Article

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

School of Molecular and Microbial Biosciences G08, The University of Sydney, Sydney, NSW 2006, Australia.
Journal of Bacteriology (Impact Factor: 2.69). 10/2004; 186(17):5614-20. DOI: 10.1128/JB.186.17.5614-5620.2004
Source: PubMed

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.

Download full-text

Full-text

Available from: Thomas Ferenci, Jun 30, 2015
0 Followers
 · 
72 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Although it is known that Escherichia coli O157 is capable of long-term soil survival, little is known about the mechanisms involved. This study investigated the role of the general stress response system RpoS in E. coli soil survival. The results showed that E. coli O157 isolates capable of long-term survival (longer than 200 days) in manure-amended soil were characterized by the absence of mutations in their rpoS gene. In contrast, the strains not capable of long-term survival all possessed mutations in their rpoS gene. In addition, the long-term surviving strains showed significantly higher levels of acid resistance in simulated gastric fluid (pH 2.5). Sequencing of rpoS gene of bovine, food and clinical isolates revealed a skweded distribution of rpoS wild-type and mutant strains among the different sources. Bovine and food isolates compromised low numbers of mutants (resp. <1.4% and 6.9%), while a relatively high number of mutants was observed among human isolates (32.9%). The results indicate that a fully functional RpoS system is an advantage for survival in the manure-amended soil environment. Further deletion and complementation studies should provide more evidence on the role of RpoS in the long-term survival of E. coli O157 in diverse environments. © 2012 Federation of European Microbiological Societies. Published by Blackwell PublishingLtd. All rights reserved.
    FEMS Microbiology Letters 10/2012; 338(1). DOI:10.1111/1574-6968.12024 · 2.72 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Plants are increasingly considered as secondary reservoirs for commensal and pathogenic Escherichia coli strains, but the ecological and functional factors involved in this association are not clear. To address this question, we undertook a comparative approach combining phenotypic and phylogenetic analyses of E. coli isolates from crops and mammalian hosts. Phenotypic profiling revealed significant differences according to the source of isolation. Notably, isolates from plants displayed higher biofilm and extracellular matrix production and higher frequency of utilization of sucrose and the aromatic compound p-hydroxyphenylacetic acid. However, when compared with mammalian-associated strains, they reached lower growth yields on many C-sources commonly used by E. coli. Strikingly, we observed a strong association between phenotypes and E. coli phylogenetic groups. Strains belonging to phylogroup B1 were more likely to harbour traits indicative of a higher ability to colonize plants, whereas phylogroup A and B2 isolates displayed phenotypes linked to an animal-associated lifestyle. This work provides clear indications that E. coli phylogroups are specifically affected by niche-specific selective pressures, and provides an explanation on why E. coli population structures vary in natural environments, implying that different lineages in E. coli have substantially different transmission ecology.
    Environmental Microbiology 07/2012; 15(2). DOI:10.1111/j.1462-2920.2012.02852.x · 6.24 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Nutrient-limited continuous cultures in chemostats have been used to study microbial cell physiology for over 60 years. Genome instability and genetic heterogeneity are possible uncontrolled factors in continuous cultivation experiments. We investigated these issues by using high-throughput (HT) DNA sequencing to characterize samples from different phases of a glucose-limited accelerostat (A-stat) experiment with Escherichia coli K-12 MG1655 and a duration regularly used in cell physiology studies (20 generations of continuous cultivation). Seven consensus mutations from the reference sequence and five subpopulations characterized by different mutations were detected in the HT-sequenced samples. This genetic heterogeneity was confirmed to result from the stock culture by Sanger sequencing. All the subpopulations in which allele frequencies increased (betA, cspG/cspH, glyA) during the experiment were also present at the end of replicate A-stats, indicating that no new subpopulations emerged during our experiments. The fact that ~31 % of the cells in our initial cultures obtained directly from a culture stock centre were mutants raises concerns that even if cultivations are started from single colonies, there is a significant chance of picking a mutant clone with an altered phenotype. Our results show that current HT DNA sequencing technology allows accurate subpopulation analysis and demonstrates that a glucose-limited E. coli K-12 MG1655 A-stat experiment with a duration of tens of generations is suitable for studying cell physiology and collecting quantitative data for metabolic modelling without interference from new mutations.
    Microbiology 06/2011; 157(Pt 9):2604-10. DOI:10.1099/mic.0.050658-0 · 2.84 Impact Factor