Global Regulatory Mutations in csrA and rpoS Cause Severe Central Carbon Stress in Escherichia coli in the Presence of Acetate

doi:10.1128/JB.182.6.1632-1640.2000

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Journal of Bacteriology, March 2000, p. 1632-1640, Vol. 182, No. 6
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Global Regulatory Mutations in csrA and rpoS Cause Severe Central Carbon Stress in Escherichia coli in the Presence of Acetate

Bangdong Wei,¹ Sooan Shin,² David LaPorte,³ Alan J. Wolfe,⁴ and Tony Romeo¹^,^*

Department of Molecular Biology and Immunology, University of North Texas Health Science Center at Fort Worth, Fort Worth, Texas 76107-2699¹; Fermentation System Research Unit, Korea Research Institute of Bioscience and Biotechnology, Yusong, Taejon, Korea²; Department of Biochemistry, University of Minnesota, Minneapolis, Minnesota 55455-0347³; and Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University, Chicago, Illinois 60153⁴

Received 24 August 1999/Accepted 13 December 1999

The csrA gene encodes a small RNA-binding protein, which acts as a global regulator in Escherichia coli and other bacteria(T. Romeo, Mol. Microbiol. 29:1321-1330, 1998). Its key regulatoryrole in central carbon metabolism, both as an activator of glycolysisand as a potent repressor of glycogen biosynthesis and gluconeogenesis,prompted us to examine the involvement of csrA in acetate metabolismand the tricarboxylic acid (TCA) cycle. We found that growth ofcsrA rpoS mutant strains was very poor on acetate as a sole carbonsource. Surprisingly, growth also was inhibited specifically bythe addition of modest amounts of acetate to rich media (e.g.,tryptone broth). Cultures grown in the presence of $>=$ 25 mM acetateconsisted substantially of glycogen biosynthesis (glg) mutants,which were no longer inhibited by acetate. Several classes ofglg mutations were mapped to known and novel loci. Several hypotheseswere examined to provide further insight into the effects of acetateon growth and metabolism in these strains. We determined thatcsrA positively regulates acs (acetyl-coenzyme A synthetase; Acs)expression and isocitrate lyase activity without affecting keyTCA cycle enzymes or phosphotransacetylase. TCA cycle intermediatesor pyruvate, but not glucose, galactose, or glycerol, restoredgrowth and prevented the glg mutations in the presence of acetate.Furthermore, amino acid uptake was inhibited by acetate specificallyin the csrA rpoS strain. We conclude that central carbon fluximbalance, inhibition of amino acid uptake, and a deficiency inacetate metabolism apparently are combined to cause metabolicstress by depleting the TCAcycle.

^* Corresponding author. Mailing address: Department of Molecular Biology and Immunology, University of North Texas Health ScienceCenter at Fort Worth, 3500 Camp Bowie Blvd., Fort Worth, TX 76107-2699.Phone: (817) 735-2121. Fax: (817) 735-2118. E-mail: tromeo{at}hsc.unt.edu.

Journal of Bacteriology, March 2000, p. 1632-1640, Vol. 182, No. 6
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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