Control of Acid Resistance in Escherichia coli

Abstract

Acid resistance (AR) in Escherichia coli is defined as the ability to withstand an acid challenge of pH 2.5 or less and is a trait generally restricted to stationary-phase cells. Earlier reports described three AR systems in E. coli. In the present study, the genetics and control of these three systems have been more clearly defined. Expression of the first AR system (designated the oxidative or glucose-repressed AR system) was previously shown to require the alternative sigma factor RpoS. Consistent with glucose repression, this system also proved to be dependent in many situations on the cyclic AMP receptor protein. The second AR system required the addition of arginine during pH 2.5 acid challenge, the structural gene for arginine decarboxylase (adiA), and the regulatorcysB, confirming earlier reports. The third AR system required glutamate for protection at pH 2.5, one of two genes encoding glutamate decarboxylase (gadA or gadB), and the gene encoding the putative glutamate:γ-aminobutyric acid antiporter (gadC). Only one of the two glutamate decarboxylases was needed for protection at pH 2.5. However, survival at pH 2 required both glutamate decarboxylase isozymes. Stationary phase and acid pH regulation of the gad genes proved separable. Stationary-phase induction of gadA and gadBrequired the alternative sigma factor ςS encoded byrpoS. However, acid induction of these enzymes, which was demonstrated to occur in exponential- and stationary-phase cells, proved to be ςS independent. Neither gad gene required the presence of volatile fatty acids for induction. The data also indicate that AR via the amino acid decarboxylase systems requires more than an inducible decarboxylase and antiporter. Another surprising finding was that the ςS-dependent oxidative system, originally thought to be acid induced, actually proved to be induced following entry into stationary phase regardless of the pH. However, an inhibitor produced at pH 8 somehow interferes with the activity of this system, giving the illusion of acid induction. The results also revealed that the AR system affording the most effective protection at pH 2 in complex medium (either Luria-Bertani broth or brain heart infusion broth plus 0.4% glucose) is the glutamate-dependent GAD system. Thus, E. coli possesses three overlapping acid survival systems whose various levels of control and differing requirements for activity ensure that at least one system will be available to protect the stationary-phase cell under naturally occurring acidic environments.

Characterization of an aspartate‐dependent acid survival system in Yersinia pseudotuberculosis

“…Deamination of aspartate to form fumarate and ammonia plays crucial role in this system. The mechanism of this acid survival system is different from other three amino acid-dependent systems which all require specific amino acid decarboxylases and their corresponding cognate antiporters [11].…”

Exploring the diversity of arsenic resistance genes from acid mine drainage microorganisms

“…Bacteria have several repair mechanisms in response to UV radiation-induced damage, all of them inducible as part of the SOS regulon (a well-known global response to DNA damage) or by a light-dependent repair mechanism (photoreactivation) (Mitchell and Karentz, 1993). On the other hand, when bacteria are exposed to acid conditions, protons may enter into the cell decreasing the cytoplasmic pH, which causes protein unfolding and uncoupling of oxidative phosphorylation disruption of regular biological processes and damage to cellular structures, eventually causing cell death (Castanie-Cornet et al, 1999;Guazzaroni et al, 2013). Besides, the response of E. coli to high temperature has been extensively investigated.…”

Ferroplasma and relatives, recently discovered cell wall‐lacking archaea making a living in extremely acid, heavy metal‐rich environments

“…In the context of acid tolerance of Ferroplasma, it is interesting that certain microorganisms growing optimally at neutral pH also have efficient systems for survival in acidic environments. Three AR systems of E. coli have been described (Castanie-Cornet et al, 1999). The first, AR1 (also designated the oxidative or glucose-repressed AR system), is stationary phase sigma factor (RpoS)-and cyclic AMP receptor protein (CRP)-dependent, but the mechanism by which AR1 protects E. coli from acid stress is presently unclear (Foster, 2004).…”

“…The first, AR1 (also designated the oxidative or glucose-repressed AR system), is stationary phase sigma factor (RpoS)-and cyclic AMP receptor protein (CRP)-dependent, but the mechanism by which AR1 protects E. coli from acid stress is presently unclear (Foster, 2004). The second and third systems, AR2 and AR3, are amino-acid-dependent (require the addition of arginine or glutamate for protection at pH 2.5) and involve amino-acid decarboxylases and antiporters (Castanie-Cornet et al, 1999;Foster, 2004). The glutamate decarboxylase isozymes GadA and GadB, and the arginine decarboxylase AdiA, replace the α-carboxyl groups of amino-acid substrates with protons from the cytoplasm, thereby producing CO 2 , γ-aminobutyric acid (GABA) or agmatine.…”

“…The glutamate decarboxylase isozymes GadA and GadB, and the arginine decarboxylase AdiA, replace the α-carboxyl groups of amino-acid substrates with protons from the cytoplasm, thereby producing CO 2 , γ-aminobutyric acid (GABA) or agmatine. The antiporters (GadC for glutamate and AdiC for arginine) expel the decarboxylation products and exchange them for new amino acid substrates (Castanie-Cornet et al, 1999;De Biase et al, 1999;Hersh et al, 1996;Foster, 2004). We tried to check the hypothesis that the yeast extract, which is the essential for growth, could serve as the source of the amino acids, i.e.…”