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Journal of Bacteriology, September 2004, p. 5614-5620, Vol. 186, No. 17
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.17.5614-5620.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

A Regulatory Trade-Off as a Source of Strain Variation in the Species Escherichia coli{dagger}

Thea King,1 Akira Ishihama,2 Ayako Kori,2 and Thomas Ferenci1*

School of Molecular and Microbial Biosciences G08, The University of Sydney, Sydney, Australia,1 Nippon Institute for Biological Science, Ome, Tokyo, Japan2

Received 30 March 2004/ Accepted 18 May 2004

There are few existing indications that strain variation in prokaryotic gene regulation is common or has evolutionary advantage. In this study, we report on isolates of Escherichia coli with distinct ratios of sigma factors (RpoD, {sigma}D, or {sigma}70 and RpoS or {sigma}S) that affect transcription initiated by RNA polymerase. Both laboratory E. coli K-12 lineages and nondomesticated isolates exhibit strain-specific endogenous levels of RpoS protein. We demonstrate that variation in genome usage underpins intraspecific variability in transcription patterns, resistance to external stresses, and the choice of beneficial mutations under nutrient limitation. Most unexpectedly, RpoS also controlled strain variation with respect to the metabolic capability of bacteria with more than a dozen carbon sources. Strains with higher {sigma}S levels were more resistant to external stress but metabolized fewer substrates and poorly competed for low concentrations of nutrients. On the other hand, strains with lower {sigma}S levels had broader nutritional capabilities and better competitive ability with low nutrient concentrations but low resistance to external stress. In other words, RpoS influenced both r and K strategist functions of bacteria simultaneously. The evolutionary principle driving strain variation is proposed to be a conceptually novel trade-off that we term SPANC (for "self-preservation and nutritional competence"). The availability of multiple SPANC settings potentially broadens the niche occupied by a species consisting of individuals with narrow specialization and reveals an evolutionary advantage offered by polymorphic regulation. Regulatory diversity is likely to be a significant contributor to complexity in a bacterial world in which multiple sigma factors are a universal feature.

* Corresponding author. Mailing address: School of Molecular and Microbial Biosciences G08, The University of Sydney, Sydney, NSW 2006, Australia. Phone: (61) (2) 9351 4277. Fax: (61) (2) 9351 4571. E-mail: tferenci{at}mail.usyd.edu.au.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, September 2004, p. 5614-5620, Vol. 186, No. 17
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.17.5614-5620.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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