1887

Abstract

The genome of the tuberculosis agent encodes a putative cellulose-binding protein (), one candidate cellulase (), and one fully active cellulase (). This observation is puzzling, because cellulose is a major component of plant cell walls, whereas is a human pathogen without known contact with plants. In order to investigate the biological role of such cellulose-targeting genes in we report here the search for and transcription analysis of this set of genes in the genus . An search for cellulose-targeting orthologues found that only 2.5 % of the sequenced bacterial genomes encode the , and gene set simultaneously, including those of the complex (MTC) members. PCR amplification and sequencing further demonstrated the presence of these three genes in five non-sequenced MTC bacteria. Among mycobacteria, the combination of , and was unique to MTC members, with the exception of BCG Pasteur, which lacked . RT-PCR in . H37Rv indicated that the three cellulose-targeting genes were transcribed into mRNA. The present work shows that MTC organisms are the sole mycobacteria among very few organisms to encode the three cellulose-targeting genes , and . Our data point toward a unique, yet unknown, relationship with non-plant cellulose-producing hosts such as amoebae.

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2010-05-01
2024-03-28
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  2. Ashford D. A., Whitney E., Raghunathan P., Cosivi O. 2001; Epidemiology of selected mycobacteria that infect humans and other animals. Rev Sci Tech 20:325–337
    [Google Scholar]
  3. Boulahrouf A., Fonty G., Gouet P. 1990; Establishment of cellulolytic bacteria in the digestive tract of conventionally reared young mice: effect of the dietary cellulose content in the adult. FEMS Microbiol Lett 57:87–90
    [Google Scholar]
  4. Brosch R., Gordon S. V., Garnier T., Eiglmeier K., Frigui W., Valenti P., Dos Santos S., Duthoy S., Lacroix C. other authors 2007; Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci U S A 104:5596–5601
    [Google Scholar]
  5. Cantarel B. L., Coutinho P. M., Rancurel C., Bernard T., Lombard V., Henrissat B. 2009; The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:D233–D238
    [Google Scholar]
  6. Cole S. T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S. V., Eiglmeier K., Gas S. other authors 1998; Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544
    [Google Scholar]
  7. Cole S. T., Eiglmeier K., Parkhill J., James K. D., Thomson N. R., Wheeler P. R., Honoré N., Garnier T., Churcher C. other authors 2001; Massive gene decay in the leprosy bacillus. Nature 409:1007–1011
    [Google Scholar]
  8. Danelishvili L., Wu M., Young L. S., Bermudez L. E. 2005; Genomic approach to identifying the putative target of and mechanisms of resistance to mefloquine in mycobacteria. Antimicrob Agents Chemother 49:3707–3714
    [Google Scholar]
  9. Doi R. H., Kosugi A. 2004; Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nat Rev Microbiol 2:541–551
    [Google Scholar]
  10. El Khechine A., Henry M., Raoult D., Drancourt M. 2009; Detection of Mycobacterium tuberculosis complex organisms in the stools of patients with pulmonary tuberculosis. Microbiology 155:2384–2389
    [Google Scholar]
  11. Garnier T., Eiglmeier K., Camus J. C., Medina N., Mansoor H., Pryor M., Duthoy S., Grondin S., Lacroix C. other authors 2003; The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci U S A 100:7877–7882
    [Google Scholar]
  12. Geiman D. E., Kaushal D., Ko C., Tyagi S., Manabe Y. C., Schroeder B. G., Fleischmann R. D., Morrison N. E., Converse P. J. other authors 2004; Attenuation of late-stage disease in mice infected by the Mycobacterium tuberculosis mutant lacking the SigF alternate sigma factor and identification of SigF-dependent genes by microarray analysis. Infect Immun 72:1733–1745
    [Google Scholar]
  13. Gilbert H. J., Stalbrand H., Brumer H. 2008; How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation. Curr Opin Plant Biol 11:338–348
    [Google Scholar]
  14. Hagedorn M., Rohde K. H., Russell D. G., Soldati T. 2009; Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 323:1729–1733
    [Google Scholar]
  15. Li L., Bannantine J. P., Zhang Q., Amonsin A., May B. J., Alt D., Banerji N., Kanjilal S., Kapur V. 2005; The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. Proc Natl Acad Sci U S A 102:12344–12349
    [Google Scholar]
  16. Lynd L. R., Weimer P. J., van Zyl W. H., Pretorius I. S. 2002; Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577
    [Google Scholar]
  17. Mahairas G. G., Sabo P. J., Hickey M. J., Singh D. C., Stover C. K. 1996; Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 178:1274–1282
    [Google Scholar]
  18. Pearce M. M., Cianciotto N. P. 2009; Legionella pneumophila secretes an endoglucanase that belongs to the family-5 of glycosyl hydrolases and is dependent upon type II secretion. FEMS Microbiol Lett 300:256–264
    [Google Scholar]
  19. Renesto P., Crapoulet N., Ogata H., La S. B., Vestris G., Claverie J. M., Raoult D. 2003; Genome-based design of a cell-free culture medium for Tropheryma whipplei. Lancet 362:447–449
    [Google Scholar]
  20. Riley R. L., Mills C. C., Nyka W., Weinstock N., Storey P. B., Sultan L. U., Riley M. C., Wells W. F. 1995; Aerial dissemination of pulmonary tuberculosis. A two-year study of contagion in a tuberculosis ward. 1959. Am J Epidemiol 142:3–14
    [Google Scholar]
  21. Rodwell T. C., Moore M., Moser K. S., Brodine S. K., Strathdee S. A. 2008; Tuberculosis from Mycobacterium bovis in binational communities, United States. Emerg Infect Dis 14:909–916
    [Google Scholar]
  22. Seki M., Honda I., Fujita I., Yano I., Yamamoto S., Koyama A. 2009; Whole genome sequence analysis of Mycobacterium bovis bacillus Calmette-Guerin (BCG) Tokyo 172: a comparative study of BCG vaccine substrains. Vaccine 27:1710–1716
    [Google Scholar]
  23. Stinear T. P., Seemann T., Pidot S., Frigui W., Reysset G., Garnier T., Meurice G., Simon D., Bouchier C. other authors 2007; Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res 17:192–200
    [Google Scholar]
  24. Stinear T. P., Seemann T., Harrison P. F., Jenkin G. A., Davies J. K., Johnson P. D., Abdellah Z., Arrowsmith C., Chillingworth T. other authors 2008; Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 18:729–741
    [Google Scholar]
  25. Sulzenbacher G., Shareck F., Morosoli R., Dupont C., Davies G. J. 1997; The Streptomyces lividans family 12 endoglucanase: construction of the catalytic core, expression, and X-ray structure at 1.75 Å resolution. Biochemistry 36:16032–16039
    [Google Scholar]
  26. Taylor S. J., Ahonen L. J., de Leij F. A., Dale J. W. 2003; Infection of Acanthamoeba castellanii with Mycobacterium bovis and M. bovis BCG and survival of M. bovis within the amoebae. Appl Environ Microbiol 69:4316–4319
    [Google Scholar]
  27. Varel V. H., Fryda S. J., Robinson I. M. 1984; Cellulolytic bacteria from pig large intestine. Appl Environ Microbiol 47:219–221
    [Google Scholar]
  28. Varner J. E., Lin L. S. 1989; Plant cell wall architecture. Cell 56:231–239
    [Google Scholar]
  29. Varrot A., Leydier S., Pell G., Macdonald J. M., Stick R. V., Henrissat B., Gilbert H. J., Davies G. J. 2005; M ycobacterium tuberculosis strains possess functional cellulases. J Biol Chem 280:20181–20184
    [Google Scholar]
  30. Wilkins M. J., Meyerson J., Bartlett P. C., Spieldenner S. L., Berry D. E., Mosher L. B., Kaneene J. B., Robinson-Dunn B., Stobierski M. G., Boulton M. L. 2008; Human Mycobacterium bovis infection and bovine tuberculosis outbreak, Michigan, 1994–2007. Emerg Infect Dis 14:657–660
    [Google Scholar]
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