Abstract
Hydrogen metabolism in Salmonella typhimurium is differentially regulated by mutations in the two anaerobic regulatory pathways, defined by the fnr (oxrA) and oxrC genes, and is controlled by catabolite repression. The synthesis of the individual hydrogenase isoenzymes is also specifically influenced by fnr and oxrC mutations and by catabolite repression in a manner entirely consistent with the proposed role for each isoenzyme in hydrogen metabolism. Synthesis of hydrogenase isoenzyme 2 was found to be fnr dependent and oxrC independent, consistent with a role in respiration-linked hydrogen uptake which was shown to be similarly regulated. Also in keeping with such a respiratory role was the finding that both hydrogen uptake and the expression of isoenzyme 2 are under catabolite repression. In contrast, formate hydrogenlyase-dependent hydrogen evolution, characteristic of fermentative growth, was reduced in oxrC strains but not in fnr strains. Hydrogenase 3 activity was similarly regulated, consistent with a role in hydrogen evolution. Unlike the expression of hydrogenases 2 and 3, hydrogenase 1 expression was both fnr and oxrC dependent. Hydrogen uptake during fermentative growth was also both fnr and oxrC dependent. This provided good evidence for a distinction between hydrogen uptake during fermentation- and respiration-dependent growth and for a hydrogen-recycling process. The pattern of anaerobic control of hydrogenase activities illustrated the functional diversity of the isoenzymes and, in addition, the physiological distinction between the two anaerobic regulatory pathways, anaerobic respiratory genes being fnr dependent and enzymes required during fermentative growth being oxrC dependent.
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Selected References
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- Adams M. W., Mortenson L. E., Chen J. S. Hydrogenase. Biochim Biophys Acta. 1980 Dec;594(2-3):105–176. doi: 10.1016/0304-4173(80)90007-5. [DOI] [PubMed] [Google Scholar]
- Ballantine S. P., Boxer D. H. Isolation and characterisation of a soluble active fragment of hydrogenase isoenzyme 2 from the membranes of anaerobically grown Escherichia coli. Eur J Biochem. 1986 Apr 15;156(2):277–284. doi: 10.1111/j.1432-1033.1986.tb09578.x. [DOI] [PubMed] [Google Scholar]
- Ballantine S. P., Boxer D. H. Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. J Bacteriol. 1985 Aug;163(2):454–459. doi: 10.1128/jb.163.2.454-459.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barrett E. L., Kwan H. S., Macy J. Anaerobiosis, formate, nitrate, and pyrA are involved in the regulation of formate hydrogenlyase in Salmonella typhimurium. J Bacteriol. 1984 Jun;158(3):972–977. doi: 10.1128/jb.158.3.972-977.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bilous P. T., Weiner J. H. Dimethyl sulfoxide reductase activity by anaerobically grown Escherichia coli HB101. J Bacteriol. 1985 Jun;162(3):1151–1155. doi: 10.1128/jb.162.3.1151-1155.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graham A., Boxer D. H., Haddock B. A., Mandrand-Berthelot A. M., Jones R. W. Immunochemical analysis of the membrane-bound hydrogenase of Escherichia coli. FEBS Lett. 1980 May 5;113(2):167–172. doi: 10.1016/0014-5793(80)80584-9. [DOI] [PubMed] [Google Scholar]
- Jamieson D. J., Higgins C. F. Two genetically distinct pathways for transcriptional regulation of anaerobic gene expression in Salmonella typhimurium. J Bacteriol. 1986 Oct;168(1):389–397. doi: 10.1128/jb.168.1.389-397.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones R. W. The role of the membrane-bound hydrogenase in the energy-conserving oxidation of molecular hydrogen by Escherichia coli. Biochem J. 1980 May 15;188(2):345–350. doi: 10.1042/bj1880345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuritzkes D. R., Zhang X. Y., Lin E. C. Use of phi(glp-lac) in studies of respiratory regulation of the Escherichia coli anaerobic sn-glycerol-3-phosphate dehydrogenase genes (glpAB). J Bacteriol. 1984 Feb;157(2):591–598. doi: 10.1128/jb.157.2.591-598.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Lambden P. R., Guest J. R. Mutants of Escherichia coli K12 unable to use fumarate as an anaerobic electron acceptor. J Gen Microbiol. 1976 Dec;97(2):145–160. doi: 10.1099/00221287-97-2-145. [DOI] [PubMed] [Google Scholar]
- Lee J. H., Patel P., Sankar P., Shanmugam K. T. Isolation and characterization of mutant strains of Escherichia coli altered in H2 metabolism. J Bacteriol. 1985 Apr;162(1):344–352. doi: 10.1128/jb.162.1.344-352.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mallick U., Herrlich P. Regulation of synthesis of a major outer membrane protein: cyclic AMP represses Escherichia coli protein III synthesis. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5520–5523. doi: 10.1073/pnas.76.11.5520. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morpeth F. F., Boxer D. H. Kinetic analysis of respiratory nitrate reductase from Escherichia coli K12. Biochemistry. 1985 Jan 1;24(1):40–46. doi: 10.1021/bi00322a007. [DOI] [PubMed] [Google Scholar]
- Newman B. M., Cole J. A. The chromosomal location and pleiotropic effects of mutations of the nirA+ gene of Escherichia coli K12: the essential role of nirA+ in nitrite reduction and in other anaerobic redox reactions. J Gen Microbiol. 1978 May;106(1):1–12. doi: 10.1099/00221287-106-1-1. [DOI] [PubMed] [Google Scholar]
- PECK H. D., Jr, GEST H. Formic dehydrogenase and the hydrogenlyase enzyme complex in coli-aerogenes bacteria. J Bacteriol. 1957 Jun;73(6):706–721. doi: 10.1128/jb.73.6.706-721.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pascal M. C., Casse F., Chippaux M., Lepelletier M. Genetic analysis of mutants of Escherichia coli K12 and Salmonella typhimurium LT2 deficient in hydrogenase activity. Mol Gen Genet. 1975 Nov 24;141(2):173–179. doi: 10.1007/BF00267682. [DOI] [PubMed] [Google Scholar]
- Pecher A., Zinoni F., Böck A. The seleno-polypeptide of formic dehydrogenase (formate hydrogen-lyase linked) from Escherichia coli: genetic analysis. Arch Microbiol. 1985 May;141(4):359–363. doi: 10.1007/BF00428850. [DOI] [PubMed] [Google Scholar]
- Pecher A., Zinoni F., Jatisatienr C., Wirth R., Hennecke H., Böck A. On the redox control of synthesis of anaerobically induced enzymes in enterobacteriaceae. Arch Microbiol. 1983 Nov;136(2):131–136. doi: 10.1007/BF00404787. [DOI] [PubMed] [Google Scholar]
- Sankar P., Lee J. H., Shanmugam K. T. Cloning of hydrogenase genes and fine structure analysis of an operon essential for H2 metabolism in Escherichia coli. J Bacteriol. 1985 Apr;162(1):353–360. doi: 10.1128/jb.162.1.353-360.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sawers R. G., Ballantine S. P., Boxer D. H. Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: evidence for a third isoenzyme. J Bacteriol. 1985 Dec;164(3):1324–1331. doi: 10.1128/jb.164.3.1324-1331.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sawers R. G., Boxer D. H. Purification and properties of membrane-bound hydrogenase isoenzyme 1 from anaerobically grown Escherichia coli K12. Eur J Biochem. 1986 Apr 15;156(2):265–275. doi: 10.1111/j.1432-1033.1986.tb09577.x. [DOI] [PubMed] [Google Scholar]
- Sawers R. G., Jamieson D. J., Higgins C. F., Boxer D. H. Characterization and physiological roles of membrane-bound hydrogenase isoenzymes from Salmonella typhimurium. J Bacteriol. 1986 Oct;168(1):398–404. doi: 10.1128/jb.168.1.398-404.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw D. J., Rice D. W., Guest J. R. Homology between CAP and Fnr, a regulator of anaerobic respiration in Escherichia coli. J Mol Biol. 1983 May 15;166(2):241–247. doi: 10.1016/s0022-2836(83)80011-4. [DOI] [PubMed] [Google Scholar]
- Spassky A., Busby S., Buc H. On the action of the cyclic AMP-cyclic AMP receptor protein complex at the Escherichia coli lactose and galactose promoter regions. EMBO J. 1984 Jan;3(1):43–50. doi: 10.1002/j.1460-2075.1984.tb01759.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stewart V., MacGregor C. H. Nitrate reductase in Escherichia coli K-12: involvement of chlC, chlE, and chlG loci. J Bacteriol. 1982 Aug;151(2):788–799. doi: 10.1128/jb.151.2.788-799.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strauch K. L., Lenk J. B., Gamble B. L., Miller C. G. Oxygen regulation in Salmonella typhimurium. J Bacteriol. 1985 Feb;161(2):673–680. doi: 10.1128/jb.161.2.673-680.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waugh R., Boxer D. H. Pleiotropic hydrogenase mutants of Escherichia coli K12: growth in the presence of nickel can restore hydrogenase activity. Biochimie. 1986 Jan;68(1):157–166. doi: 10.1016/s0300-9084(86)81080-x. [DOI] [PubMed] [Google Scholar]
- Wu L. F., Mandrand-Berthelot M. A. Genetic and physiological characterization of new Escherichia coli mutants impaired in hydrogenase activity. Biochimie. 1986 Jan;68(1):167–179. doi: 10.1016/s0300-9084(86)81081-1. [DOI] [PubMed] [Google Scholar]