Differential regulation by cyclic AMP of starvation protein synthesis in Escherichia coli

Abstract

Of the 30 carbon starvation proteins whose induction has been previously shown to be important for starvation survival of Escherichia coli, two-thirds were not induced in cya or crp deletion mutants of E. coli at the onset of carbon starvation. The rest were induced, although not necessarily with the same temporal pattern as exhibited in the wild type. The starvation proteins that were homologous to previously identified heat shock proteins belonged to the latter class and were hyperinduced in Acya or Acrp mutants during starvation. Most of the cyciic AMP-dependent proteins were synthesized in the Acya mutant if exogenous cyclic AMP was added at the onset of starvation. Furthermore, ,l-galactosidase induction of several carbon starvation response gene fusions occurred only in a cyd+ genetic background. Thus, two-thirds of the carbon starvation proteins of E. coi require cyclic AMP and its receptor protein for induction; the rest do not. The former class evidently has no role in starvation survival, since Acya or Acip mutants of either E. coli or Salmonella typhimurium survived starvation as well as thefr wild-type parents did. The latter class, therefore, is likely to have a direct role in starvation survival. This possibility is strengthened by the finding that nearly all of the cya-and cip-independent proteins were also induced during nitrogen starvation and, as shown previousl, during phosphate starvation. Proteins whose synthesis is independent of cya-and crp control are referred to as Pex (postexponential).Starving bacteria are of both fundamental and applied interest (14,15,21,27,28). We have shown that during the first 4 to 5 h of starvation for carbon substrates (glucose or succinate) approximately 30 proteins are induced in Escherichia coli K-12 (14, 15) and that these proteins are important in starvation survival (27,28,32). Starvation-induced proteins have different temporal patterns of synthesis-some are synthesized very transiently during starvation, whereas others have a broader peak of synthesis (15). Investigators in other laboratories have also shown that unique genes are switched on and new proteins are synthesized at the onset of starvation (10,33,34).To better understand the regulation of starvation protein synthesis, we have focused on the role of the signal molecule adenosine 3',5'-cyclic monophosphate (cAMP) and its receptor protein (CRP). Intracellular cAMP levels increase at the onset of carbon starvation (5,8,19,26), and there appears to be an inverse relationship between the energetic state of the cell and cAMP levels (8, 13). This raises the possibility that cAMP acts as a signal for starvation protein synthesis. We have therefore investigated the effect of the loss of cAMP control on starvation protein synthesis in E. coli. Isogenic E. coli strains deleted in the adenylate cyclase gene (Acya) or the gene encoding CRP (Acrp) were examined. The results indicate that although several starvation genes are positively regulated by cAMP, many others are not, and that the latter class of ge...

The putative sigma factor KatF is regulated posttranscriptionally during carbon starvation

“…If a Acya background reduces katF transcription and abolishes its induction by starvation, as shown above, how are the KatF-regulated starvation proteins induced during carbon starvation in M9 medium in a Acya strain, as we have previously reported (27)? When the protein fusion to +786 was examined in a Acya background (strain AMS167) it exhibited ca.…”

“…Cyclic AMP appears to play a role in stimulating the transcription of katF. This observation was initially surprising in light of the ability of Acya strains to induce KatF-regulated starvation proteins (27). However, the kinetics of expression of the protein fusions suggest that the posttranscriptional regulatory mechanisms can compensate for the lack of increased katF transcription in the absence of cyclic AMP.…”

“…When Eschenchia coli is starved for carbon in a minimal medium, it induces over 50 proteins in a temporally regulated fashion (2,(13)(14)(15)27). The induction of at least 32 of these proteins requires the putative a factor KatF, since a strain containing a katF::TnlO mutation fails to induce these proteins (9, 15).…”

Ribosomes exist in large excess over the apparent demand for protein synthesis during carbon starvation in marine Vibrio sp. strain CCUG 15956

“…For example, E. coli mutants that are not capable of stationary-phase survival have been isolated (58), and tentative regulators of starvation protein synthesis have been identified (17,28). A specific set of starvation-induced proteins (Pex) have been identified as the proteins that are essential for starvation survival and development of cross-protection in E. coli (19,55). Most of the Pex proteins are among the proteins that E. coli synthesizes regardless of whether it is starved for carbon, nitrogen, or phosphorus (35).…”

Dormancy in non-sporulating bacteria

“…[76]. The regulatory role of cAMP during the transition of the cells to starvation conditions has also been demonstrated, at least for E. coli [77,78].…”