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
Source: PubMed


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, σD, or σ70 and RpoS or σS) 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 σS 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 σS 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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    • "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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    • "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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    • "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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