1887

Abstract

The coenzyme B production pathway in has been deduced using a combination of genetic, biochemical and bioinformatics approaches. The coenzyme B gene cluster of CRL1098 has the unique feature of clustering together the , and genes. It consists of 29 ORFs encoding the complete enzymic machinery necessary for biosynthesis. Transcriptional analysis showed it to be expressed as two tandem transcripts of approximately 22 and 4 kb, carrying , , , , , and , respectively. Both transcripts appear to be similarly regulated, and under the conditions assayed are induced in the late-exponential growth phase. Evidence for a regulatory mechanism of negative feedback inhibition by vitamin B itself was observed. Comparative genomics analysis of the coding sequences showed them to be most similar to those coding for the anaerobic coenzyme B pathways previously characterized in a few representatives of the genera and . This contrasts with the trusted species phylogeny and suggests horizontal gene transfer of the B biosynthesis genes. G+C content and codon adaptation index analysis is suggestive that the postulated transfer of these genes was not a recent event. Additional comparative genomics and transcriptional analysis of the sequences acquired during this study suggests a functional link between coenzyme B biosynthesis and reuterin production, which might be implicated in 's success in colonizing the gastrointestinal tract. This information on gene organization, gene transcription and gene acquisition is relevant for the development of (fermented) foods and probiotics enriched in B.

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2008-01-01
2024-03-29
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References

  1. Ailion M., Bobik T. A., Roth J. R. 1993; Two global regulatory systems (Crp and Arc) control the cobalamin/propanediol regulon of Salmonella typhimurium . J Bacteriol 175:7200–7208
    [Google Scholar]
  2. Albert M. J., Mathan V. I., Baker S. J. 1980; Vitamin B12 synthesis by human small intestinal bacteria. Nature 283:781–782
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
    [Google Scholar]
  4. Anderson P. J., Entsch B., McKay D. B. 2001; A gene, cobA + hemD , from Selenomonas ruminantium encodes a bifunctional enzyme involved in the synthesis of vitamin B12 . Gene 281:63–70
    [Google Scholar]
  5. Banerjee R. 2006; B12 trafficking in mammals: a for coenzyme escort service. ACS Chem Biol 1:149–159
    [Google Scholar]
  6. Battersby A. R. 1994; How nature builds the pigments of life: the conquest of vitamin B12 . Science 264:1551–1557
    [Google Scholar]
  7. Bengert P., Dandekar T. 2004; Riboswitch finder – a tool for identification of riboswitch RNAs. Nucleic Acids Res 32:W154–W159
    [Google Scholar]
  8. Bobik T. A., Ailion M., Roth J. R. 1992; A single regulatory gene integrates control of vitamin B12 synthesis and propanediol degradation. J Bacteriol 174:2253–2266
    [Google Scholar]
  9. Bobik T. A., Havemann G. D., Busch R. J., Williams D. S., Aldrich H. C. 1999; The propanediol utilization ( pdu ) operon of Salmonella enterica serovar Typhimurium LT2 includes genes necessary for formation of polyhedral organelles involved in coenzyme B12-dependent 1,2-propanediol degradation. J Bacteriol 181:5967–5975
    [Google Scholar]
  10. Croft M. T., Lawrence A. D., Raux-Deery E., Warren M. J., Smith A. G. 2005; Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93
    [Google Scholar]
  11. Daniel R., Bobik T. A., Gottschalk G. 1998; Biochemistry of coenzyme B12-dependent glycerol and diol dehydratases and organization of the encoding genes. FEMS Microbiol Rev 22:553–566
    [Google Scholar]
  12. Deng W., Liou S.-R., Plunkett G. III, Mayhew G. F., Rose D. J., Burland V., Kodoyianni V., Schwartz D. C., Blattner F. R. 2003; Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J Bacteriol 185:2330–2337
    [Google Scholar]
  13. Edgar R. C. 2004; MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113
    [Google Scholar]
  14. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P. other authors 2001; Comparative genomics of Listeria species. Science 294:849–852
    [Google Scholar]
  15. Griffiths-Jones S., Bateman A., Marshall M., Khanna A., Eddy S. R. 2003; Rfam: an RNA family database. Nucleic Acids Res 31:439–441
    [Google Scholar]
  16. Kuipers O. P., Beerthuyzen M. M., Siezen R. J., De Vos W. M. 1993; Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis . Requirement of expression of the nisA and nisI genes for development of immunity. Eur J Biochem 216:281–291
    [Google Scholar]
  17. Kumar S., Tamura K., Nei M. 2004; MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163
    [Google Scholar]
  18. Ma D., Forsythe P., Bienenstock J. 2004; Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect Immun 72:5308–5314
    [Google Scholar]
  19. Maggio-Hall L. A., Escalante-Semerena J. C. 1999; In vitro synthesis of the nucleotide loop of cobalamin by Salmonella typhimurium enzymes. Proc Natl Acad Sci U S A 96:11798–11803
    [Google Scholar]
  20. Maloy S. R., Stewart V. L., Taylor R. K. 1996 Genetic Analysis of Pathogenic Bacteria: a Laboratory Manual Plainview, NY: Cold Spring Harbor Laboratory;
  21. Martens J. H., Barg H., Warren M. J., Jahn D. 2002; Microbial production of vitamin B12 . Appl Microbiol Biotechnol 58:275–285
    [Google Scholar]
  22. O'Toole G. A., Rondon M. R., Escalante-Semerena J. C. 1993; Analysis of mutants of Salmonella typhimurium defective in the synthesis of the nucleotide loop of cobalamin. J Bacteriol 175:3317–3326
    [Google Scholar]
  23. Overbeek R., Larsen N., Walunas T., D'Souza M., Pusch G., Selkov E. Jr, Liolios K., Joukov V., Kaznadzey D. other authors 2003; The ERGO genome analysis and discovery system. Nucleic Acids Res 31:164–171
    [Google Scholar]
  24. Raux E., Lanois A., Levillayer F., Warren M. J., Brody E., Rambach A., Thermes C. 1996; Salmonella typhimurium cobalamin (vitamin B12) biosynthetic genes: functional studies in S. typhimurium and Escherichia coli . J Bacteriol 178:753–767
    [Google Scholar]
  25. Rice P., Longden I., Bleasby A. 2000; EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277
    [Google Scholar]
  26. Rodionov D. A., Vitreschak A. G., Mironov A. A., Gelfand M. S. 2003; Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 278:41148–41159
    [Google Scholar]
  27. Roessner C. A., Scott A. I. 2006; Fine-tuning our knowledge of the anaerobic route to cobalamin (vitamin B12 . J Bacteriol 188:7331–7334
    [Google Scholar]
  28. Roest K., Heilig H. G., Smidt H., de Vos W. M., Stams A. J., Akkermans A. D. 2005; Community analysis of a full-scale anaerobic bioreactor treating paper mill wastewater. Syst Appl Microbiol 28:175–185
    [Google Scholar]
  29. Roth J. R., Lawrence J. G., Rubenfield M., Kieffer-Higgins S., Church G. M. 1993; Characterization of the cobalamin (vitamin B12) biosynthetic genes of Salmonella typhimurium . J Bacteriol 175:3303–3316
    [Google Scholar]
  30. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  31. Saxelin M., Tynkkynen S., Mattila-Sandholm T., de Vos W. M. 2005; Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16:204–211
    [Google Scholar]
  32. Sharp P. M., Li W. H. 1987; The codon adaptation index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295
    [Google Scholar]
  33. St Maurice M., Mera P. E., Taranto M. P., Sesma F., Escalante-Semerena J. C., Rayment I. 2007; Structural characterization of the active site of the PduO-type ATP : Co(I)rrinoid adenosyltransferase from Lactobacillus reuteri . J Biol Chem 282:2596–2605
    [Google Scholar]
  34. Stabler S. P. 1999; B12 and nutrition. In Chemistry and Biochemistry ofB12 pp 343–365 Edited by Banerjee R. New York: Wiley;
    [Google Scholar]
  35. Sybesma W., Starrenburg M., Kleerebezem M., Mierau I., de Vos W. M., Hugenholtz J. 2003; Increased production of folate by metabolic engineering of Lactococcus lactis . Appl Environ Microbiol 69:3069–3076
    [Google Scholar]
  36. Sybesma W., Burgess C., Starrenburg M., van Sinderen D., Hugenholtz J. 2004; Multivitamin production in Lactococcus lactis using metabolic engineering. Metab Eng 6:109–115
    [Google Scholar]
  37. Talarico T. L., Dobrogosz W. J. 1989; Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri . Antimicrob Agents Chemother 33:674–679
    [Google Scholar]
  38. Talarico T. L., Casas I. A., Chung T. C., Dobrogosz W. J. 1988; Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri . Antimicrob Agents Chemother 32:1854–1858
    [Google Scholar]
  39. Taranto M. P., Medici M., Perdigon G., Ruiz Holgado A. P., Valdez G. F. 2000; Effect of Lactobacillus reuteri on the prevention of hypercholesterolemia in mice. J Dairy Sci 83:401–403
    [Google Scholar]
  40. Taranto M. P., Vera J. L., Hugenholtz J., De Valdez G. F., Sesma F. 2003; Lactobacillus reuteri CRL1098 produces cobalamin. J Bacteriol 185:5643–5647
    [Google Scholar]
  41. Thompson J. D., Higgins D. G., Gibson T. J. 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
    [Google Scholar]
  42. van der Heijden R. T., Snel B., van Noort V., Huynen M. A. 2007; Orthology prediction at scalable resolution by phylogenetic tree analysis. BMC Bioinformatics 8:83
    [Google Scholar]
  43. van Kranenburg R., Kleerebezem M., de Vos W. M. 2000; Nucleotide sequence analysis of the lactococcal EPS plasmid pNZ4000. Plasmid 43:130–136
    [Google Scholar]
  44. Vitreschak A. G., Rodionov D. A., Mironov A. A., Gelfand M. S. 2003; Regulation of the vitamin B12 metabolism and transport in bacteria by a conserved RNA structural element. RNA 9:1084–1097
    [Google Scholar]
  45. Walter J., Heng N. C., Hammes W. P., Loach D. M., Tannock G. W., Hertel C. 2003; Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl Environ Microbiol 69:2044–2051
    [Google Scholar]
  46. Wegkamp A., Starrenburg M., de Vos W. M., Hugenholtz J., Sybesma W. 2004; Transformation of folate-consuming Lactobacillus gasseri into a folate producer. Appl Environ Microbiol 70:3146–3148
    [Google Scholar]
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