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Abstract
Inhibition of bacterial growth under aerobic conditions by elevated levels of cyclic adenosine 3′,5′-monophosphate (cAMP), first revealed more than 50 years ago, was attributed to accumulation of toxic methylglyoxal (MG). Here, we report a Crp-dependent mechanism rather than MG accumulation that accounts for the phenotype in Shewanella oneidensis, an emerging research model for the bacterial physiology. We show that a similar phenotype can be obtained by removing CpdA, a cAMP phosphodiesterase that appears more effective than its Escherichia coli counterpart. Although production of heme c and cytochromes c is correlated well with cAMP levels, neither is sufficient for the retarded growth. Quantities of overall cytochromes c increased substantially in the presence of elevated cAMP, a phenomenon resembling cells respiring on non-oxygen electron acceptors. In contrast, transcription of Crp-dependent genes encoding both cytochromes bd and cbb3 oxidases is substantially repressed under the same condition. Overall, our results suggest that cAMP of elevated levels drives cells into a low-energetic status, under which aerobic respiration is inhibited.
Highlights
Among living organisms, prokaryotes thrive in every potential habitat on the Earth suitable for life because of their unparallel metabolic diversity
In both cases cell densities increased constantly when growth was not completely prohibited, a phenomenon not observed in E. coli, whose growth is completely arrested by much less cAMP (0.5 mM)[22]
Cell viability of S. oneidensis appeared to be slightly reduced. This was due to the growth defect because there was no difference in the number of viable cells between samples treated by cAMP and not from viable-cell counting
Summary
Prokaryotes thrive in every potential habitat on the Earth suitable for life because of their unparallel metabolic diversity. The primary role of the canonical cAMP-Crp system, revealed mostly by early studies on Escherichia coli, is to regulate uptake of preferred carbon sources and repression of genes required for utilization of less preferred ones, a process called carbon catabolite repression (CCR)[3]. The bacterium, probably all of shewanellae, is regarded respiratory versatile because it derives energy by coupling organic matter oxidation to the respiration of an array of terminal electron acceptors (EAs), such as oxygen, fumarate, nitrate, and metal oxides[5] To date, how this bacterium adopts different metabolic modes in response to the availability of different EAs has been intensively studied, and some progresses have been made. This effect of cAMP is attributed to accumulation of methylglyoxal (MG), which is a toxic intermediate produced from dihydroxyacetone phosphate (DHAP) by MG synthase (MGS)[22,24]
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