Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Jun;179(11):3706–3710. doi: 10.1128/jb.179.11.3706-3710.1997

Transcriptional regulation of delta-aminolevulinic acid dehydratase synthesis by oxygen in Bradyrhizobium japonicum and evidence for developmental control of the hemB gene.

S Chauhan 1, M R O'Brian 1
PMCID: PMC179168  PMID: 9171420

Abstract

An increased demand for cytochromes is associated with symbiotic development and microaerobic metabolism in the bacterium Bradyrhizobium japonicum, and evidence suggests that hemB, rather than hemA, is the first essential bacterial heme synthesis gene in symbiosis with soybean. Steady-state levels of mRNA and protein encoded by hemB were strongly and rapidly induced by O2 deprivation as determined by RNase protection and immunoblot analyses, but hemH message was not induced. Oxygen limitation resulted in a greater-than-10-fold increase in the rate of hemB mRNA synthesis as determined by transcriptional runoff experiments, whereas hemH transcription was unaffected by the O2 status. Thus, hemB is a regulated gene in B. japonicum and is transcriptionally controlled by O2. Unlike the expression in parent strain I110, hemB expression was not affected by O2 in the fixJ strain 7360, and O2-limited cultures of the mutant contained quantities of hemB mRNA and protein that were comparable to uninduced levels found in aerobic cells. In addition, spectroscopic analysis of cell extracts showed that increases in b- and c-type cytochromes and the disappearance of cytochrome aa3 in response to microaerobic growth in wild-type cells were not observed in the fixJ mutant. FixJ is a key transcriptional regulator that mediates O2-dependent differentiation in rhizobia, and therefore hemB expression is under developmental control. Furthermore, the data suggest a global control of cytochrome expression and heme biosynthesis in response to the cellular O2 status.

Full Text

The Full Text of this article is available as a PDF (314.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anthamatten D., Hennecke H. The regulatory status of the fixL- and fixJ-like genes in Bradyrhizobium japonicum may be different from that in Rhizobium meliloti. Mol Gen Genet. 1991 Jan;225(1):38–48. doi: 10.1007/BF00282640. [DOI] [PubMed] [Google Scholar]
  2. Appleby C. A. Electron transport systems of Rhizobium japonicum. I. Haemoprotein P-450, other CO-reactive pigments, cytochromes and oxidases in bacteroids from N2-fixing root nodules. Biochim Biophys Acta. 1969 Jan 14;172(1):71–87. doi: 10.1016/0005-2728(69)90093-0. [DOI] [PubMed] [Google Scholar]
  3. Appleby C. A. Electron transport systems of Rhizobium japonicum. II. Rhizobium haemoglobin, cytochromes and oxidases in free-living (cultured) cells. Biochim Biophys Acta. 1969 Jan 14;172(1):88–105. doi: 10.1016/0005-2728(69)90094-2. [DOI] [PubMed] [Google Scholar]
  4. Avissar Y. J., Nadler K. D. Stimulation of tetrapyrrole formation in Rhizobium japonicum by restricted aeration. J Bacteriol. 1978 Sep;135(3):782–789. doi: 10.1128/jb.135.3.782-789.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Batut J., Boistard P. Oxygen control in Rhizobium. Antonie Van Leeuwenhoek. 1994;66(1-3):129–150. doi: 10.1007/BF00871636. [DOI] [PubMed] [Google Scholar]
  6. Chauhan S., O'Brian M. R. A mutant Bradyrhizobium japonicum delta-aminolevulinic acid dehydratase with an altered metal requirement functions in situ for tetrapyrrole synthesis in soybean root nodules. J Biol Chem. 1995 Aug 25;270(34):19823–19827. doi: 10.1074/jbc.270.34.19823. [DOI] [PubMed] [Google Scholar]
  7. Chauhan S., O'Brian M. R. Bradyrhizobium japonicum delta-aminolevulinic acid dehydratase is essential for symbiosis with soybean and contains a novel metal-binding domain. J Bacteriol. 1993 Nov;175(22):7222–7227. doi: 10.1128/jb.175.22.7222-7227.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. David M., Daveran M. L., Batut J., Dedieu A., Domergue O., Ghai J., Hertig C., Boistard P., Kahn D. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell. 1988 Aug 26;54(5):671–683. doi: 10.1016/s0092-8674(88)80012-6. [DOI] [PubMed] [Google Scholar]
  9. Fischer H. M. Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev. 1994 Sep;58(3):352–386. doi: 10.1128/mr.58.3.352-386.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fisher R. F., Long S. R. Rhizobium--plant signal exchange. Nature. 1992 Jun 25;357(6380):655–660. doi: 10.1038/357655a0. [DOI] [PubMed] [Google Scholar]
  11. Frustaci J. M., O'Brian M. R. Analysis of the Bradyrhizobium japonicum hemH gene and its expression in Escherichia coli. Appl Environ Microbiol. 1993 Aug;59(8):2347–2351. doi: 10.1128/aem.59.8.2347-2351.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Frustaci J. M., O'Brian M. R. Characterization of a Bradyrhizobium japonicum ferrochelatase mutant and isolation of the hemH gene. J Bacteriol. 1992 Jul;174(13):4223–4229. doi: 10.1128/jb.174.13.4223-4229.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Frustaci J. M., Sangwan I., O'Brian M. R. Aerobic growth and respiration of a delta-aminolevulinic acid synthase (hemA) mutant of Bradyrhizobium japonicum. J Bacteriol. 1991 Feb;173(3):1145–1150. doi: 10.1128/jb.173.3.1145-1150.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Frustaci J. M., Sangwan I., O'Brian M. R. gsa1 is a universal tetrapyrrole synthesis gene in soybean and is regulated by a GAGA element. J Biol Chem. 1995 Mar 31;270(13):7387–7393. doi: 10.1074/jbc.270.13.7387. [DOI] [PubMed] [Google Scholar]
  15. Gabel C., Maier R. J. Oxygen-dependent transcriptional regulation of cytochrome aa3 in Bradyrhizobium japonicum. J Bacteriol. 1993 Jan;175(1):128–132. doi: 10.1128/jb.175.1.128-132.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gilles-Gonzalez M. A., Ditta G. S., Helinski D. R. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature. 1991 Mar 14;350(6314):170–172. doi: 10.1038/350170a0. [DOI] [PubMed] [Google Scholar]
  17. Hershey J. W. Translational control in mammalian cells. Annu Rev Biochem. 1991;60:717–755. doi: 10.1146/annurev.bi.60.070191.003441. [DOI] [PubMed] [Google Scholar]
  18. Kaczor C. M., Smith M. W., Sangwan I., O'Brian M. R. Plant delta-aminolevulinic acid dehydratase. Expression in soybean root nodules and evidence for a bacterial lineage of the Alad gene. Plant Physiol. 1994 Apr;104(4):1411–1417. doi: 10.1104/pp.104.4.1411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Keefe R. G., Maier R. J. Purification and characterization of an O2-utilizing cytochrome-c oxidase complex from Bradyrhizobium japonicum bacteroid membranes. Biochim Biophys Acta. 1993 Nov 2;1183(1):91–104. doi: 10.1016/0005-2728(93)90008-4. [DOI] [PubMed] [Google Scholar]
  20. Madsen O., Sandal L., Sandal N. N., Marcker K. A. A soybean coproporphyrinogen oxidase gene is highly expressed in root nodules. Plant Mol Biol. 1993 Oct;23(1):35–43. doi: 10.1007/BF00021417. [DOI] [PubMed] [Google Scholar]
  21. McGinnis S. D., O'Brian M. R. The Rhizobial hemA Gene Is Required for Symbiosis in Species with Deficient [delta]-Aminolevulinic Acid Uptake Activity. Plant Physiol. 1995 Aug;108(4):1547–1552. doi: 10.1104/pp.108.4.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mylona P., Pawlowski K., Bisseling T. Symbiotic Nitrogen Fixation. Plant Cell. 1995 Jul;7(7):869–885. doi: 10.1105/tpc.7.7.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. O'Brian M. R. Heme synthesis in the rhizobium-legume symbiosis: a palette for bacterial and eukaryotic pigments. J Bacteriol. 1996 May;178(9):2471–2478. doi: 10.1128/jb.178.9.2471-2478.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Page K. M., Guerinot M. L. Oxygen control of the Bradyrhizobium japonicum hemA gene. J Bacteriol. 1995 Jul;177(14):3979–3984. doi: 10.1128/jb.177.14.3979-3984.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pfeifer K., Kim K. S., Kogan S., Guarente L. Functional dissection and sequence of yeast HAP1 activator. Cell. 1989 Jan 27;56(2):291–301. doi: 10.1016/0092-8674(89)90903-3. [DOI] [PubMed] [Google Scholar]
  26. Preisig O., Anthamatten D., Hennecke H. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3309–3313. doi: 10.1073/pnas.90.8.3309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Preisig O., Zufferey R., Thöny-Meyer L., Appleby C. A., Hennecke H. A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol. 1996 Mar;178(6):1532–1538. doi: 10.1128/jb.178.6.1532-1538.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sangwan I., O'Brian M. R. Expression of the soybean (Glycine max) glutamate 1-semialdehyde aminotransferase gene in symbiotic root nodules. Plant Physiol. 1993 Jul;102(3):829–834. doi: 10.1104/pp.102.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sangwan I., O'brian M. R. Characterization of delta-Aminolevulinic Acid Formation in Soybean Root Nodules. Plant Physiol. 1992 Mar;98(3):1074–1079. doi: 10.1104/pp.98.3.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sangwan I., O'brian M. R. Evidence for an inter-organismic heme biosynthetic pathway in symbiotic soybean root nodules. Science. 1991 Mar 8;251(4998):1220–1222. doi: 10.1126/science.251.4998.1220. [DOI] [PubMed] [Google Scholar]
  31. Schilke B. A., Donohue T. J. ChrR positively regulates transcription of the Rhodobacter sphaeroides cytochrome c2 gene. J Bacteriol. 1995 Apr;177(8):1929–1937. doi: 10.1128/jb.177.8.1929-1937.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Soupène E., Foussard M., Boistard P., Truchet G., Batut J. Oxygen as a key developmental regulator of Rhizobium meliloti N2-fixation gene expression within the alfalfa root nodule. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3759–3763. doi: 10.1073/pnas.92.9.3759. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES