1887

Microbiology Society logo

Volume 144, Issue 9

Glutamine biosynthesis and the utilization of succinate and glutamine by Rhizobium etli and Sinorhizobium meliloti Free

Abstract

1021 and CE3 turn over nitrogen and carbon from glutamine to ammonium and CO, respectively. Some of the ammonium released is assimilated back into glutamine, indicating that a glutamine cycle similar to that in operates in In addition, a previously unrecognized metabolic pathway in was discovered - namely, conversion of glutamine-carbon to γ-hydroxybutyric acid and β-hydroxybutyric acid. Additionally, some of the 2-oxoglutarate derived from glutamine catabolism in is converted to succinate in glutamine-containing medium. Both 1021 and CE3 oxidize succinate preferentially over glutamine when provided with both carbon sources. In contrast to 1021 and CE3, an double mutant that lacks both glutamine synthetase (GS) I and II preferentially oxidizes glutamine over succinate when supplied with both substrates. GSII activity is induced in wild-type 1021 and CE3 grown in succinate-glutamine medium, and this enzyme participates in the cycling of glutamine-carbon and -nitrogen. On the other hand, GSII activity is repressed in both micro-organisms when glutamine is the only carbon source. These findings show that, in medium containing both glutamine and succinate, glutamine synthesis helps drive the utilization of succinate. When glutamine is in excess as an energy-providing substrate its synthesis is restricted, allowing for more effective utilization of glutamine as an energy source.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): carbon metabolism , glutamine cycle , nitrogen metabolism , Rhizobium etli and Sinorhizobium meliloti
© Society for General Microbiology 1998
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-144-9-2629
1998-09-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/144/9/mic-144-9-2629.html?itemId=/content/journal/micro/10.1099/00221287-144-9-2629&mimeType=html&fmt=ahah

References

  1. Bender R.A., Janssen K.A., Resnick A.D., Blumenberg M., Poor F., Magasanik B. 1977; Biochemical parameters of glutamine synthetase from Klebsiella aerogenes. . J Bacterial 129:1001–1009
     [Google Scholar]
  2. Bravo A., Mora J. 1988; Ammonium assimilation in Rhizo- bium phaseoli by the glutamine synthetase-glutamate synthase pathway.. J Bacterial 170:980–984
     [Google Scholar]
  3. Bravo A., Becerril B., Mora J. 1988; Introduction of the Escherichia cali gdhA gene into Rhizabium phaseali: effect on nitrogen fixation.. J Bacterial 170:985–988
     [Google Scholar]
  4. deBruijn F.J., Rossbach S., Schneider M., Ratet P., Messmer S., Szeto W.W., Ausubel F.M., Schell J. 1989; Rhizabium melilati 1021 has three differentially regulated loci involved in glutamine biosynthesis, none of which is essential for symbiotic nitrogen fixation.. Bacterial 171:1673–1682
     [Google Scholar]
  5. Calderón J., Mora J. 1985; Glutamine cycling in Neuraspara crassa. . J Gen Micrabial 131:3237–3242
     [Google Scholar]
  6. Calderón J., Mora J. 1989; Glutamine assimilation pathways in Neuraspara crassa growing on glutamine as sole nitrogen and carbon source.. J Gen Microbial 135:2699–2707
     [Google Scholar]
  7. Calderón J., Morett E., Mora J. 1985; Ω-Amidase pathway in the degradation of glutamine in Neuraspara crassa. . J Bacterial 161:807–809
     [Google Scholar]
  8. Calderón J., Cooper A.J.L., Gelbard A.S., Mora J. 1989; 13N isotope studies of glutamine assimilation pathways in Neuraspara crassa. . J Bacterial 171:1772–1774
     [Google Scholar]
  9. Carlson T.A., Martin G.B., Chelm B.K. 1987; Differential transcription of the two glutamine synthetase genes of Brady- rhizabium japonicum. . J Bacterial 169:5861–5866
     [Google Scholar]
  10. Chiurazzi M., Meza R., Lara M., Lahm A., Defez R., laccarino M., Espín G. 1992; The Rhizabium leguminasarum biovar phaseali glnT gene, encoding glutamine synthetase III.. Gene 119:1–8
     [Google Scholar]
  11. Darrow R.A., Knotts R.R. 1977; Two forms of glutamine synthetase in free-living root-nodule bacteria.. Biachem Biophys Res Commun 78:554–559
     [Google Scholar]
  12. Durán S., Calderón J. 1995; Role of the glutamine transaminase Ω-amidase pathway and glutaminase in glutamine degradation in Rhizobium etli. . Microbiology 141:589–595
     [Google Scholar]
  13. Durán S., Du Pont G., Huerta-Zepeda J., Calderdn J. 1995; The role of glutaminase in Rhizobium etli: studies with a new mutant.. Microbiology 141:2883–2889
     [Google Scholar]
  14. Durán S., Sánchez-Linares L, Huetta-Saquero A., Du Pont G., Huerta-Zepeda A., Calderón J. 1996; Identification of two glutaminases in . Rhizobium etli. Biochem Genet 34:453–65
     [Google Scholar]
  15. Encarnacion S., Dunn M., Willms K., Mora J. 1995; Fermentative and aerobic metabolism in Rhizobium etli. . J Bacteriol 177:3058–3066
     [Google Scholar]
  16. Espín G., Palacios R., Mora J. 1979; Glutamine metabolism in nitrogen-starved conidia of Neurospora crassa. . J Gen Microbiol 115:59–68
     [Google Scholar]
  17. Espín G., Moreno S., Wild M., Meza R., laccarino M. 1990; A previously unrecognized glutamine synthetase expressed in Klebsiella pneumoniae from the glnT locus of Rhizobium leguminosarum. . Mol Gen Genet 223:513–516
     [Google Scholar]
  18. Hardman J.K., Stadtman T.C. 1963; Metabolism of a"-amino acids. IV. γ-Aminobutyrate fermentation by cell-free extracts of Clostridium aminobutyricum. . J Biol Chem 238:2088–2093
     [Google Scholar]
  19. Helling R.B. 1994; Why does Escherichia coli have two primary pathways for synthesis of glutamate?. J Bacteriol 176:4664–4668
     [Google Scholar]
  20. Hernández G., Mora J. 1986; Glutamine synthesis regulates sucrose catabolism in Neurospora crassa. . J Gen Microbiol 132:3315–3323
     [Google Scholar]
  21. Hernández G., Mora Y., Mora J. 1986; Regulation of glutamine synthesis by glycine and serine in Neurospora crassa. . J Bacteriol 165:133–138
     [Google Scholar]
  22. Larsson Ch., Nilsson A., Blomberg A., Gustafsson L. 1997; Glycolytic flux is conditionally correlated with ATP concentration in Saccharomyces cerevisiae: a chemostat study under carbon- or nitrogen-limiting conditions.. J Bacteriol 179:7243–7250
     [Google Scholar]
  23. Law J.H., Slepecky R.A. 1961; Assay of poly-βhydroxy- butyric acid.. Bacteriol 82:33–36
     [Google Scholar]
  24. Lomnitz A., CalderÖn J. 1987; Functional analysis of ammonium assimilation enzymes in Neurospora crassa. . J Gen Microbiol 133:2333–2340
     [Google Scholar]
  25. Metzer E., Halpern Y.S. 1990; In vivo cloning and characterization of the ga^CTDP gene cluster of Escherichia coli K-12. . J Bacteriol 172:3250–3256
     [Google Scholar]
  26. Miller R.W., McRae D.G., Joy K. 1991; Glutamate and γ- aminobutyrate metabolism in isolated Rhizobium meliloti bac- teroids.. Mol Plant-Microbe Interact 4:37–45
     [Google Scholar]
  27. Mora J. 1990; Glutamine metabolism and cycling in Neurospora crassa. . Microbiol Rev 54:293–304
     [Google Scholar]
  28. Mora J., Salceda R. 1972; Regulation of arginase activity by intermediates of the arginine biosynthetic pathway in Neurospora crassa. . J Bacteriol 110:870–877
     [Google Scholar]
  29. Osburne M.S., Signe E.R. 1980; Ammonium assimilation in Rhizobium meliloti. . J Bacteriol 143:1234–1240
     [Google Scholar]
  30. Ronzio R.A., Meister A. 1968; Phosphorylation of methionine sulfoximine by glutamine synthetase.. Proc Natl Acad Sci USA 59:164–170
     [Google Scholar]
  31. Shatters R.G., Liu Y., Kahn M.L. 1993; Isolation and characterization of a novel glutamine synthetase from Rhizobium meliloti. . J Bacteriol 268:469–75
     [Google Scholar]
  32. Steinbüchel A. 1991; Physiology and molecular genetics of poly(β-hydroxy-alkanoic acid) synthesis in Alcaligenes eutrophus. . Mol Microbiol 5:535–542
     [Google Scholar]
  33. Stucki J.W. 1980; The optimal efficiency and the economic degrees of coupling of oxidative phosphorylation.. Eur J Biochem 109:269–283
     [Google Scholar]
  34. Tempest D.W. 1978; The biochemical significance of microbial growth yields: a reassessment.. Trends Biochem Sci 3:180–184
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-144-9-2629
Loading
Glutamine biosynthesis and the utilization of succinate and glutamine by Rhizobium etli and Sinorhizobium meliloti
Microbiology 144, 2629 (1998); https://doi.org/10.1099/00221287-144-9-2629
/content/journal/micro/10.1099/00221287-144-9-2629
/content/journal/micro/10.1099/00221287-144-9-2629
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