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: 2.81). 10/2004; 186(17):5614-20. DOI: 10.1128/JB.186.17.5614-5620.2004
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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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Available from: Thomas Ferenci, Oct 05, 2015
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    • "Subsequently, E. coli O157 gains advantage by simultaneously consuming several sugars that may be available because they are not consumed by the commensal intestinal microbiota (Fabich et al., 2008). This system could select for rpoS mutations as these mutants are characterized by increased nutrient scavenging abilities at the expense of stress-resistance (King et al., 2004). Further deletion and complementation studies ideally using in vivo systems (human and animal gut, and soil systems) should provide more insight into the role of RpoS in the adaptation of E. coli O157 to diverse environments. "
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    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 · 2.12 Impact Factor
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    • "For example, a commensal murine isolate of E. coli upregulates stress response genes in the IL-10-/- mouse model of colitis that decrease luminal bacterial densities in vivo, but have no effect on growth or persistence in vitro [28]. Additionally, a survey of many E. coli isolates has shown that high levels of σs, a transcription factor that controls expression of stress-response genes, correlates with increased resistance to environmental stress, but decreased ability to metabolize low concentrations of nutrients [34]. Thus, the functional outcome of bacterial responses to environmental conditions can lead to growth or persistence depending on the nature of the stimulus and the genetic composition of the bacteria. "
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    ABSTRACT: Inflammatory bowel diseases (IBD) may be caused in part by aberrant immune responses to commensal intestinal microbes including the well-characterized anaerobic gut commensal Bacteroides thetaiotaomicron (B. theta). Healthy, germ-free HLA-B27 transgenic (Tg) rats develop chronic colitis when colonized with complex gut commensal bacteria whereas non-transgenic (nTg) rats remain disease-free. However, the role of B. theta in causing disease in Tg rats is unknown nor is much known about how gut microbes respond to host inflammation. Tg and nTg rats were monoassociated with a human isolate of B. theta. Colonic inflammation was assessed by histologic scoring and tissue pro-inflammatory cytokine measurement. Whole genome transcriptional profiling of B. theta recovered from ceca was performed using custom GeneChips and data analyzed using dChip, Significance Analysis of Microarrays, and Gene Set Enrichment Analysis (GSEA) software. Western Blots were used to determine adaptive immune responses to a differentially expressed B. theta gene. B. theta monoassociated Tg rats, but not nTg or germ-free controls, developed chronic colitis. Transcriptional profiles of cecal B. theta were significantly different in Tg vs. nTg rats. GSEA revealed that genes in KEGG canonical pathways involved in bacterial growth and metabolism were downregulated in B. theta from Tg rats with colitis though luminal bacterial concentrations were unaffected. Bacterial genes in the Gene Ontology molecular function "receptor activity", most of which encode nutrient binding proteins, were significantly upregulated in B. theta from Tg rats and include a SusC homolog that induces adaptive immune responses in Tg rats. B. theta induces colitis in HLA-B27 Tg rats, which is associated with regulation of bacterial genes in metabolic and nutrient binding pathways that may affect host immune responses. These studies of the host-microbial dialogue may lead to the identification of novel microbial targets for IBD therapies.
    PLoS ONE 08/2012; 7(8):e42645. DOI:10.1371/journal.pone.0042645 · 3.23 Impact Factor
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    • "Similarly, while GMB isolates have decreased nutritional abilities, they possess traits indicating increased resistance to environmental challenges. Differences in SPANC-balance have been mainly linked to mutations affecting the levels of the alternative sigma factor RpoS (s S or s 38 ), with strains displaying low RpoS levels more able to acquire nutrients, but less capable of surviving stresses such as acid shock or starvation (King et al., 2004). However, we found very few strains with strongly impaired RpoS activity as assessed by catalase assays. "
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    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 · 6.20 Impact Factor
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