1887

Abstract

A genetic locus encoding erythritol uptake and catabolism genes was identified in bv. , and shown to be plasmid encoded in a wide range of strains. A Tn-B22 mutant (19B-3) unable to grow on erythritol was isolated from a mutant library of strain VF39SM. The mutated gene was cloned and partially sequenced, and determined to have a high homology to permease genes of ABC transporters. A cosmid complementing the mutation (pCos42) was identified and was shown to carry all the genes necessary to restore the ability to grow on erythritol to a VF39SM strain cured of pRleVF39f. In the genomic DNA sequence of strain 3841, the gene linked to the mutation in 19B-3 is flanked by a cluster of genes with high homology to the known erythritol catabolic genes from spp. Through mutagenesis studies, three distinct operons on pCos42 that are required for growth on erythritol were identified: an ABC-transporter operon (), a catabolic operon () and an operon () that encodes a gene with significant homology to triosephosphate isomerase (). These genes all share high sequence identity to genes in the erythritol catabolism region of spp., and alignments suggest that horizontal transfer of the erythritol locus may have occurred between and . Transcription of the operon is repressed by EryD and is induced by the presence of erythritol. Mutant 19B-3 was impaired in its ability to compete against wild-type for nodulation of pea plants but was still capable of forming nitrogen-fixing nodules.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28938-0
2006-07-01
2019-11-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/7/2061.html?itemId=/content/journal/micro/10.1099/mic.0.28938-0&mimeType=html&fmt=ahah

References

  1. 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.[CrossRef]
    [Google Scholar]
  2. Baldani, J. I., Weaver, R. W., Hynes, M. F. & Eardly, B. D. ( 1992; ). Utilization of carbon substrates, electrophoretic enzyme patterns, and symbiotic performance of plasmid-cured clover rhizobia. Appl Environ Microbiol 58, 2308–2314.
    [Google Scholar]
  3. Barnett, M. J., Fisher, R. F., Jones, T. & 23 other authors ( 2001; ). Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci U S A 98, 9883–9888.[CrossRef]
    [Google Scholar]
  4. Beattie, G. A. & Handelsman, J. ( 1989; ). A rapid method for the isolation and identification of Rhizobium from root nodules. J Microbiol Methods 9, 29–33.[CrossRef]
    [Google Scholar]
  5. Beringer, J. E. ( 1974; ). R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84, 188–198.[CrossRef]
    [Google Scholar]
  6. Boivin, C., Barran, L. R., Malpica, C. A. & Rosenberg, C. ( 1991; ). Genetic analysis of a region of the Rhizobium meliloti pSym plasmid specifying catabolism of trigonelline, a secondary metabolite present in legumes. J Bacteriol 173, 2809–2817.
    [Google Scholar]
  7. Brewin, N. J., Wood, E. A., Johnston, A. W. B., Dibb, N. J. & Hombrecher, G. ( 1982; ). Recombinant nodulation plasmids in Rhizobium leguminosarum. J Gen Microbiol 128, 1817–1827.
    [Google Scholar]
  8. Brom, S., García-de los Santos, A., Stepkowsky, T., Flores, M., Davila, G., Romero, D. & Palacios, R. ( 1992; ). Different plasmids of Rhizobium leguminosarum bv. phaseoli are required for optimal symbiotic performance. J Bacteriol 174, 5183–5189.
    [Google Scholar]
  9. Brom, S., García-de los Santos, A., Cervantes, L., Palacios, R. & Romero, D. ( 2000; ). In Rhizobium etli symbiotic plasmid transfer, nodulation competitivity and cellular growth require interaction among different replicons. Plasmid 44, 34–43.[CrossRef]
    [Google Scholar]
  10. Capela, D., Barloy-Hubler, F., Gouzy, J. & 25 other authors ( 2001; ). Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci U S A 98, 9877–9882.[CrossRef]
    [Google Scholar]
  11. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G. & Thompson, J. D. ( 2003; ). Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31, 3497–3500.[CrossRef]
    [Google Scholar]
  12. DelVecchio, V. G., Kapatral, V., Redkar, R. J. & 23 other authors ( 2002; ). The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc Natl Acad Sci U S A 99, 443–448.[CrossRef]
    [Google Scholar]
  13. Eardly, B. D., Nour, S. M., van Berkum, P. & Selander, R. K. ( 2005; ). Rhizobial 16S rRNA and dnaK genes: mosaicism and the uncertain phylogenetic placement of Rhizobium galegae. Appl Environ Microbiol 71, 1328–1335.[CrossRef]
    [Google Scholar]
  14. Eckhardt, T. ( 1978; ). A rapid method for the identification of plasmid desoxyribonucleic acid in bacteria. Plasmid 1, 584–588.[CrossRef]
    [Google Scholar]
  15. Englesberg, E., Anderson, R. L., Weinberg, R. N. L. P. H., Huttenhauer, G. & Boyer, H. ( 1962; ). l-Arabinose-sensitive, l-ribulose 5-phosphate 4-epimerase-deficient mutants of Escherichia coli. J Bacteriol 84, 137–146.
    [Google Scholar]
  16. Fellay, R., Frey, J. & Krisch, H. ( 1987; ). Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52, 147–154.[CrossRef]
    [Google Scholar]
  17. Finan, T. M., Weidner, S., Wong, K. & 9 other authors ( 2001; ). The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti. Proc Natl Acad Sci U S A 98, 9889–9894.[CrossRef]
    [Google Scholar]
  18. 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 Interact 14, 1016–1025.[CrossRef]
    [Google Scholar]
  19. Galibert, F., Finan, T. M., Long, S. R. & 47 other authors ( 2001; ). The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293, 668–672.[CrossRef]
    [Google Scholar]
  20. García-de los Santos, A., Morales, A., Baldomá, L., Clark, S. R., Brom, S., Yost, C. K., Hernández-Lucas, I., Aguilar, J. & Hynes, M. F. ( 2002; ). The glcB locus of Rhizobium leguminosarum VF39 encodes an arabinose-inducible malate synthase. Can J Microbiol 48, 922–932.[CrossRef]
    [Google Scholar]
  21. Gaunt, M. W., Turner, S. L., Rigottier-Gois, L., Lloyd-Macgilp, S. A. & Young, J. P. ( 2001; ). Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51, 2037–2048.[CrossRef]
    [Google Scholar]
  22. Goldmann, A., Boivin, C., Fleury, V., Message, B., Lecoeur, L., Maille, M. & Tepfer, D. ( 1991; ). Betaine use by rhizosphere bacteria: genes essential for trigonelline, stachydrine, and carnitine catabolism in Rhizobium meliloti are located on pSym in the symbiotic region. Mol Plant Microbe Interact 4, 571–578.[CrossRef]
    [Google Scholar]
  23. Guntli, D., Heeb, M., Moënne-Loccoz, Y. & Defago, G. ( 1999; ). Contribution of calystegine catabolic plasmid to competitive colonization of the rhizosphere of calystegine-producing plants by Sinorhizobium meliloti Rm41. Mol Ecol 8, 855–863.[CrossRef]
    [Google Scholar]
  24. Halling, S. M., Peterson-Burch, B. D., Bricker, B. J., Zuerner, R. L., Qing, Z., Li, L. L., Kapur, V., Alt, D. P. & Olsen, S. C. ( 2005; ). Completion of the genome sequence of Brucella abortus and comparison to the highly similar genomes of Brucella melitensis and Brucella suis. J Bacteriol 187, 2715–2726.[CrossRef]
    [Google Scholar]
  25. Heinrich, K., Gordon, D. M., Ryder, M. H. & Murphy, P. J. ( 1999; ). A rhizopine strain of Sinorhizobium meliloti remains at a competitive nodulation advantage after an extended period in the soil. Soil Biol Biochem 31, 1063–1065.[CrossRef]
    [Google Scholar]
  26. Hirsch, P. R. ( 1979; ). Plasmid-determined bacteriocin production by Rhizobium leguminosarum. J Gen Microbiol 113, 219–228.[CrossRef]
    [Google Scholar]
  27. Hynes, M. F. & Finan, T. M. ( 1998; ). General genetic knowledge. In The Rhizobiaceae: Molecular Biology of Plant Associated Bacteria, pp. 25–34. Edited by H. P. Spaink, A. Kondorosi & P. J. J. Hooykaas. Dordrecht: Kluwer Academic.
  28. Hynes, M. F. & McGregor, N. F. ( 1990; ). Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol Microbiol 4, 567–574.[CrossRef]
    [Google Scholar]
  29. Hynes, M. F. & O'Connell, M. P. ( 1990; ). Host plant effect on competition among strains of Rhizobium leguminosarum. Can J Microbiol 36, 864–869.[CrossRef]
    [Google Scholar]
  30. Hynes, M. F., Simon, R. & Pühler, A. ( 1985; ). The development of plasmid-free strains of Agrobacterium tumefaciens by using incompatibility with a Rhizobium meliloti plasmid to eliminate pAtC58. Plasmid 13, 99–105.[CrossRef]
    [Google Scholar]
  31. Hynes, M. F., Brucksch, K. & Priefer, U. ( 1988; ). Melanin production encoded by a cryptic plasmid in a Rhizobium leguminosarum strain. Arch Microbiol 150, 326–332.[CrossRef]
    [Google Scholar]
  32. Hynes, M. F., Quandt, J., O'Connell, M. P. & Pühler, A. ( 1989; ). Direct selection for curing and deletion of Rhizobium plasmids using transposons carrying the Bacillus subtilis sacB gene. Gene 78, 111–120.[CrossRef]
    [Google Scholar]
  33. Irani, M. H. & Maitra, P. K. ( 1977; ). Properties of Escherichia coli mutants deficient in enzymes of glycolysis. J Bacteriol 132, 398–410.
    [Google Scholar]
  34. Jiménez-Zurdo, J. I., van Dillewijn, P., Soto, M. J., de Felipe, M. R., Olivares, J. & Toro, N. ( 1995; ). Characterization of a Rhizobium meliloti proline dehydrogenase mutant altered in nodulation efficiency and competitiveness on alfalfa roots. Mol Plant Microbe Interact 8, 492–498.[CrossRef]
    [Google Scholar]
  35. Jordan, D. C. ( 1984; ). Family III Rhizobiaceae. In Bergey's Manual of Systematic Bacteriology, pp. 234–244. Edited by N. R. Kreig & J. G. Holt. Baltimore: Williams & Wilkins.
  36. Kaneko, T., Nakamura, Y., Sato, S. & 21 other authors ( 2000; ). Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7, 331–338.[CrossRef]
    [Google Scholar]
  37. Kaneko, T., Nakamura, Y., Sato, S. & 14 other authors ( 2002; ). Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9, 189–197.[CrossRef]
    [Google Scholar]
  38. Lamb, J. W., Hombrecher, G. & Johnston, A. W. B. ( 1982; ). Plasmid-determined nodulation and nitrogen-fixation abilities in Rhizobium phaseoli. Mol Gen Genet 186, 449–452.[CrossRef]
    [Google Scholar]
  39. Martínez-Romero, E. & Rosenblueth, M. ( 1990; ). Increased bean (Phaseolus vulgaris) nodulation competitiveness of genetically modified Rhizobium strains. Appl Environ Microbiol 56, 2384–2388.
    [Google Scholar]
  40. Medrano-Soto, A., Moreno-Hagelsieb, G., Vinuesa, P., Christen, J. A. & Collado-Vides, J. ( 2004; ). Successful lateral transfer requires codon usage compatibility between foreign genes and recipient genomes. Mol Biol Evol 21, 1884–1894.[CrossRef]
    [Google Scholar]
  41. Miller, J. H. ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  42. Moënne-Loccoz, Y. & Weaver, R. W. ( 1995; ). Plasmids influence growth of rhizobia in the rhizosphere of clover. Soil Biol Biochem 27, 1001–1004.[CrossRef]
    [Google Scholar]
  43. Mulligan, J. T. & Long, S. R. ( 1985; ). Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD. Proc Natl Acad Sci U S A 82, 6609–6613.[CrossRef]
    [Google Scholar]
  44. New, P. B. & Kerr, A. ( 1971; ). A selective medium for Agrobacterium radiobacter biotype 2. J Appl Bacteriol 34, 233–236.[CrossRef]
    [Google Scholar]
  45. Noel, K. D., Sanchez, A., Fernandez, L., Leemans, J. & Cevallos, M. A. ( 1984; ). Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. J Bacteriol 158, 148–155.
    [Google Scholar]
  46. Oresnik, I. J., Pacarynuk, L. A., O'Brien, S. A. P., Yost, C. K. & Hynes, M. F. ( 1998; ). Plasmid-encoded catabolic loci in Rhizobium leguminosarum bv. trifolii. Evidence for a plant-inducible rhamnose utilisation locus involved in competition for nodulation. Mol Plant Microbe Interact 11, 1175–1185.[CrossRef]
    [Google Scholar]
  47. Oresnik, I. J., Liu, S. L., Yost, C. K. & Hynes, M. F. ( 2000; ). Megaplasmid pRme2011a of Sinorhizobium meliloti is not required for viability. J Bacteriol 182, 3582–3586.[CrossRef]
    [Google Scholar]
  48. Poole, P. S., Schofield, N. A., Reid, C. J., Drew, E. M. & Walshaw, D. L. ( 1994; ). Identification of chromosomal genes located downstream of dctD that affect the requirement for calcium and the lipopolysaccharide layer of Rhizobium leguminosarum. Microbiology 140, 2797–2809.[CrossRef]
    [Google Scholar]
  49. Priefer, U. B. ( 1989; ). Genes involved in lipopolysaccharide production and symbiosis are clustered on the chromosome of Rhizobium leguminosarum biovar viciae VF39. J Bacteriol 171, 6161–6168.
    [Google Scholar]
  50. Quandt, J. & Hynes, M. F. ( 1993; ). Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127, 15–21.[CrossRef]
    [Google Scholar]
  51. Reeve, W. G., Tiwari, R. P., Worsley, P. S., Dilworth, M. J., Glenn, A. R. & Howieson, J. G. ( 1999; ). Constructs for insertional mutagenesis, transcriptional signal localization and gene regulation studies in root nodule and other bacteria. Microbiology 145, 1307–1316.[CrossRef]
    [Google Scholar]
  52. Reiner, A. M. ( 1977; ). Xylitol and d-arabitol toxicities due to derepressed fructose, galactitol, and sorbitol phosphotransferases of Escherichia coli. J Bacteriol 132, 166–173.
    [Google Scholar]
  53. 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 Bacteriol 186, 8433–8442.[CrossRef]
    [Google Scholar]
  54. Ronson, C. W. & Primrose, S. B. ( 1979; ). Effect of glucose on polyol metabolism by Rhizobium trifolii. J Bacteriol 139, 1075–1078.
    [Google Scholar]
  55. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  56. Sangari, F. J., Aguero, J. & García-Lobo, J. M. ( 2000; ). The genes for erythritol catabolism are organized as an inducible operon in Brucella abortus. Microbiology 146, 487–495.
    [Google Scholar]
  57. Simon, R., Priefer, U. & Pühler, A. ( 1983; ). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1, 784–791.[CrossRef]
    [Google Scholar]
  58. Soedarjo, M. & Borthakur, D. ( 1998; ). Mimosine, a toxin produced by the tree-legume Leucaena provides a nodulation competition advantage to mimosine-degrading Rhizobium strains. Soil Biol Biochem 30, 1605–1613.[CrossRef]
    [Google Scholar]
  59. Sperry, J. F. & Robertson, D. C. ( 1975a; ). Erythritol catabolism by Brucella abortus. J Bacteriol 121, 619–630.
    [Google Scholar]
  60. Sperry, J. F. & Robertson, D. C. ( 1975b; ). Inhibition of growth by erythritol catabolism in Brucella abortus. J Bacteriol 124, 391–397.
    [Google Scholar]
  61. Streit, W. R., Schmitz, R. A., Perret, X., Staehelin, C., Deakin, W. J., Raasch, C., Liesegang, H. & Broughton, W. J. ( 2004; ). An evolutionary hot spot: the pNGR234b replicon of Rhizobium sp. strain NGR234. J Bacteriol 186, 535–542.[CrossRef]
    [Google Scholar]
  62. Verger, J. M., Grimont, F., Grimont, P. A. D. & Grayon, M. ( 1985; ). Brucella, a monospecific genus as shown by deoxyribonucleic acid hybridization. Int J Syst Bacteriol 35, 292–295.[CrossRef]
    [Google Scholar]
  63. Vincent, J. M. ( 1970; ). A Manual for the Practical Study of Root-nodule Bacteria (IBP handbook no. 15). Oxford: Blackwell Scientific Publications.
  64. Wang, Y. P., Birkenhead, K., Boesten, B., Manian, S. & O'Gara, F. ( 1989; ). Genetic analysis and regulation of the Rhizobium meliloti genes controlling C4-dicarboxylic acid transport. Gene 85, 135–144.[CrossRef]
    [Google Scholar]
  65. Wood, D. W., Setubal, J. C., Kaul, & 48 other authors ( 2001; ). The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294, 2317–2323.[CrossRef]
    [Google Scholar]
  66. Yost, C. K. ( 1998; ). Characterization of Rhizobium leguminosarum genes homologous to chemotaxis chemoreceptors. PhD thesis, University of Calgary.
  67. Yost, C. K., Rochepeau, P. & Hynes, M. F. ( 1998; ). Rhizobium leguminosarum contains a group of genes that appear to code for methyl-accepting chemotaxis proteins. Microbiology 144, 1945–1956.[CrossRef]
    [Google Scholar]
  68. Yost, C. K., Del Bel, K. L., Quandt, J. & Hynes, M. F. ( 2004; ). Rhizobium leguminosarum methyl-accepting chemotaxis protein genes are down-regulated in the pea nodule. Arch Microbiol 182, 505–513.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28938-0
Loading
/content/journal/micro/10.1099/mic.0.28938-0
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