Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium.

Abstract

We isolated mutant strains of the facultative anaerobe Salmonella typhinuinum that grow either aerobically or anaerobically. Strict anaerobic mutants contained a defective DNA topoisomerase I gene (topi), while strict aerobic mutants contained a defective DNA gyrase subunit A gene (gyrA, also naLA). Topoisomerase I activity was detected in cell-free extracts of strict aerobic mutants but not of strict anaerobic mutant strains, whereas gyrase activity was detected in extracts of strict anaerobic mutants but not of strict aerobic mutants. Furthermore, extracts of wild-type cells, cultured under vigorous aerobic condition, contain topoisomerase I activity but no significant gyrase activity. In contrast, the extracts of anaerobically cultured wild-type cells contain gyrase activity but no significant topoisomerase I activity. Sucrose gradient centrifugation with ethidium bromide showed that chromosomal DNA in strict aerobic mutants and aerobically grown wild-type cells was relaxed, while the chromosomal DNA of strict anaerobic mutants and anaerobically grown wild-type cells was more supercoiled. Aerobic cultures of wild type and strict aerobic mutants produced both superoxide dismutase and catalase, whereas anaerobic cultures of wild type and strict anaerobic mutants did not. These results lead us to conclude that activity of topoisomerase I, associated with relaxation of chromosomal DNA, is necessary for expression of genes required for aerobic growth, whereas activity of gyrase, associated with supercoiling of chromosomal DNA, is necessary for expression of genes required for anaerobic growth.

Osmotic repression of anaerobic metabolic systems in Escherichia coli

“…Aside from its response to osmotic stress, DNA supercoiling was also involved in the regulation of anaerobic gene expression (13,32,33,52). The relationship between gyrasedependent and FNR-dependent anaerobic regulation has been observed by investigators in different laboratories.…”

Aerobic regulation of cytochrome d oxidase (cydAB ) operon expression in Escherichia coli: roles of Fnr and ArcA in repression and activation

“…One mechanism that may be responsible for this effect is the contribution of DNA supercoiling on P2 transcription during anaerobic vs. aerobic conditions. Studies with gyrase and topoisomerase mutants showed that the DNA in anaerobically grown cells is more highly supercoiled than in aerobically grown cells (Yamamoto and Droffner, 1985). Expression of the proU, tonB and fdhH genes has been shown to be directly influenced by the degree of DNA supercoiling (Axley and Stadtman, 1988;Dorman et al, 1988;Higgins et al, 1988).…”

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

“…Experimental data demonstrating a response at the level of DNA supercoiling to variations in pH (Bang et al 2002;Karem and Foster 1993;Quinn et al 2014), temperature (Goldstein and Drlica 1984), osmotic pressure (Alice and Sanchez-Rivas 1997; Bordes et al 2003;Cheung et al 2003;Higgins et al 1988;Meury and Kohiyama 1992;O'Byrne et al 1992;Sheehan et al 1992), oxygen supply (Bebbington and Williams 2001;Cameron et al 2011Cameron et al , 2013Cortassa and Aon 1993;Dixon et al 1988;Dorman et al 1988;Malkhosyan et al 1991;Yamamoto and Droffner 1985), oxidative stress (Weinstein-Fischer et al 2000), nutrition (Balke and Gralla 1987), growth phase (Bordes et al 2003;Conter et al 1997), intracellular growth (Ó Cróinín et al 2006) and much more have been reported. A rapidly growing cell has different gene expression requirements to one that is in stationary phase and one that is undergoing a growth phase transition has yet another set of needs.…”