1887

Abstract

Biotin has a profound effect on the metabolism of rhizobia. It is reported here that the activities of the biotin-dependent enzymes acetyl-coenzyme A carboxylase (ACC; EC 6.4.1.2) and propionyl-coenzyme A carboxylase (PCC; EC 6.4.1.3) are present in all species of the five genera comprising the which were examined. Evidence is presented that the ACC and PCC activities detectable in extracts are catalysed by a single acyl-coenzyme A carboxylase. The enzyme from strain 12-53 was purified 478-fold and displayed its highest activity with propionyl-CoA as substrate, with apparent and values of 0·064 mM and 2885 nmol min (mg protein), respectively. The enzyme carboxylated acetyl-CoA and butyryl-CoA with apparent values of 0·392 and 0·144 mM, respectively, and values of 423 and 268 nmol min (mg protein), respectively. K, or Cs markedly activated the enzyme, which was essentially inactive in their absence. Electrophoretic analysis indicated that the acyl-CoA carboxylase was composed of a 74 kDa biotin-containing subunit and a 45 kDa biotin-free subunit, and gel chromatography indicated a total molecular mass of 620 000 Da. The strong kinetic preference of the enzyme for propionyl-CoA is consistent with its participation in an anaplerotic pathway utilizing this substrate.

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2004-02-01
2020-03-31
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References

  1. Alberts A. W., Vagelos P. R. 1968; Acetyl CoA carboxylase. I. Requirement for two protein fractions. Proc Natl Acad Sci U S A59:561–568[CrossRef]
    [Google Scholar]
  2. Brom S. A., García-de los Santos L., Cervantes, Palacios R., Romero D. 2000; In Rhizobium etli symbiotic plasmid transfer, nodulation competitivity and cellular growth require interaction among different replicons. Plasmid44:34–43[CrossRef]
    [Google Scholar]
  3. Charles T. C., Aneja P. 1999; Methylmalonyl-CoA mutase encoding gene of Sinorhizobium meliloti . Gene226:121–127[CrossRef]
    [Google Scholar]
  4. Cronan J. E. Jr, Waldrop G. L. 2002; Multi-subunit acetyl-CoA carboxylases. Prog Lipid Res41:407–435[CrossRef]
    [Google Scholar]
  5. DeHertogh A. A., Mayeux P. A., Evans H. J. 1964; The relationship of cobalt requirement to propionate metabolism in Rhizobium . J Biol Chem239:2446–2453
    [Google Scholar]
  6. Diacovich L. S., Gramajo H, Peirú. S., Kurth D., Rodríguez E., Podestá F., Kohosla C.. 2002; Kinetic and structural analysis of a new group of acyl-CoA carboxylases found in Streptomyces coelicolor A3(2). J Biol Chem277:31228–31236[CrossRef]
    [Google Scholar]
  7. Dreyfus B., Dommergues Y. R. 1981; Nitrogen-fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata . FEMS Microbiol Lett10:313–317[CrossRef]
    [Google Scholar]
  8. Dunn M. F., Mora Y., Mora J, Encarnación S., Araíza G., Vargas M. C., Dávalos A., Peralta H.. 1996; Pyruvate carboxylase from Rhizobium etli : mutant characterization, nucleotide sequence, and physiological role. J Bacteriol178:5960–5970
    [Google Scholar]
  9. Dunn M. F., Mora J, Araíza G., Cevallos M. A.. 1997; Regulation of pyruvate carboxylase in Rhizobium etli . FEMS Microbiol Lett157:301–306[CrossRef]
    [Google Scholar]
  10. 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]
    [Google Scholar]
  11. Dunn M. F., Mora J, Araíza G., Encarnación S., Vargas M. C.. 2002; Effect of aniA (carbon flux regulator) and phaC (poly- β -hydroxybutyrate synthase) mutations on pyruvate metabolism in Rhizobium etli . J Bacteriol184:2296–2299[CrossRef]
    [Google Scholar]
  12. Dunn M. F., Mora J, Araíza G., Encarnación S., Finan T.. 2002a; Characteristics and metabolic roles of biotin-dependent carboxylases in rhizobia. In Nitrogen Fixation: Global Perspectives pp158–162 Edited by Finan T. M., O’Brian M., Layzell D., Vessey K., Newton W.. Oxford: CABI;
    [Google Scholar]
  13. Encarnación S., Dunn M., Willms K., Mora J. 1995; Fermentative and aerobic metabolism in Rhizobium etli . J Bacteriol177:3058–3066
    [Google Scholar]
  14. Encarnación S., Guzmán Y., Dunn M. F., Hernández M., Vargas M. C., Mora J. 2003; Proteome analysis of aerobic and fermentative metabolism in Rhizobium etli CE3. Proteomics3:1077–1085[CrossRef]
    [Google Scholar]
  15. Fall R. R. 1976; Stabilization of an acetyl-coenzyme A carboxylase complex from Pseudomonas citronellolis . Biochim Biophys Acta450:475–480[CrossRef]
    [Google Scholar]
  16. Guchait R. B., Polakis S. E., Dimroth P., Stoll E., Moss J., Lane M. D. 1974; Acetyl coenzyme A carboxylase system of Escherichia coli . Purification and properties of the biotin carboxylase, carboxyltransferase, and carboxyl carrier protein components. J Biol Chem249:6633–6645
    [Google Scholar]
  17. Haase F. C., Hendrikson K. P., Treble D. H., Allen S. H. G. 1982; The subunit structure and function of the propionyl-coenzyme carboxylase of Mycobacterium smegmatis . J Biol Chem257:11994–11999
    [Google Scholar]
  18. Hector M. L., Fall R. R. 1976; Multiple acyl-coenzyme A carboxylases in Pseudomonas citronellolis . Biochemistry15:3465–3472[CrossRef]
    [Google Scholar]
  19. Heinz E. B., Streit W. R. 2003; Biotin limitation in Sinorhizobium meliloti strain 1021 alters transcription and translation. Appl Environ Microbiol69:1206–1213[CrossRef]
    [Google Scholar]
  20. Hopwood D. A., Sherman D. H. 1990; Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annu Rev Genet24:37–66[CrossRef]
    [Google Scholar]
  21. Jarvis B. D. W., Chen W. X., Nour S. M., Gillis M, van Berkum P., Fernández M. P., Cleyet-Marel J.-C.. 1997; Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum , and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol47:895–898[CrossRef]
    [Google Scholar]
  22. Johnston A. W. B., Beringer J. E. 1975; Identification of the Rhizobium strains in pea root nodules using genetic markers. J Gen Microbiol87:343–350[CrossRef]
    [Google Scholar]
  23. Kaneko T., Nakamura Y., Sato S.. 13 other authors 2002; Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res9:189–197[CrossRef]
    [Google Scholar]
  24. Keyser H. H., Griffin R. F. 1987; Beltsville Rhizobium Culture Collection Catalog Beltsville, MD: US Department of Agriculture;
    [Google Scholar]
  25. Kimura Y., Kojyo T., Kimura I., Sato M. 1998; Propionyl-CoA carboxylase of Myxococcus xanthus : catalytic properties and function in developing cells. Arch Microbiol170:179–184[CrossRef]
    [Google Scholar]
  26. Lowe R. H., Evans H. J. 1962; Carbon dioxide requirement for growth of legume nodule bacteria. Soil Sci94:351–356[CrossRef]
    [Google Scholar]
  27. Martínez E., Palacios R., Sánchez F. 1987; Nitrogen-fixing nodules induced by Agrobacterium tumefaciens harboring Rhizobium phaseoli plasmids. J Bacteriol169:2828–2834
    [Google Scholar]
  28. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. 1982; Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn 5 mutagenesis. J Bacteriol149:114–122
    [Google Scholar]
  29. Menendez C., Bauer Z., Huber H., Gad’on N., Stetter K.-O., Fuchs G. 1999; Presence of acetyl coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J Bacteriol181:1088–1098
    [Google Scholar]
  30. Meyer H., Meyer F. 1978; Acyl-coenzyme A carboxylase from the free-living nematode Turbatrix aceti . 2. Its catalytic properties and activation by monovalent cations. Biochemistry17:1828–1833[CrossRef]
    [Google Scholar]
  31. Miyamoto E., Watanabe F., Charles T. C., Yamaji R., Inui H., Nakano Y. 2003; Purification and characterization of homodimeric methylmalonyl-CoA mutase from Sinorhizobium meliloti . Arch Microbiol180:151–154[CrossRef]
    [Google Scholar]
  32. Mohamed M. E. 2000; Biochemical and molecular characterization of phenylacetate-coenzyme A ligase, an enzyme catalyzing the first step in aerobic metabolism of phenylacetic acid in Azoarcus evansii . J Bacteriol182:286–294[CrossRef]
    [Google Scholar]
  33. Noel K. D., Cevallos M. A, Sánchez A., Fernández L., Leemans J.. 1984; Rhizobium phaseoli symbiotic mutants with transposon Tn 5 insertions. J Bacteriol158:148–155
    [Google Scholar]
  34. Rainwater D. L., Kolattukudy P. E. 1982; Isolation and characterization of acyl-coenzyme A carboxylases from Mycobacterium tuberculosis and Mycobacterium bovis , which produce multiple methyl-branched mycosteric acids. J Bacteriol151:905–911
    [Google Scholar]
  35. Rodríguez E., Banchio C., Diacovich L., Bibb M. J., Gramajo H. 2001; Role of essential acyl coenzyme A carboxylase in the primary and secondary metabolism of Streptomyces coelicolor A3(2). Appl Environ Microbiol67:4166–4176[CrossRef]
    [Google Scholar]
  36. Scholla M. H., Elkan G. H. 1984; Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybeans. Int J Syst Bacteriol34:484–486[CrossRef]
    [Google Scholar]
  37. Streit W. R., Joseph C. M., Phillips D. A. 1996; Biotin and other water-soluble vitamins are key growth factors for alfalfa root colonization by Rhizobium meliloti 1021. Mol Plant–Microbe Interact9:330–338[CrossRef]
    [Google Scholar]
  38. Watson R. J., Heys R., Martin T., Sevard M. 2001; Sinorhizobium meliloti cells require biotin and either cobalt or methionine for growth. Appl Environ Microbiol67:3767–3770[CrossRef]
    [Google Scholar]
  39. West P. M., Wilson P. W. 1940; Biotin as a growth stimulant for the root nodule bacteria. Enzymology8:152–162
    [Google Scholar]
  40. Zubay G. 1988; Biochemistry New York: Macmillan;
    [Google Scholar]
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