1887

Microbiology Society logo

Volume 150, Issue 2

Biochemical characterization of a monovalent cation-stimulated acyl-coenzyme A carboxylase with a high substrate specificity constant for propionyl-coenzyme A Free

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.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): ACC, acetyl-CoA carboxylase , PCC, propionyl-CoA carboxylase and PYC, pyruvate carboxylase
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26779-0
2004-02-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/2/mic1500399.html?itemId=/content/journal/micro/10.1099/mic.0.26779-0&mimeType=html&fmt=ahah

References

  1. Alberts A. W., Vagelos P. R. 1968; Acetyl CoA carboxylase. I. Requirement for two protein fractions. Proc Natl Acad Sci U S A 59:561–568 [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. Plasmid 44:34–43 [CrossRef]
     [Google Scholar]
  3. Charles T. C., Aneja P. 1999; Methylmalonyl-CoA mutase encoding gene of Sinorhizobium meliloti . Gene 226:121–127 [CrossRef]
     [Google Scholar]
  4. Cronan J. E. Jr, Waldrop G. L. 2002; Multi-subunit acetyl-CoA carboxylases. Prog Lipid Res 41:407–435 [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 Chem 239:2446–2453
     [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 Chem 277:31228–31236 [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 Lett 10:313–317 [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 Bacteriol 178:5960–5970
     [Google Scholar]
  9. Dunn M. F., Mora J, Araíza G., Cevallos M. A. 1997; Regulation of pyruvate carboxylase in Rhizobium etli . FEMS Microbiol Lett 157:301–306 [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 Microbiol 176:355–363 [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 Bacteriol 184:2296–2299 [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 pp 158–162 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 Bacteriol 177:3058–3066
     [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. Proteomics 3:1077–1085 [CrossRef]
     [Google Scholar]
  15. Fall R. R. 1976; Stabilization of an acetyl-coenzyme A carboxylase complex from Pseudomonas citronellolis . Biochim Biophys Acta 450:475–480 [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 Chem 249:6633–6645
     [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 Chem 257:11994–11999
     [Google Scholar]
  18. Hector M. L., Fall R. R. 1976; Multiple acyl-coenzyme A carboxylases in Pseudomonas citronellolis . Biochemistry 15:3465–3472 [CrossRef]
     [Google Scholar]
  19. Heinz E. B., Streit W. R. 2003; Biotin limitation in Sinorhizobium meliloti strain 1021 alters transcription and translation. Appl Environ Microbiol 69:1206–1213 [CrossRef]
     [Google Scholar]
  20. Hopwood D. A., Sherman D. H. 1990; Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annu Rev Genet 24:37–66 [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 Bacteriol 47:895–898 [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 Microbiol 87:343–350 [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 Res 9:189–197 [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 Microbiol 170:179–184 [CrossRef]
     [Google Scholar]
  26. Lowe R. H., Evans H. J. 1962; Carbon dioxide requirement for growth of legume nodule bacteria. Soil Sci 94:351–356 [CrossRef]
     [Google Scholar]
  27. Martínez E., Palacios R., Sánchez F. 1987; Nitrogen-fixing nodules induced by Agrobacterium tumefaciens harboring Rhizobium phaseoli plasmids. J Bacteriol 169:2828–2834
     [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 Bacteriol 149:114–122
     [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 Bacteriol 181:1088–1098
     [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. Biochemistry 17:1828–1833 [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 Microbiol 180:151–154 [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 Bacteriol 182:286–294 [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 Bacteriol 158:148–155
     [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 Bacteriol 151:905–911
     [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 Microbiol 67:4166–4176 [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 Bacteriol 34:484–486 [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 Interact 9:330–338 [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 Microbiol 67:3767–3770 [CrossRef]
     [Google Scholar]
  39. West P. M., Wilson P. W. 1940; Biotin as a growth stimulant for the root nodule bacteria. Enzymology 8:152–162
     [Google Scholar]
  40. Zubay G. 1988 Biochemistry New York: Macmillan;
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26779-0
Loading
Biochemical characterization of a Rhizobium etli monovalent cation-stimulated acyl-coenzyme A carboxylase with a high substrate specificity constant for propionyl-coenzyme A
Microbiology 150, 399 (2004); https://doi.org/10.1099/mic.0.26779-0
/content/journal/micro/10.1099/mic.0.26779-0
/content/journal/micro/10.1099/mic.0.26779-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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