The general stress resistance of Escherichia coli is controlled by the RpoS sigma factor ( S ), but mutations in rpoS are surprisingly common in natural and laboratory populations. Evidence for the selective advantage of losing rpoS was obtained from experiments with nutrient-limited bacteria at different growth rates. Wild-type bacteria were rapidly displaced by rpoS mutants in both glucose-and nitrogen-limited chemostat populations. Nutrient limitation led to selection and sweeps of rpoS null mutations and loss of general stress resistance. The rate of takeover by rpoS mutants was most rapid (within 10 generations of culture) in slower-growing populations that initially express higher S levels. Competition for core RNA polymerase is the likeliest explanation for reduced expression from distinct promoters dependent on 70 and involved in the hunger response to nutrient limitation. Indeed, the mutation of rpoS led to significantly higher expression of genes contributing to the high-affinity glucose scavenging system required for the hunger response. Hence, rpoS polymorphism in E. coli populations may be viewed as the result of competition between the hunger response, which requires sigma factors other than S for expression, and the maintenance of the ability to withstand external stresses. The extent of external stress significantly influences the spread of rpoS mutations. When acid stress was simultaneously applied to glucose-limited cultures, both the phenotype and frequency of rpoS mutations were attenuated in line with the level of stress. The conflict between the hunger response and maintenance of stress resistance is a potential weakness in bacterial regulation.
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, D , or 70 and RpoS or 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 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 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.The major source of variation in prokaryotes is thought to be the loss or gain of functional genes or elements, such as pathogenicity islands (14, 33). Members of a bacterial species such as Escherichia coli have common properties and similar chromosomal organizations, but the species is phenotypically diverse (44). Isolates of E. coli exhibit many distinct properties, including distinct growth rates (28) and stress sensitivities (1, 43). Some of the differences are undoubtedly due to loss or gain of genes, but is there also a difference in gene usage or expression between strains? The gene regulatory consistency of bacteria is relatively poorly studied, but it needs to be understood if the full range of bacterial variation is to be established. In this study, we investigated whether strain-specific gene usage is a source of bacterial variation in E. coli.Our starting point for examining this question arose from recent studies of the polymorphism of the RpoS sigma factor in isolates of E. coli and Salmonella (11, 31). If a central regulator of stress resistance genes (RpoS or S [24,40]) is not conserved, then how constant is gene usage on a global scale? It is evident from both laboratory studies and the occurrence of rpoS mutations in natural populations that ...
SummaryStress protection is an important but costly contributor to bacterial survival. Two distinct forms of environmental protection share a common cost and a significant species-wide variability. Porin-mediated outer membrane permeability and the RpoS-controlled general stress response both involve a tradeoff between self-preservation and nutritional competence, called the SPANC balance. Interestingly, different Escherichia coli strains exhibit distinct settings of the SPANC balance. It is tilted towards high stress resistance and a restricted diet in some isolates whereas others have broader nutritional capability and better nutrient affinity but lower levels of resistance. Growth-or stress-related selective pressures working in opposite directions (antagonistic pleiotropy) result in polymorphisms affecting porins and RpoS. Consequently, these important cellular components are present at distinct concentrations in different isolates. A generalized hypothesis to explain bacterial adaptation, based on the SPANC investigations, is offered. A holistic approach to bacterial adaptation, involving a gamut of regulation and mutation, is likely to be the norm in broadening the capabilities of a species. Indeed, there is unlikely to be a standard regulatory setting typical for all members of a species. Gene regulation provides a limited fine control for maintaining the right level of adaptation in a particular niche but mutational changes provide the coarse control for adaptation between the specieswide environments of free-living bacteria .
The evolution of new combinations of bacterial properties contributes to biodiversity and the emergence of new diseases. We investigated the capacity for bacterial divergence with a chemostat culture of Escherichia coli. A clonal population radiated into more than five phenotypic clusters within 26 days, with multiple variations in global regulation, metabolic strategies, surface properties, and nutrient permeability pathways. Most isolates belonged to a single ecotype, and neither periodic selection events nor ecological competition for a single niche prevented an adaptive radiation with a single resource. The multidirectional exploration of fitness space is an underestimated ingredient to bacterial success even in unstructured environments.
Free-living bacteria are expert in adapting to variations in nutrient availability, often using an array of transport systems of different affinities to scavenge for particular substrates (multiport). This review concentrates on the regulation of expression of different transporters contributing to multiport in response to varying nutrient levels. A novel mechanism of controlling bacterial transport affinity under sugar limitation is described. In particular, switching from glucose-rich to glucose-limited conditions results in Escherichia coli orchestrating outer membrane changes as well as the induction of a periplasmic binding protein-dependent (ABC-type) transport system. The changes leading to the high affinity transport pathway are directed towards uptake of rapidly utilisable concentrations and are optimal close to 10-6 M medium glucose. High affinity transport is absent under both glucose-rich 'feast' and glucose-starved 'famine' conditions hence high affinity transporters are not simply repressed by excess nutrient. Rather, the improvement in glucose scavenging involves induction of genes in 2 distinct regulons (mgl/gal and mal/lamB) through synthesis of 2 different endogenous inducer molecules (galactose, maltotriose). Endoinducer levels are tightly controlled by extracellular glucose concentration at different glucose-limited growth rates. Aside from endoinducers, the elevated intracellular level of cAMP plays a role in induction of the high-affinity pathway but cAMP-mediated relief from catabolite repression is not itself sufficient for high affinity transport. In contrast to the repressive role of glucose when present at millimolar concentrations, micromolar glucose also leads to the induction of transport systems for other sugars, further broadening the scavenging potential of nutrient-limited bacteria for other substrates.
Bacteria are sometimes neither starving nor under nutrient-excess conditions. When growing with suboptimal levels of nutrients, hungry bacteria express appropriate cellular responses. This review discusses approaches to defining the hunger response in both molecular and growth kinetic terms. The gene expression changes unique to hunger conditions are described, using Escherichia coli as the primary example. Metabolite changes with hunger and starvation and the differing role of the stationary phase regulator RpoS also lead to the hypothesis proposed in this review that bacteria undertake distinct approaches to hunger and starvation. Indeed, an understanding of the difference between hunger and starvation and the incompatibility between hunger and starvation responses explains some of the paradoxical mutational adaptations, such as rpoS inactivation, found in natural populations.
Environmental stresses increase genetic variation in bacteria, plants, and human cancer cells. The linkage between various environments and mutational outcomes has not been systematically investigated, however. Here, we established the influence of nutritional stresses commonly found in the biosphere (carbon, phosphate, nitrogen, oxygen, or iron limitation) on both the rate and spectrum of mutations in Escherichia coli. We found that each limitation was associated with a remarkably distinct mutational profile. Overall mutation rates were not always elevated, and nitrogen, iron, and oxygen limitation resulted in major spectral changes but no net increase in rate. Our results thus suggest that stress-induced mutagenesis is a diverse series of stress input–mutation output linkages that is distinct in every condition. Environment-specific spectra resulted in the differential emergence of traits needing particular mutations in these settings. Mutations requiring transpositions were highest under iron and oxygen limitation, whereas base-pair substitutions and indels were highest under phosphate limitation. The unexpected diversity of input–output effects explains some important phenomena in the mutational biases of evolving genomes. The prevalence of bacterial insertion sequence transpositions in the mammalian gut or in anaerobically stored cultures is due to environmentally determined mutation availability. Likewise, the much-discussed genomic bias towards transition base substitutions in evolving genomes can now be explained as an environment-specific output. Altogether, our conclusion is that environments influence genetic variation as well as selection.
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