1887

Abstract

The locus necessary for the utilization of erythritol as a sole carbon source, contains 17 genes, including genes that encode an ABC transporter necessary for the transport of erythritol, as well as the genes encoding EryA, EryB, EryC, TpiB and the regulators EryD and EryR (SMc01615). Construction of defined deletions and complementation experiments show that the other genes at this locus encode products that are necessary for the catabolism of adonitol (ribitol) and -arabitol, but not -arabitol. These analyses show that aside from one gene that is specific for the catabolism of -arabitol (, ), the rest of the catabolic genes are necessary for both polyols (, ; , ; , ). Genetic and biochemical data show that in addition to utilizing erythritol as a substrate, EryA is also capable of utilizing adonitol and -arabitol. Similarly, transport experiments using labelled erythritol show that adonitol, -arabitol and erythritol share a common transporter (MptABCDE). Quantitative RT-PCR experiments show that transcripts containing genes necessary for adonitol and -arabitol utilization are induced by these sugars in an -dependent manner.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.057877-0
2012-08-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/8/2180.html?itemId=/content/journal/micro/10.1099/mic.0.057877-0&mimeType=html&fmt=ahah

References

  1. Adhya S. L., Shapiro J. A.. ( 1969;). The galactose operon of E. coli K-12. I. Structural and pleiotropic mutations of the operon. Genetics62:231–247[PubMed]
    [Google Scholar]
  2. Alexeyev M. F.. ( 1999;). The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. Biotechniques26:824–826, 828[PubMed]
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J. H., Zhang Z., Miller W., Lipman D. J.. ( 1997;). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  4. Anderson R. L., Sapico V. L.. ( 1975;). d-Fructose (d-mannose) kinase. Methods Enzymol42:39–43 [CrossRef][PubMed]
    [Google Scholar]
  5. Clark S. R. D., Oresnik I. J., Hynes M. F.. ( 2001;). RpoN of Rhizobium leguminosarum bv. viciae strain VF39SM plays a central role in FnrN-dependent microaerobic regulation of genes involved in nitrogen fixation. Mol Gen Genet264:623–633 [CrossRef][PubMed]
    [Google Scholar]
  6. Dahms A. S., Anderson R. L.. ( 1969;). 2-Keto-3-deoxyl-l-arabonate aldolase and its role in a new pathway of l-arabinose degradation. Biochem Biophys Res Commun36:809–814 [CrossRef][PubMed]
    [Google Scholar]
  7. Dunn M. F., Araíza G., Finan T. M.. ( 2001;). Cloning and characterization of the pyruvate carboxylase from Sinorhizobium meliloti Rm1021. Arch Microbiol176:355–363 [CrossRef][PubMed]
    [Google Scholar]
  8. Finan T. M., Hartweig E., LeMieux K., Bergman K., Walker G. C., Signer E. R.. ( 1984;). General transduction in Rhizobium meliloti . J Bacteriol159:120–124[PubMed]
    [Google Scholar]
  9. Finan T. M., Hirsch A. M., Leigh J. A., Johansen E., Kuldau G. A., Deegan S., Walker G. C., Signer E. R.. ( 1985;). Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell40:869–877 [CrossRef][PubMed]
    [Google Scholar]
  10. Finan T. M., Kunkel B., De Vos G. F., Signer E. R.. ( 1986;). Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol167:66–72[PubMed]
    [Google Scholar]
  11. Finan T. M., Oresnik I., Bottacin A.. ( 1988;). Mutants of Rhizobium meliloti defective in succinate metabolism. J Bacteriol170:3396–3403[PubMed]
    [Google Scholar]
  12. Fry J., Wood M., Poole P. S.. ( 2001;). Investigation of myo-inositol catabolism in Rhizobium leguminosarum bv. viciae and its effect on nodulation competitiveness. Mol Plant Microbe Interact14:1016–1025 [CrossRef][PubMed]
    [Google Scholar]
  13. Geddes B. A., Pickering B. S., Poysti N. J., Collins H., Yudistira H., Oresnik I. J.. ( 2010;). A locus necessary for the transport and catabolism of erythritol in Sinorhizobium meliloti . Microbiology156:2970–2981 [CrossRef][PubMed]
    [Google Scholar]
  14. Geer L. Y., Domrachev M., Lipman D. J., Bryant S. H.. ( 2002;). CDART: protein homology by domain architecture. Genome Res12:1619–1623 [CrossRef][PubMed]
    [Google Scholar]
  15. Ghalambor M. A., Heath E. C.. ( 1962;). The metabolism of L-fucose. II. The enzymatic cleavage of L-fuculose 1-phosphate. J Biol Chem237:2427–2433[PubMed]
    [Google Scholar]
  16. Hanahan D.. ( 1983;). Studies on transformation of Escherichia coli with plasmids. J Mol Biol166:557–580 [CrossRef][PubMed]
    [Google Scholar]
  17. House B. L., Mortimer M. W., Kahn M. L.. ( 2004;). New recombination methods for Sinorhizobium meliloti genetics. Appl Environ Microbiol70:2806–2815 [CrossRef][PubMed]
    [Google Scholar]
  18. Hunter S., Apweiler R., Attwood T. K., Bairoch A., Bateman A., Binns D., Bork P., Das U., Daugherty L.. & other authors ( 2009;). InterPro: the integrative protein signature database. Nucleic Acids Res37:Database issueD211–D215 [CrossRef][PubMed]
    [Google Scholar]
  19. Jacob A. I., Adham S. A., Capstick D. S., Clark S. R. D., Spence T., Charles T. C.. ( 2008;). Mutational analysis of the Sinorhizobium meliloti short-chain dehydrogenase/reductase family reveals substantial contribution to symbiosis and catabolic diversity. Mol Plant Microbe Interact21:979–987 [CrossRef][PubMed]
    [Google Scholar]
  20. Jones J. D. G., Gutterson N.. ( 1987;). An efficient mobilizable cosmid vector, pRK7813, and its use in a rapid method for marker exchange in Pseudomonas fluorescens strain HV37a. Gene61:299–306 [CrossRef][PubMed]
    [Google Scholar]
  21. Kohler P. R. A., Zheng J. Y., Schoffers E., Rossbach S.. ( 2010;). Inositol catabolism, a key pathway in Sinorhizobium meliloti for competitive host nodulation. Appl Environ Microbiol76:7972–7980 [CrossRef][PubMed]
    [Google Scholar]
  22. Krol E., Becker A.. ( 2004;). Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. Mor Gen Genet272:1–17 [CrossRef][PubMed]
    [Google Scholar]
  23. LeBlanc D. J., Mortlock R. P.. ( 1971;). Metabolism of d-arabinose: a new pathway in Escherichia coli . J Bacteriol106:90–96[PubMed]
    [Google Scholar]
  24. Lodwig E., Poole P.. ( 2003;). Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci22:37–78 [CrossRef]
    [Google Scholar]
  25. Luo Y., Samuel J., Mosimann S. C., Lee J. E., Tanner M. E., Strynadka N. C.. ( 2001;). The structure of l-ribulose-5-phosphate 4-epimerase: an aldolase-like platform for epimerization. Biochemistry40:14763–14771 [CrossRef][PubMed]
    [Google Scholar]
  26. Martinez De Drets G., Arias A.. ( 1970;). Metabolism of some polyols by Rhizobium meliloti . J Bacteriol103:97–103[PubMed]
    [Google Scholar]
  27. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. R.. ( 1982;). Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol149:114–122[PubMed]
    [Google Scholar]
  28. Miller-Williams M., Loewen P. C., Oresnik I. J.. ( 2006;). Isolation of salt-sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiology152:2049–2059 [CrossRef][PubMed]
    [Google Scholar]
  29. Mortlock R. P.. ( 1984;). The utilization of pentitols in the studies of the evolution of enzyme pathways. Microorganisms as Model Systems for Studying Evolution1–21 Mortlock R. P.. New York: Plenum Press;[CrossRef]
    [Google Scholar]
  30. Mortlock R. P., Wood W. A.. ( 1964a;). Metabolism of pentoses and pentitols by Aerobacter aerogenes. I. Demonstration of pentose isomerase, penulokinase, and pentitiol dehydrogenase enzyme families. J Bacteriol88:838–844[PubMed]
    [Google Scholar]
  31. Mortlock R. P., Wood W. A.. ( 1964b;). Metabolism of pentoses and pentitols by Aerobacter aerogenes. II. Mechanism of acquistion of kinase, isomerase, and dehydrogenase activity. J Bacteriol88:845–849[PubMed]
    [Google Scholar]
  32. Mortlock R. P., Fossitt D. D., Petering D. H., Wood W. A.. ( 1965a;). Metabolism of pentoses and pentitols by Aerobacter aerogenes. III. Physical and immunological properties of pentitol dehydrogenases and pentulokinases. J Bacteriol89:129–135[PubMed]
    [Google Scholar]
  33. Mortlock R. P., Fossitt D. D., Wood W. A.. ( 1965b;). A basis for utlization of unnatural pentoses and pentitols by Aerobacter aerogenes . Proc Natl Acad Sci U S A54:572–579 [CrossRef][PubMed]
    [Google Scholar]
  34. Oresnik I. J., Layzell D. B.. ( 1994;). Composition and distribution of adenylates in soybean (Glycine max L.) nodule tissue. Plant Physiol104:217–225[PubMed]
    [Google Scholar]
  35. Oresnik I. J., Pacarynuk L. A., O'Brien S. A. P., Yost C. K., Hynes M. F.. ( 1998;). Plasmid encoded catabolic genes in Rhizobium leguminosarum bv. trifolii: evidence for a plant-inducible rhamnose locus involved in competition for nodulation. Mol Plant Microbe Interact11:1175–1185 [CrossRef]
    [Google Scholar]
  36. Pedrosa F. O., Zancan G. T.. ( 1974;). l-Arabinose metabolism in Rhizobium japonicum . J Bacteriol119:336–338[PubMed]
    [Google Scholar]
  37. Pickering B. S., Oresnik I. J.. ( 2008;). Formate-dependent autotrophic growth in Sinorhizobium meliloti . J Bacteriol190:6409–6418 [CrossRef][PubMed]
    [Google Scholar]
  38. Platt R., Dresner S. K., Park S. K., Phillips G. J.. ( 2000;). Genetic systems for reversible integration of DNA constructs and lacZ gene fusions into the Escherichia coli chromosome. Plasmid43:12–23[PubMed][CrossRef]
    [Google Scholar]
  39. Poysti N. J., Oresnik I. J.. ( 2007;). Characterization of Sinorhizobium meliloti triose phosphate isomerase genes. J Bacteriol189:3445–3451 [CrossRef][PubMed]
    [Google Scholar]
  40. Poysti N. J., Loewen E. D., Wang Z., Oresnik I. J.. ( 2007;). Sinorhizobium meliloti pSymB carries genes necessary for arabinose transport and catabolism. Microbiology153:727–736 [CrossRef][PubMed]
    [Google Scholar]
  41. Primrose S. B., Ronson C. W.. ( 1980;). Polyol metabolism by Rhizobium trifolii . J Bacteriol141:1109–1114[PubMed]
    [Google Scholar]
  42. Quandt J., Hynes M. F.. ( 1993;). Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene127:15–21 [CrossRef][PubMed]
    [Google Scholar]
  43. Ramachandran V. K., East A. K., Karunakaran R., Downie J. A., Poole P. S.. ( 2011;). Adaptation of Rhizobium leguminosarum to pea, alfalfa and sugar beet rhizospheres investigated by comparative transcriptomics. Genome Biol12:R106 [CrossRef][PubMed]
    [Google Scholar]
  44. Richardson J. S., Hynes M. F., Oresnik I. J.. ( 2004;). A genetic locus necessary for rhamnose uptake and catabolism in Rhizobium leguminosarum bv. trifolii . J Bacteriol186:8433–8442 [CrossRef][PubMed]
    [Google Scholar]
  45. Richardson J. S., Carpena X., Switala J., Perez-Luque R., Donald L. J., Loewen P. C., Oresnik I. J.. ( 2008;). RhaU of Rhizobium leguminosarum is a rhamnose mutarotase. J Bacteriol190:2903–2910 [CrossRef][PubMed]
    [Google Scholar]
  46. Ronson C. W., Primrose S. B.. ( 1979;). Effect of glucose on polyol metabolism by Rhizobium trifolii . J Bacteriol139:1075–1078[PubMed]
    [Google Scholar]
  47. Sambrook J., Fritsch E. F., Maniatis T.. ( 1989;). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  48. Sangari F. J., Agüero J., García-Lobo J. M.. ( 2000;). The genes for erythritol catabolism are organized as an inducible operon in Brucella abortus . Microbiology146:487–495[PubMed]
    [Google Scholar]
  49. Schroeder B. K., House B. L., Mortimer M. W., Yurgel S. N., Maloney S. C., Ward K. L., Kahn M. L.. ( 2005;). Development of a functional genomics platform for Sinorhizobium meliloti: construction of an ORFeome. Appl Environ Microbiol71:5858–5864 [CrossRef][PubMed]
    [Google Scholar]
  50. Simon R., Priefer U., Pühler A.. ( 1983;). A broad host range mobilization system for in vivo engineering: transposon mutagenesis in gram-negative bacteria. Biotechniques1:784–791 [CrossRef]
    [Google Scholar]
  51. Sperry J. F., Robertson D. C.. ( 1975;). Inhibition of growth by erythritol catabolism in Brucella abortus . J Bacteriol124:391–397[PubMed]
    [Google Scholar]
  52. Vincent J. M.. ( 1970;). A manual for the Practical Study of Root-Nodule Bacteria Oxford, UK: Blackwell Scientific Publications;
    [Google Scholar]
  53. Wang C., Meek D. J., Panchal P., Boruvka N., Archibald F. S., Driscoll B. T., Charles T. C.. ( 2006;). Isolation of poly-3-hydroxybutyrate metabolism genes from complex microbial communities by phenotypic complementation of bacterial mutants. Appl Environ Microbiol72:384–391 [CrossRef][PubMed]
    [Google Scholar]
  54. White J., Prell J., James E. K., Poole P.. ( 2007;). Nutrient sharing between symbionts. Plant Physiol144:604–614 [CrossRef][PubMed]
    [Google Scholar]
  55. Wood W. A., McDonough M. J., Jacobs L. B.. ( 1961;). Ribitol and D-arabitol utilization by Aerobacter aerogenes . J Biol Chem236:2190–2195[PubMed]
    [Google Scholar]
  56. Yost C. K., Rath A. M., Noel T. C., Hynes M. F.. ( 2006;). Characterization of genes involved in erythritol catabolism in Rhizobium leguminosarum bv. viciae . Microbiology152:2061–2074 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.057877-0
Loading
/content/journal/micro/10.1099/mic.0.057877-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error