Literature DB >> 15317765

A regulatory trade-off as a source of strain variation in the species Escherichia coli.

Thea King1, Akira Ishihama, Ayako Kori, Thomas Ferenci.   

Abstract

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, sigmaD, or sigma70 and RpoS or sigmaS) 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 sigmaS 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 sigmaS 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.

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Year:  2004        PMID: 15317765      PMCID: PMC516835          DOI: 10.1128/JB.186.17.5614-5620.2004

Source DB:  PubMed          Journal:  J Bacteriol        ISSN: 0021-9193            Impact factor:   3.490


  38 in total

1.  Definition of the Escherichia coli MC4100 genome by use of a DNA array.

Authors:  Joseph E Peters; Timothy E Thate; Nancy L Craig
Journal:  J Bacteriol       Date:  2003-03       Impact factor: 3.490

Review 2.  Multiple sigma subunits and the partitioning of bacterial transcription space.

Authors:  Tanja M Gruber; Carol A Gross
Journal:  Annu Rev Microbiol       Date:  2003       Impact factor: 15.500

Review 3.  Regulation by proteolysis in bacterial cells.

Authors:  Urs Jenal; Regine Hengge-Aronis
Journal:  Curr Opin Microbiol       Date:  2003-04       Impact factor: 7.934

4.  The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations.

Authors:  Lucinda Notley-McRobb; Shona Seeto; Thomas Ferenci
Journal:  Proc Biol Sci       Date:  2003-04-22       Impact factor: 5.349

Review 5.  Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation.

Authors:  Santiago F Elena; Richard E Lenski
Journal:  Nat Rev Genet       Date:  2003-06       Impact factor: 53.242

6.  Prokaryotic chromosomes and disease.

Authors:  Jörg Hacker; Ute Hentschel; Ulrich Dobrindt
Journal:  Science       Date:  2003-08-08       Impact factor: 47.728

7.  What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli?

Authors:  Thomas Ferenci
Journal:  Trends Microbiol       Date:  2003-10       Impact factor: 17.079

8.  Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu.

Authors:  M J Casadaban
Journal:  J Mol Biol       Date:  1976-07-05       Impact factor: 5.469

9.  Standard reference strains of Escherichia coli from natural populations.

Authors:  H Ochman; R K Selander
Journal:  J Bacteriol       Date:  1984-02       Impact factor: 3.490

Review 10.  Regulation by nutrient limitation.

Authors:  T Ferenci
Journal:  Curr Opin Microbiol       Date:  1999-04       Impact factor: 7.934

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  73 in total

Review 1.  The RpoS-mediated general stress response in Escherichia coli.

Authors:  Aurelia Battesti; Nadim Majdalani; Susan Gottesman
Journal:  Annu Rev Microbiol       Date:  2011       Impact factor: 15.500

2.  Genomic identification of a novel mutation in hfq that provides multiple benefits in evolving glucose-limited populations of Escherichia coli.

Authors:  Ram Maharjan; Zhemin Zhou; Yan Ren; Yang Li; Joël Gaffé; Dominique Schneider; Christopher McKenzie; Peter R Reeves; Thomas Ferenci; Lei Wang
Journal:  J Bacteriol       Date:  2010-06-11       Impact factor: 3.490

3.  The Polymorphic Aggregative Phenotype of Shiga Toxin-Producing Escherichia coli O111 Depends on RpoS and Curli.

Authors:  M E Diodati; A H Bates; W G Miller; M Q Carter; Y Zhou; M T Brandl
Journal:  Appl Environ Microbiol       Date:  2015-12-28       Impact factor: 4.792

4.  Starvation for different nutrients in Escherichia coli results in differential modulation of RpoS levels and stability.

Authors:  Mark J Mandel; Thomas J Silhavy
Journal:  J Bacteriol       Date:  2005-01       Impact factor: 3.490

5.  Divergence and redundancy of transport and metabolic rate-yield strategies in a single Escherichia coli population.

Authors:  Ram Prasad Maharjan; Shona Seeto; Thomas Ferenci
Journal:  J Bacteriol       Date:  2006-12-08       Impact factor: 3.490

6.  Loss of expression of cspC, a cold shock family gene, confers a gain of fitness in Escherichia coli K-12 strains.

Authors:  Devashish Rath; Narendra Jawali
Journal:  J Bacteriol       Date:  2006-10       Impact factor: 3.490

7.  Stationary phase reorganisation of the Escherichia coli transcription machinery by Crl protein, a fine-tuner of sigmas activity and levels.

Authors:  Athanasios Typas; Claudia Barembruch; Alexandra Possling; Regine Hengge
Journal:  EMBO J       Date:  2007-03-01       Impact factor: 11.598

8.  Guanosine 3',5'-bispyrophosphate coordinates global gene expression during glucose-lactose diauxie in Escherichia coli.

Authors:  Matthew F Traxler; Dong-Eun Chang; Tyrrell Conway
Journal:  Proc Natl Acad Sci U S A       Date:  2006-02-07       Impact factor: 11.205

9.  Genotype-by-environment interactions influencing the emergence of rpoS mutations in Escherichia coli populations.

Authors:  Thea King; Shona Seeto; Thomas Ferenci
Journal:  Genetics       Date:  2006-02-19       Impact factor: 4.562

10.  Identification of conserved amino acid residues of the Salmonella sigmaS chaperone Crl involved in Crl-sigmaS interactions.

Authors:  Véronique Monteil; Annie Kolb; Jacques D'Alayer; Pierre Beguin; Françoise Norel
Journal:  J Bacteriol       Date:  2009-12-11       Impact factor: 3.490

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