Tuning of the porin expression under anaerobic growth conditions by His-to-Asp cross-phosphorelay through both the EnvZ-osmosensor and ArcB-anaerosensor in Escherichia coli

Background: Widespread bacterial signal transduction circuits are generally referred to as 'two-component systems' or 'histidine (His)-to-aspartate (Asp) phosphorelays.' In Escherichia coli, as many as 30 distinct His-to-Asp phosphorelay signalling pathways operate in response to a wide variety of environmental stimuli, such as medium osmolarity and anaerobiosis. In this regard, it is of interest whether or not some of them together constitute a network of signalling pathways through a physiologically relevant mechanism (often referred to as 'cross-regulation'). We have addressed this issue, with special reference to the osmo-responsive EnvZ and anaero-responsive ArcB phosphorelay signalling pathways in E. coli. Results: Under standard aerobic growth conditions, it is well known that the osmoregulatory profile of the outer membrane porins (OmpC and OmpF) is mainly regulated by the EnvZ-OmpR phosphorelay system in response to medium osmolarity. In this study, it was found that, under anaerobic growth conditions, E. coli cells exhibit a markedly altered expression profile of OmpC and OmpF This profile was significantly different from that observed for the cells grown aerobically. Results from extensive genetic studies showed that, under such anaerobic growth conditions, the arcB gene encoding the anaero-sensory His-kinase appears to be an auxiliary genetic determinant that regulates the expression profile of porins. We then provided several lines of in vivo and in vitro evidence, which taken together, supported the following conclusions. Conclusions: Under anaerobic growth conditions, porin expression is tuned not only by the authentic osmo-resposive EnvZ sensor, but also by the anaero-responsive ArcB sensor, in an OmpR-dependent manner. It is suggested that such ArcB-mediated cross-regulation plays a physiological role by integrating anaerobic respiratory signals into the porin regulation in E. coli anaerobiosis. The proposed model is a clear example of the interplay of two distinct His-to-Asp phosphorelay signalling pathways.