Lactobacillus reuteri DSM 20016 produces cobalamin-dependent diol dehydratase in metabolosomes and metabolizes 1,2-propanediol by disproportionation

Journal of Bacteriology

Volumn 190, Issue 13, 2008, Pages 4559-4567

  Sriramulu, Dinesh Diraviam ^a   Liang, Mingzhi ^a   Hernandez Romero, Diana ^a   Raux Deery, Evelyne ^b   Lünsdorf, Heinrich ^c   Parsons, Joshua B ^b   Warren, Martin J ^b   Prentice, Michael B ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF KENT   (United Kingdom)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COBALAMIN; HYDROLYASE; PROPANOL; PROPIONIC ACID; PROPYLENE GLYCOL;

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM ISOLATION; CYTOPLASM; DNA SEQUENCE; ELECTRON MICROSCOPY; ENTEROBACTERIACEAE; ENZYME SYNTHESIS; GENE SEQUENCE; GENE STRUCTURE; INTESTINE; LACTOBACILLLUS REUTERI; LACTOBACILLUS; METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PRIORITY JOURNAL; STRUCTURAL GENE;

1-PROPANOL; BACTERIAL PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCERALDEHYDE; LACTOBACILLUS REUTERI; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; OPERON; POLYMERASE CHAIN REACTION; PROPANE; PROPANEDIOL DEHYDRATASE; PROPIONATES; PROPYLENE GLYCOL; SEQUENCE ANALYSIS, DNA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VITAMIN B 12;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; LACTOBACILLUS; LACTOBACILLUS REUTERI; LACTOBACILLUS REUTERI JCM 1112; NEGIBACTERIA;

EID: 46049098363     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01535-07     Document Type: Article

References (63)

1. Ailion, M., T. A. Bobik, and J. R. Roth. 1993. Two global regulatory systems (Crp and Arc) control the cobalamin/propanediol regulon of Salmonella typhimurium. J. Bacteriol. 175:7200-7208.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25:3389-3402.
3. Anderson, R. C., M. A. Rasmussen, and M. J. Allison. 1993. Metabolism of the plant toxins nitropropionic acid and nitropropanol by ruminal microorganisms. Appl. Environ. Microbiol. 59:3056-3061.
4. Andersson, U., D. Molenaar, P. Radstrom, and W. M. de Vos. 2005. Unity in organisation and regulation of catabolic operons in Lactobacillus plantarum, Lactococcus lactis and Listeria monocytogenes. Syst. Appl. Microbiol. 28:187-195.
5. Bailey, T. L., and C. Elkan. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2:28-36.
6. Barrangou, R., M. A. Azcarate-Peril, T. Duong, S. B. Conners, R. M. Kelly, and T. R. Klaenhamnier. 2006. Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc. Natl. Acad. Sci. USA 103:3816-3821.
7. Belkin, S., R. J. Mehlhorn, and L. Packer. 1987. Proton gradients in intact cyanobacteria. Plant Physiol. 84:25-30.
8. 12-dependent 1,2-propanediol degradation. J. Bacteriol. 181:5967-5975.
9. Booth, I. R. 1985. Regulation of cytoplasmic pH in bacteria. Microbiol. Rev. 49:359-378.
10. Brinsmade, S. R., T. Paldon, and J. C. Escalante-Semerena. 2005. Minimal functions and physiological conditions required for growth of Salmonella enterica on ethanolamine in the absence of the metabolosome. J. Bacteriol. 187:8039-8046.
11. Cannon, G. C., C. E. Bradburne, H. C. Aldrich, S. H. Baker, S. Heinhorst, and J. M. Shively. 2001. Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl. Environ Microbiol. 67:5351-5361.
12. Casas, I., and W. Dobrogosz. 2000. Validation of the probiotic concept: Lactobacillus reuteri confers broad-spectrum protection against disease in humans and animals. Microb. Ecol. Health Dis. 12:247-285.
13. Daniel, R., T. A. Bobik, and G. Gottschalk. 1998. Biochemistry of coenzyme B12-dcpcndent glycerol and diol dehydratases and organization of the encoding genes. FEMS Microbiol. Rev. 22:553-566.
14. de Man, J., M. Ragosa, and M. Sharpe. 1960. A medium for the cultivation of lactobacilli. J. Appl. Bacteriol. 23:130-135.
15. 12-dependent degradation of 1,2-propanediol in Salmonella enterica serovar Typhimurium LT2. J. Bacteriol. 185:5086-5095.
16. Horswill, A. R., and J. C. Escalante-Semerena. 1999. Salmonella typhimurium LT2 catabolizcs propionate via the 2-methylcitric acid cycle. J. Bacteriol. 181:5615-5623.
17. Kerfeld, C. A., M. R. Sawaya, S. Tanaka, C. V. Nguyen, M. Phillips, M. Beeby, and T. O. Yeates. 2005. Protein structures forming the shell of primitive bacterial organelles. Science 309:936-938.
18. Kim, J. H., Y. K. Yang, and G. H. Chambliss. 2005. Evidence that Bacillus catabolite control protein CcpA interacts with RNA polymerase to inhibit transcription. Mol. Microbiol. 56:155-162.
19. Konings, W. N. 2002. The cell membrane and the struggle for life of lactic acid bacteria. Antonie Leeuwenhoek 82:3-27.
20. Krooneman, J., F. Faber, A. C. Alderkamp, S. Oude Elferink, F. Driehuis, I. Cleenwerck, J. Swings, J. C. Gottschal, and M. Vancanneyt. 2002. Lactobacillus diolivorans sp. nov., a 1,2-propanediol-degrading bacterium isolated from aerobically stable maize silage. Int. J. Syst. Evol. Microbiol. 52:639-646.
21. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
22. Lawrence, J. G., and J. R. Roth. 1996. Evolution of coenzyme B12 synthesis among enteric bacteria: evidence for loss and reacquisition of a multigene complex. Genetics 142:11-24.
23. Leal, N. A., G. D. Havemann, and T. A. Bobik. 2003. PduP is a coenzyme-a-acylating propionaldehyde dehydrogenase associated with the polyhedral bodies involved in B12-dependent 1,2-propanediol degradation by Salmonella enterica serovar Typhimurium LT2. Arch. Microbiol. 180:353-361.
24. Luthi-Peng, Q., F. B. Dileme, and Z. Puhan. 2002. Effect of glucose on glycerol bioconversion by Lactobacillus reuteri. Appl. Microbiol. Biotechnol. 59:289-296.
25. Makarova, K., A. Slesarev, Y. Wolf, A. Sorokin, B. Mirkin, E. Koonin, A. Pavlov, N. Pavlova, V. Karamychev, N. Polouchine, V. Shakhova, I. Grigoriev, Y. Lou, D. Rohksar, S. Lucas, K. Huang, D. M. Goodstein, T. Hawkins, V. Plengvidhya, D. Welker, J. Hughes, Y. Goh, A. Benson, K. Baldwin, J. H. Lee, I. Diaz-Muniz, B. Dosti, V. Smeianov, W. Wechter, R. Barabote, G. Lorca, E. Altermann, R. Barrangou, B. Ganesan, Y. Xie, H. Rawsthorne, D. Tamir, C. Parker, F. Breidt, J. Broadbent, R. Hutkins, D. O'Sullivan, J. Steele, G. Unlu, M. Saier, T. Klaenhammer, P. Richardson, S. Kozyavkin, B. Weimer, and D. Mills. 2006. Comparative genomics of the lactic acid bacteria. Proc. Natl. Acad. Sci. USA 103:15611-15616.
26. Miwa, Y., A. Nakata, A. Ogiwara, M. Yamamoto, and Y. Fujita. 2000. Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. Nucleic Acids Res. 28:1206-1210.
27. Munch, R., K. Hiller, A. Grote, M. Scheer, J. Klein, M. Schobert, and D. Jahn. 2005. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21:4187-4189.
28. Obradors, N., J. Badia, L. Baldoma, and J. Aguilar. 1988. Anaerobic metabolism of the L-rhamnosc fermentation product 1,2-propanediol in Salmonella typhimurium. J. Bacteriol. 170:2159-2162.
29. Palacios, S., V. J. Starai, and J. C. Escalante-Semerena. 2003. Propionyl coenzyme A is a common intermediate in the 1,2-propanediol and propionate catabolic pathways needed for expression of the prpBCDE operon during growth of Salmonella enterica on 1,2-propanediol. J. Bacteriol. 185: 2802-2810.
30. Penrod, J. T., and J. R. Roth. 2006. Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. J. Bacteriol. 188: 2865-2874.
31. Price-Carter, M., J. Tingey, T. A. Bobik, and J. R. Roth. 2001. The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonella enterica serovar typhimurium on cthanolamine or 1,2-propanediol. J. Bacteriol. 183:2463-2475.
32. 12) biosynthetic genes: functional studies in S. typhimurium and Escherichia coli. J. Bacteriol. 178:753-767.
33. Rodriguez, E., J. L. Arques, R. Rodriguez, M. Nunez, and M. Medina. 2003. Reuterin production by lactobacilli isolated from pig faeces and evaluation of probiotic traits. Lett. Appl. Microbiol. 37:259-263.
34. Rozen, S., and H. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
35. Rutherford, K., J. Parkhill, J. Crook, T. Horsnell, P. Rice, M. A. Rajandream, and B. Barrell. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
36. Saier, M. H., Jr., S. Chauvaux, J. Deutscher, J. Reizer, and J. J. Ye. 1995. Protein phosphorylation and regulation of carbon metabolism in gram-negative versus gram-positive bacteria. Trends Biochem. Sci. 20:267-271.
37. 12-dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. J. Bacteriol. 190:2966-2971.
38. 12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098. Microbiology 154:81-93.
39. Sauvageot, N. 2002. Ph.D. thesis. Etude du métabolisme du glycerol chez Lactobacillus collinoides: aspects physiologiques, génétiques et biochimiques Université de Caen, Caen, France.
40. Sauvageot, N., V. Pichereau, L. Louarme, A. Hartbe, Y. Auffray, and J.-M. Laplace. 2002. Purification, characterization and subunits identification of the diol dehydratase of Lactobacillus collinoides. Eur. J. Biochem. 269:5731-5737.
41. Sauvageot, N., C. Muller, A. Hartke, Y. Auffray, and J. M. Laplace. 2002. Characterisation of the diol dehydratase pdu operon of Lactobacillus collinoides. FEMS Microbiol. Lett. 209:66-71.
42. Schutz, H., and F. Radler. 1984. Anaerobic reduction of glycerol to propanediol-1,3 by Lactobacillus brevis and Lactobacillus luchneri. Syst. Appl. Microbiol. 5:169-178.
43. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
44. Shively, J. M., C. E. Bradburne, H. C. Aldrich, T. A. Bobik, J. L. Mehlman, S. Jin, and S. H. Baker. 1998. Sequence homologs of the carboxysomal polypeptide CsoS1 of the thiobacilli are present in cyanobacteria and enteric bacteria that form carboxysomes-polyhedral bodies. Can. J. Bot. Rev. Can. Bot. 76:906-916.
45. Siegumfeldt, H., K. Bjorn Rechinger, and M. Jakobsen. 2000. Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl. Environ. Microbiol. 66:2330-2335.
46. Smiley, K. L., and M. Sobolov. 1962. A cobamide-requiring glycerol dehydrase from an acrolein-forming Lactobacillus. Arch. Biochem. Biophys. 97:538-543.
47. Spurr, A. R. 1969. A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43.
48. Talarico, T. L., L. T. Axelsson, J. Novotny, M. Fiuzat, and W. J. Dobrogosz. 1990. Utilization of glycerol as a hydrogen acceptor by Lactobacillus reuteri: purification of 1,3-propanediol:NAD oxidoreductase. Appl. Environ. Microbiol. 56:943-948.
49. Talarico, T. L., I. A. Casas, T. C. Chung, and W. J. Dobrogosz. 1988. Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 32:1854-1858.
50. Talarico, T. L., and W. J. Dobrogosz. 1989. Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 33:674-679.
51. Talarico, T. L., and W. J. Dobrogosz. 1990. Purification and characterization of glycerol dehydratase from Lactobacillus reuteri. Appl. Environ. Microbiol. 56:1195-1197.
52. Taranto, M. P., J. L. Vera, J. Hugenholtz, G. F. De Valdez, and F. Sesma. 2003. Lactobacillus reuteri CRL1098 produces cobalamin. J. Bacteriol. 185: 5643-5647.
53. Toraya, T., and S. Fukui. 1977. Immunochemical evidence for the difference between coenzyme-B12-dependent diol dehydratase and glycerol dehydratase. Eur. J. Biochem. 76:285-289.
54. 12-dependent diol dehydratase. J. Bacteriol. 139:39-47.
55. Toraya, T., S. Kuno, and S. Fukui. 1980. Distribution of coenzyme B12-dependent diol dehydratase and glycerol dehydratase in selected genera of Enterobacteriaceae and Propionibacteriaceae. J. Bacteriol. 141:1439-1442.
56. Toraya, T., T. Shirakashi, T. Kosuga, and S. Fukui. 1976. Substrate specificity of coenzyme B12-dependcnt diol dehydrase: glycerol as both a good substrate and a potent inactivator. Biochem. Biophys. Res. Commun. 69:475-480.
57. Toraya, T., K. Ushio, S. Fukui, and P. C. Hogenkamp. 1977. Studies on the mechanism of the adenosylcobalamin-dependent diol dehydrase reaction by the use of analogs of the coenzyme. J. Biol. Chem. 252:963-970.
58. van Helden, J. 2003. Regulatory sequence analysis tools. Nucleic Acids Res. 31:3593-3596.
59. Ventura, M., C. Canchaya, R. Zink, G. F. Fitzgerald, and D. van Sinderen. 2004. Characterization of the groEL and groES Loci in Bifidobacterium breve UCC 2003: genetic, transcriptional, and phylogenetic analyses. Appl. Environ. Microbiol. 70:6197-6209.
60. Vollenweider, S., and C. Lacroix. 2004. 3-Hydroxypropionaldehyde: applications and perspectives of biotechnological production. Appl. Microbiol. Biotechnol. 64:16-27.
61. Wall, T., K. Bath, R. A. Britton, H. Jonsson, J. Versalovic, and S. Roos. 2007. The early response to acid shock in Lactobacillus reuteri involves the ClpL chaperone and a putative cell wall-altering esterase. Appl. Environ. Microbiol. 73:3924-3935.
62. Wesney, E., and G. Tannock. 1979. Association of rat, pig and fowl biotypes of lactobacilli with the stomach of gnotobiotic mice. Microb. Ecol. 5:35-42.
63. Zomer, A. L., G. Buist, R. Larsen, J. Kok, and O. P. Kuipers. 2007. Time-resolved determination of the CcpA regulon of Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189:16.