenhout, and G. Volckaert. 2007. Targeted molecular engineering of a family 11 endoxylanase to decrease its sensitivity towards Triticum aestivum endoxylanase inhibitor types. J. Biotechnol. 130:95-105.
4. Brady, S. F. 2007. Construction of soil environmental DNA cosmid libraries and screening for clones that produce biologically active small molecules. Nat. Protoc. 2:1297-1305.
5. Brauman, A., J. Dore, P. Eggleton, D. Bignell, J. A. Breznak, and M. D. Kane. 2001. Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol. Ecol. 35:27-36.
6. Brauman, A., M. D. Kane, M. Labat, and J. A. Breznak. 1992. Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384-1387.
7. Brennan, Y., W. N. Callen, L. Christoffersen, P. Dupree, F. Goubet, S. Healey, M. Hernandez, M. Keller, K. Li, N. Palackal, A. Sittenfeld, G. Tamayo, S. Wells, G. P. Hazlewood, E. J. Mathur, J. M. Short, D. E. Robertson, and B. A. Steer. 2004. Unusual microbial xylanases from insect guts. Appl. Environ. Microbiol. 70:3609-3617.
8. Brune, A. 1998. Termite guts: the world's smallest bioreactors. Trends Biotechnol. 16:16-21.
9. Brune, A., and M. Friedrich. 2000. Microecology of the termite gut: structure and function on a microscale. Curr. Opin. Microbiol. 3:263-269.
10. Cai, S. C., J. B. Li, F. Z. Hu, K. G. Zhang, Y. M. Luo, B. Janto, R. Boissy, G. Ehrlich, and X. Z. Dong. 2010. Cellulosilyticum ruminicola, a newly described rumen bacterium that possesses redundant fibrolytic-protein-encoding genes and degrades lignocellulose with multiple carbohydrate-borne fibrolytic enzymes. Appl. Environ. Microbiol. 76:3818-3824.
11. Chen, Y., M. G. Dumont, J. D. Neufeld, L. Bodrossy, N. Stralis-Pavese, N. P.McNamara, N. Ostle, M. J. I. Briones, and J. C. Murrell. 2008. Revealingthe uncultivated majority: combining DNA stable-isotope probing, multiple displacement amplification and metagenomic analyses of uncultivated Methylocystis in acidic peatlands. Environ. Microbiol. 10:2609-2622.
12. Creste, S., A. T. Neto, and A. Figueira. 2001. Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol. Biol. Rep. 19:299-306.
13. Damiano, V. B., R. Ward, E. Gomes, H. F. Alves-Prado, and R. Da Silva. 2006. Purification and characterization of two xylanases from alkalophilicand thermophilic Bacillus licheniformis 77-2. Appl. Biochem. Biotechnol. 129:289-302.
14. Duan, C. J., L. Xian, G. C. Zhao, Y. Feng, H. Pang, X. L. Bai, J. L. Tang, Q. S. Ma, and J. X. Feng. 2009. Isolation and partial characterization ofnovel genes encoding acidic cellulases from metagenomes of buffalo rumens. J. Appl. Microbiol. 107:245-256.
15. Gabor, E. M., E. J. de Vries, and D. B. Janssen. 2003. Efficient recovery of environmental DNA for expression cloning by indirect extraction methods. FEMS Microbiol. Ecol. 44:153-163.
16. Handelsman, J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68:669-685. (Author's correction, 69:195, 2005.)
17. Handelsman, J., M. R. Rondon, S. F. Brady, J. Clardy, and R. M. Goodman. 1998. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5:R245-R249.
18. Heo, S., J. Kwak, H. W. Oh, D. S. Park, K. S. Bae, D. H. Shin, and H. Y. Park. 2006. Characterization of an extracellular xylanase in Paenibacillus sp. HY-8 isolated from an herbivorous longicorn beetle. J. Microbiol. Biotechnol. 16:1753-1759.
19. Hinman, N. D., D. J. Schell, C. J. Riley, P. W. Bergeron, and P. J. Walter. 1992. Preliminary estimate of the cost of ethanol-production for Ssf technology. Appl. Biochem. Biotechnol 34-35:639-649.
20. Hinze, B., K. Crailsheim, and R. H. Leuthold. 2002. Polyethism in food processing and social organisation in the nest of Macrotermes bellicosus (Isoptera, Termitidae). Insectes Soc. 49:31-37.
21. Jiang, Z. Q., W. Deng, Y. P. Zhu, L. T. Li, Y. J. Sheng, and K. Hayashi. 2004. The recombinant xylanase B of Thermotoga maritima is highly xylan specific and produces exclusively xylobiose from xylans, a unique character for industrial applications. J. Mol. Catal. B Enzym. 27:207-213.
22. Johjima, T., Y. Taprab, N. Noparatnaraporn, T. Kudo, and M. Ohkuma. 2006. Large-scale identification of transcripts expressed in a symbiotic fungus (Termitomyces) during plant biomass degradation. Appl. Microbiol. Biotechnol. 73:195-203.
23. Joshi, M. D., G. Sidhu, I. Pot, G. D. Brayer, S. G. Withers, and L. P. McIntosh. 2000. Hydrogen bonding and catalysis: a novel explanation for how a single amino acid substitution can change the pH optimum of a glycosidase. J. Mol. Biol. 299:255-279.
24. Kim, D. Y., M. K. Han, D. S. Park, J. S. Lee, H. W. Oh, D. H. Shin, T. S. Jeong, S. U. Kim, K. S. Bae, K. H. Son, and H. Y. Park. 2009. Novel GH10 xylanase, with a fibronectin type 3 domain, from Cellulosimicrobium sp. strain HY-13, a bacterium in the gut of Eisenia fetida. Appl. Environ. Microbiol. 75:7275-7279.
25. Kvist, T., B. K. Ahring, R. S. Lasken, and P. Westermann. 2007. Specific single-cell isolation and genomic amplification of uncultured microorganisms. Appl. Microbiol. Biotechnol. 74:926-935.
26. Kwon, K. S., J. Lee, H. G. Kang, and Y. C. Hah. 1994. Detection of betaglucosidase activity in polyacrylamide gels with esculin as substrate. Appl. Environ. Microbiol. 60:4584-4586.
27. Lo, N., G. Tokuda, H. Watanabe, H. Rose, M. Slaytor, K. Maekawa, C. Bandi, and H. Noda. 2000. Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr. Biol. 10:801-804.
28. Martin, M. M., and J. S. Martin. 1978. Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: the role of acquired digestive enzymes. Science 199:1453-1455.
29. Matoub, M., and C. Rouland. 1995. Purification and properties of the xylanases from the termite Macrotermes bellicosus and its symbiotic fungus Termitomyces sp. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 112:629-635.
30. Matson, E., E. Ottesen, and J. Leadbetter. 2007. Extracting DNA from the gut microbes of the termite (Zootermopsis nevadensis). J. Vis. Exp. 195:1-2.
31. Miller, G. L. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31:426-428.
32. Neufeld, J. D., Y. Chen, M. G. Dumont, and J. C. Murrell. 2008. Marinemethylotrophs revealed by stable-isotope probing, multiple displacementamplification and metagenomics. Environ. Microbiol. 10:1526-1535.
33. Ohkuma, M., H. Yuzawa, W. Amornsak, Y. Sornnuwat, Y. Takematsu, A. Yamada, C. Vongkaluang, O. Sarnthoy, N. Kirtibutr, N. Noparatnaraporn, T. Kudo, and T. Inoue. 2004. Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences. Mol. Phylogenet. Evol. 31:701-710.
34. a.Okada, H., and A. Shinmyo. 1988. Xylanase of Bacillus pumilus. Methods Enzymol. 160:632-637.
35. Ovreas, L., L. Forney, F. L. Daae, and V. Torsvik. 1997. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 63:3367-3373.
36. Ragauskas, A. J., C. K. Williams, B. H. Davison, G. Britovsek, J. Cairney, C. A. Eckert, W. J. Frederick, J. P. Hallett, D. J. Leak, C. L. Liotta, J. R. Mielenz, R. Murphy, R. Templer, and T. Tschaplinski. 2006. The path forward for biofuels and biomaterials. Science 311:484-489.
37. Reinholdhurek, B., T. Hurek, M. Claeyssens, and M. Vanmontagu. 1993. Cloning, expression in Escherichia coli, and characterization of cellulolytic enzymes of Azoarcus sp., a root-invading diazotroph. J. Bacteriol. 175:7056-7065.
38. Sapag, A., J. Wouters, C. Lambert, P. de Ioannes, J. Eyzaguirre, and E. Depiereux. 2002. The endoxylanases from family 11: computer analysis of protein sequences reveals important structural and phylogenetic relationships. J. Biotechnol. 95:109-131.
39. Schmeisser, C., H. Steele, and W. R. Streit. 2007. Metagenomics, biotech- nology with non-culturable microbes. Appl. Microbiol. Biotechnol. 75:955-962.
40. Reference deleted.
41. 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 deepsea and the underexplored "rare biosphere." Proc. Natl. Acad. Sci. U. S. A. 103:12115-12120.
42. Subramaniyan, S., and P. Prema. 2002. Biotechnology of microbial xylanases: enzymology, molecular biology, and application. Crit. Rev. Biotechnol.22:33-64.
43. Teather, R. M., and P. J. Wood. 1982. Use of Congo red polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl. Environ. Microbiol. 43:777-780.
44. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
45. Tokuda, G., N. Lo, H. Watanabe, M. Slaytor, T. Matsumoto, and H. Noda. 1999. Metazoan cellulase genes from termites: intron/exon structures and sites of expression. Biochim. Biophys. Acta 1447:146-159.
46. Tomme, P., R. A. Warren, and N. R. Gilkes. 1995. Cellulose hydrolysis by bacteria and fungi. Adv. Microb. Physiol. 37:1-81.
47. Voget, S., H. L. Steele, and W. R. Streit. 2006. Characterization of a metagenome-derived halotolerant cellulase. J. Biotechnol. 126:26-36.
48. Wakarchuk, W. W., R. L. Campbell, W. L. Sung, J. Davoodi, and M. Yaguchi. 1994. Mutational and crystallographic analyses of the active-site residues of the Bacillus circulans xylanase. Protein Sci. 3:467-475.
49. Walfridsson, M., X. M. Bao, M. Anderlund, G. Lilius, L. Bulow, and B. Hahn-Hagerdal. 1996. Ethanolic fermentation of xylose with Saccharomyces cerevisiae harboring the Thermus thermophilus xylA gene, which expresses an active xylose (glucose) isomerase. Appl. Environ. Microbiol. 62:4648-4651.
50. Warnecke, F., P. Luginbuhl, N. Ivanova, M. Ghassemian, T. H. Richardson, J. T. Stege, M. Cayouette, A. C. McHardy, G. Djordjevic, N. Aboushadi, R. Sorek, S. G. Tringe, M. Podar, H. G. Martin, V. Kunin, D. Dalevi, J. Madejska, E. Kirton, D. Platt, E. Szeto, A. Salamov, K. Barry, N. Mikhailova, N. C. Kyrpides, E. G. Matson, E. A. Ottesen, X. N. Zhang, M. Hernandez, C. Murillo, L. G. Acosta, I. Rigoutsos, G. Tamayo, B. D. Green, C. Chang, E. M. Rubin, E. J. Mathur, D. E. Robertson, P. Hugenholtz, and J. R. Leadbetter. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560-565.
51. Watanabe, H., H. Noda, G. Tokuda, and N. Lo. 1998. A cellulase gene of termite origin. Nature 394:330-331.
52. Wegley, L., R. Edwards, B. Rodriguez-Brito, H. Liu, and F. Rohwer. 2007. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9:2707-2719.
53. Wood, T. G., and R. J. Thomas. 1989. The mutualistic association between Macrotermitinae and Termitomyces, p. 69-92. In N. Wilding, N. M. Collins, P. M. Hammond, and J. F. Webber (ed.), Insect-fungus interaction. Academic Press, London, England.
54. Yamada, A., T. Inoue, D. Wiwatwitaya, M. Ohkuma, T. Kudo, T. Abe, and A. Sugimoto. 2005. Carbon mineralization by termites in tropical forests, with emphasis on fungus combs. Ecol. Res. 20:453-460.
55. Yu, J. H., Y. S. Park, D. Y. Yum, J. M. Kim, I. S. Kong, and D. H. Bai. 1993. Nucleotide sequence and analysis of a xylanase gene (xynS) from alkalitolerant Bacillus sp. YA-14 and comparison with other xylanases. J. Microbiol. Biotechnol. 3:139-145.
56. Zhang, K., A. C. Martiny, N. B. Reppas, K. W. Barry, J. Malek, S. W. Chisholm, and G. M. Church. 2006. Sequencing genomes from single cells by polymerase cloning. Nat. Biotechnol. 24:680-686.
57. Zhang, Z. Q., et al. 2005. Thin layer chromatography analysis of several uronates and their oligosaccharides. Chin. J. Analyt. Chem. 33:1750-1752.
58. Zhou, J. Z., M. A. Bruns, and J. M. Tiedje. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.