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Escherichia coli acid resistance: tales of an amateur acidophile

Nature Reviews Microbiology volume 2, pages 898–907 (2004)Cite this article

Key Points

  • There are four known acid-resistance systems present in pathogenic and non-pathogenic strains of Escherichia coli.

  • The two most effective systems involve the decarboxylation of glutamate or arginine, a process that consumes an intracellular proton.

  • In combination with cognate amino acid antiporters, the amino-acid-dependent systems increase intracellular pH and reverse transmembrane potential. Cl−/H+ antiporters are also important in this process.

  • Genetic regulation of the glutamate-dependent acid-resistance system involves a complex regulatory network of at least 10 proteins that mediate induction of gadE, the direct activator of the glutamate decarboxylase and antiporter genes.

  • Glutamate-dependent acid resistance seems to be important for the survival of E. coli O157:H7 in the bovine gastrointestinal tract.

Abstract

Gastrointestinal pathogens are faced with an extremely acidic environment. Within moments, a pathogen such as Escherichia coli O157:H7 can move from the nurturing pH 7 environment of a hamburger to the harsh pH 2 milieu of the stomach. Surprisingly, certain microorganisms that grow at neutral pH have elegantly regulated systems that enable survival during excursions into acidic environments. The best-characterized acid-resistance system is found in E. coli.

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Figure 1: Consumption of protons during decarboxylation of glutamate (a) and arginine (b).
Figure 2: Model of ClC chloride channel involvement in acid resistance.
Figure 3: Acid resistance reverses electrical potential (ΔΨ).
Figure 4: Model of acid resistance with positive-inside electrical potential.
Figure 5: Activation and accessory circuits controlling glutamate-dependent acid resistance.
Figure 6: Summary of microarray studies.

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Acknowledgements

I would like to thank the many colleagues and collaborators that have contributed to our current understanding of E. coli acid resistance. Specifically, J. Slonczewski, T. Conway, G. Church, G. Storz, P. Small, D. De Biase, G. Bennett and C. Miller. I also gratefully acknowledge the generous support of the National Institutes of Health and the United States Department of Agriculture.

Author information

Authors and Affiliations

  1. Department of Microbiology and Immunology, University of South Alabama College of Medicine, Mobile, 36695, Alabama, USA

    John W. Foster

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DATABASES

Entrez

Brucella melitensis

Chlamydia pneumoniae

Clostridium perfringens

Coxiella burnettii

Escherichia coli

gadA

Helicobacter pylori

Salmonella enterica serovar Typhimurium

Vibrio cholerae

SwissProt

AdiC

CRP

EvgA

EvgS

GadE

GadX

TrmE

YdeO

FURTHER INFORMATION

John W. Foster's laboratory

BRENDA enzyme database

Glossary

STATIONARY PHASE

A stage of extremely slow growth that occurs when nutrients are limited, or when detrimental metabolic end products accumulate.

SIGMA FACTOR

The subunit of RNA polymerase holoenzyme that is required for promoter sequence recognition and the ability to initiate transcription.

ANTIPORTERS

Inner membrane transport proteins that expel one compound that is present in the cytoplasm in exchange for importing a different compound into the cell.

PROTONMOTIVE FORCE

The force attempting to draw protons across the cytoplasmic membrane. It is a combination of the inwardly directed chemical concentration gradient of H+ plus the attractive force of an internal negative electrical charge.

ELECTROGENIC

When a coupled transport system alters the transmembrane electrical gradient — for example, antiport exchange of a +1 charged molecule for a +2 charged molecule. Any pump, whether ATP-dependent or Na+-dependent, which moves net electrical charge across the membrane is called an electrogenic pump.

HYPERPOLARIZATION

When the electrical gradient across the membrane becomes too large and compromises membrane integrity.

EXPONENTIAL GROWTH

A stage of rapid growth where cells multiply exponentially.

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Foster, J. Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2, 898–907 (2004). https://doi.org/10.1038/nrmicro1021

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