Escherichia coli Transcriptome Dynamics during the Transition from Anaerobic to Aerobic Conditions

Abstract

Escherichia coli is a metabolically versatile bacterium that is able to grow in the presence and absence of oxygen. Several previous transcript-profiling experiments have compared separate anaerobic and aerobic cultures. Here the process of adaptation was investigated by determining changes in transcript profiles when anaerobic steady-state cultures were perturbed by the introduction of air. Within 5 min of culture aeration the abundances of transcripts associated with anaerobic metabolism were decreased, whereas transcripts associated with aerobic metabolism were increased. In addition to the rapid switch to aerobic central metabolism, transcript profiling, supported by experiments with relevant mutants, revealed transient changes suggesting that the peroxide stress response, methionine biosynthesis, and degradation of putrescine play important roles during the adaptation to aerobic conditions. Escherichia coli is a metabolically versatile bacterium that is able to grow in the presence and absence of oxygen. As an inhabitant of the lower intestine, E. coli often occupies an oxygen-starved niche only to be excreted from the host into an aerobic external environment. The ability to adapt to such changes is rooted in altered patterns of gene expression in response to key cues, such as O 2 availability.Depending on the availabilities of electron donors and acceptors, E. coli uses one of three metabolic modes to support growth (1). In the presence of O 2 , aerobic respiration allows the complete oxidation of a growth substrate and therefore is the most productive and hence the preferred metabolic mode (1). During aerobic metabolism, the glycolytic conversion of glucose to pyruvate and the oxidative decarboxylation of pyruvate by the pyruvate dehydrogenase complex leads to the formation of acetyl-CoA, which feeds the citric acid cycle (CAC).2 Oxidation of the acetyl units generates reducing equivalents that are transferred to O 2 via aerobic electron transport chains, creating proton gradients that can be used to generate ATP and drive other essential activities (2). In the absence of O 2 , two alternative metabolic modes are available. If a terminal electron acceptor, such as NO 3 Ϫ , is present, then anaerobic respiration is possible. During anaerobic respiration the role of the pyruvate dehydrogenase complex is assumed by pyruvate formate-lyase; the CAC is repressed, and the metabolic flow in the C 4 section of the CAC is reversed. Anaerobic respiration yields less energy than aerobic respiration because the substrate is only partially oxidized (1). However, anaerobic respiration is more productive than fermentation, where energy is conserved by substrate level phosphorylation, and redox balance is achieved by the formation of acetate, ethanol, H 2 , CO 2 , formate, succinate, and lactate (3). Thus, enormous changes in E. coli physiology are provoked by changes in O 2 availability.Previous reports of the effects of O 2 on the transcript profile of E. coli have compared separate aerobic and anaerobic cultures, usua...

γ-Glutamylputrescine Synthetase in the Putrescine Utilization Pathway of Escherichia coli K-12

“…Accordingly the physiological role and kinetic parameters of PuuA could not be evaluated meaningfully. Also regulation of the expression of puuA was not fully reported except that the regulation of puuA occurring in response to O 2 was mediated by ArcA and FNR (27). Furthermore experimental comparison of two putrescine degradation pathways in E. coli (9,10,12,13) (Fig.…”

“…The puuP promoter (puuP p ) is a putative promoter. The positions of other promoters were described previously (27). It was reported previously (27) that there were FNR and ArcA (transcriptional regulators) sites in the intergenic region between puuA and puuD.…”

“…YgjG and YdcW comprise the traditional pathway to degrade putrescine to GABA without ␥-glutamylation. It was reported that PuuR (10), ArcA, and FNR (27) are transcriptional repressors of puuA and puuD. ␥-Glu-␥-aminobutyraldehyde, ␥-glutamyl-␥-aminobutyraldehyde; ␣-KG, ␣-ketoglutarate.…”

The anatomy of microbial cell state transitions in response to oxygen

“…Cold Spring Harbor Laboratory Press on April 28, 2019 -Published by genome.cshlp.org Downloaded from served in other organisms such as E. coli (Partridge et al 2006(Partridge et al , 2007.…”

Adaptation of anaerobic cultures of Escherichia coli K‐12 in response to environmental trimethylamine‐N‐oxide

“…The assertion that the increased abundance of the cyo transcript was not caused by unintended introduction of O 2 was supported by the absence of the broad transcriptional response that is observed upon transfer of E. coli cultures to micro‐aerobic or aerobic growth conditions (Partridge et al ., 2006; Trotter et al ., 2011; Rolfe et al ., 2012). …”