1887

Abstract

The symbiosis island of sp. strain R7A is a 500 kb chromosomal genetic element that upon transfer converts nonsymbiotic mesorhizobia to symbionts able to nodulate and fix nitrogen with . Four genomic species of nonsymbiotic mesorhizobia have been isolated. All were auxotrophic for thiamin and biotin and three were auxotrophic for nicotinate, whereas derivatives of the strains containing the symbiosis island were prototrophic for all three vitamins. In this work, a 132 kb region of the island that converts the nonsymbionts to nicotinate and biotin prototrophy was characterized. The region contained orthologues of the and genes arranged in an operon with a novel gene, , a operon, the nitrogen-fixation regulatory gene , and a homologue of the pantothenate biosynthesis gene . The gene product was similar toβ-ketoacyl-acyl carrier protein synthase III (FabH). ::Tn mutants grew poorly in the absence of biotin and the gene complemented an mutant, suggesting that its product is involved in the synthesis of pimeloyl-CoA. The operon was not required for symbiosis, as only mutants in the gene were impaired in symbiosis, and a ::Tn mutant was not impaired in rhizosphere colonization. The rationale for the vitamin biosynthetic loci being located on an acquired genetic element that is absent from nonsymbiotic mesorhizobia remains to be determined.

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2001-05-01
2024-04-18
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References

  1. Altschul S. F., Madden T. L., Schaffer 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 Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  2. Beringer J. E. 1974; R factor transfer in Rhizobium leguminosarum . J Gen Microbiol 84:188–198 [CrossRef]
    [Google Scholar]
  3. Besemer J., Borodovsky M. 1999; Heuristic approach to deriving models for gene finding. Nucleic Acids Res 27:3911–3920 [CrossRef]
    [Google Scholar]
  4. Bower S., Perkins J. B., Yocum R. R., Howitt C. L., Rahaim P., Pero J. 1996; Cloning, sequencing, and characterization of the Bacillus subtilis biotin biosynthetic operon. J Bacteriol 178:4122–4130
    [Google Scholar]
  5. Boyer H. W., Roulland-Dussoix D. 1969; A complementation analysis of the restriction and modification of DNA in Escherichia coli . J Mol Biol 41:459 [CrossRef]
    [Google Scholar]
  6. de Bruijn F. J. Lupski J. R. 1984; The use of transposon Tn 5 mutagenesis in the rapid generation of correlated physical and genetic maps of DNA segments cloned into multicopy plasmids – a review. Gene 27:131–149 [CrossRef]
    [Google Scholar]
  7. Cleary P. P., Campbell A. 1972; Deletion and complementation analysis of the biotin gene cluster of Escherichia coli . J Bacteriol 112:830–839
    [Google Scholar]
  8. Demoll E. others 1996; Biosynthesis of biotin and lipoic acid. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp 704–709 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  9. Ditta G. S., Stanfield D., Corbin D., Helinski D. R. 1980; Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti . Proc Natl Acad Sci USA 77:7347–7351 [CrossRef]
    [Google Scholar]
  10. Dreyfus B. L., Elmerich C., Dommergues Y. R. 1983; Free living Rhizobium strain able to grow on N2 as the sole nitrogen source. Appl Environ Microbiol 45:711–713
    [Google Scholar]
  11. Eisenberg M. A. others 1987; Biosynthesis of biotin and lipoic acid. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp 544–550 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  12. 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 Bacteriol 167:66–72
    [Google Scholar]
  13. Fischer H. M. 1994; Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58:352–386
    [Google Scholar]
  14. Friedman A. M., Long S. R., Brown S. E., Buikema W. J., Ausubel F. M. 1982; Construction of a broad host range cosmid cloning vector and its use in genetic analysis of Rhizobium mutants. Gene 18:289–296 [CrossRef]
    [Google Scholar]
  15. Gloeckler R., Ohsawa I., Speck D. 7 other authors 1990; Cloning and characterization of the Bacillus sphaericus genes controlling the bioconversion of pimelate into dethiobiotin. Gene 87:63–70 [CrossRef]
    [Google Scholar]
  16. Graham P. H. 1963; Vitamin requirements of root nodule bacteria. J Gen Microbiol 30:245–248 [CrossRef]
    [Google Scholar]
  17. Hatfield D., Hofnung M., Schwartz M. 1969; Genetic analysis of the maltose A region in Escherichia coli . J Bacteriol 98:559–567
    [Google Scholar]
  18. Heath R. J., Rock C. O. 1996; Roles of the FabA and FabZ beta-hydroxyacyl-acyl carrier protein dehydratases in Escherichia coli fatty acid biosynthesis. J Biol Chem 271:27795–27801 [CrossRef]
    [Google Scholar]
  19. Hirsch P. R. 1979; Plasmid-determined bacteriocin production by Rhizobium leguminosarum . J Gen Microbiol 113:219–228 [CrossRef]
    [Google Scholar]
  20. Ifuku O., Miyaoka H., Koga N., Kishimoto J., Haze S., Wachi Y., Kajiwara M. 1994; Origin of carbon atoms of biotin: C-13-NMR studies on biotin biosynthesis in Escherichia coli . Eur J Biochem 220:585–591 [CrossRef]
    [Google Scholar]
  21. Ifuku O., Koga N., Haze S., Kishimoto J., Arai T., Wachi Y. 1995; Molecular analysis of growth inhibition caused by overexpression of the biotin operon in Escherichia coli . Biosci Biotechnol Biochem 59:184–189 [CrossRef]
    [Google Scholar]
  22. Labes M., Puhler A., Simon R. 1990; A new family of RSF1010-derived expression and lac -fusion broad-host-range vectors for Gram-negative bacteria. Gene 89:37–46 [CrossRef]
    [Google Scholar]
  23. Levy-Schil S., Debussche L., Rigault S. 7 other authors 1993; Biotin biosynthetic pathway in recombinant strains of Escherichia coli overexpressing bio genes: evidence for a limiting step upstream from KAPA. Appl Microbiol Biotechnol 38:755–762 [CrossRef]
    [Google Scholar]
  24. Liu Y. N., Tang J. L., Clarke B. R., Dow J. M., Daniels M. J. 1990; A multipurpose broad host range cloning vector and its use to characterize an extracellular protease gene of Xanthomonas campestris pathovar campestris . Mol Gen Genet 220:433–440 [CrossRef]
    [Google Scholar]
  25. Miranda-Rios J., Morera C., Taboada H., Davalos A., Encarnacion S., Mora J., Soberon M. 1997; Expression of thiamin biosynthetic genes ( thiCOGE ) and production of symbiotic terminal oxidase cbb3 in Rhizobium etli . J Bacteriol 179:6887–6893
    [Google Scholar]
  26. Penfound T., Foster J. W. others 1996; Biosynthesis and recycling of NAD. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp 721–730 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  27. Ronson C. W., Nixon B. T., Albright L. M., Ausubel F. M. 1987; Rhizobium meliloti ntrA ( rpoN ) gene is required for diverse metabolic functions. J Bacteriol 169:2424–2431
    [Google Scholar]
  28. Ruvkun G. B., Ausubel F. M. 1981; A general method for site-directed mutagenesis in prokaryotes. Nature 289:85–88 [CrossRef]
    [Google Scholar]
  29. Sakurai N., Imai Y., Masuda M., Komatsubara S., Tosa T. 1993; Molecular breeding of a biotin-hyperproducing Serratia marcescens strain. Appl Environ Microbiol 10:3225–3232
    [Google Scholar]
  30. 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]
  31. Sanyal I., Lee S. L., Flint D. H. 1994; Biosynthesis of pimeloyl-CoA, a biotin precursor in Escherichia coli , follows a modified fatty acid synthesis pathway: 13C-labeling studies. J Am Chem Soc 116:2637–2638 [CrossRef]
    [Google Scholar]
  32. Streit W. R., Phillips D. A. 1996; Recombinant Rhizobium meliloti strains with extra biotin synthesis capability. Appl Environ Microbiol 62:3333–3338
    [Google Scholar]
  33. Streit W. R., Joseph C. M., Philips D. A. 1996; Biotin and other water-soluble vitamins are key growth factors for alfalfa root colonisation by Rhizobium meliloti 1021. Mol Plant–Microbe Interact 9:330–338 [CrossRef]
    [Google Scholar]
  34. Sullivan J. T., Ronson C. W. 1998; Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95:5145–5149 [CrossRef]
    [Google Scholar]
  35. Sullivan J. T., Patrick H. N., Lowther W. L., Scott D. B., Ronson C. W. 1995; Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92:8985–8989 [CrossRef]
    [Google Scholar]
  36. Sullivan J. T., Eardly B. D., Ronson C. W, van Berkum P. 1996; Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus . Appl Environ Microbiol 62:2818–2825
    [Google Scholar]
  37. Tsay J. T., Oh W., Larson T. J., Jackowski S., Rock C. O. 1992; Isolation and characterization of the beta-ketoacyl-acyl carrier protein synthase-III gene ( fabH ) from Escherichia coli K-12. J Biol Chem 267:6807–6814
    [Google Scholar]
  38. Vincent J. M. 1970 A Manual for the Practical Study of Root Nodule Bacteria Oxford: Blackwell Scientific Publications;
    [Google Scholar]
  39. Wilson J. B., Wilson P. W. 1942; Biotin as a growth factor for rhizobia. J Bacteriol 43:329–341
    [Google Scholar]
  40. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–109 [CrossRef]
    [Google Scholar]
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