A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

Abstract

Bacterial species are internally diverse in genomic and multi-locus gene comparisons. The ecological causes of phenotypic and genotypic diversity within species are far less well understood. Here, we focus on the competitive fitness for growth on nutrients within Escherichia coli, an internally rich species. Competition experiments in nutrient-limited chemostats revealed that members of the ECOR collection exhibited a wide continuum of competitive abilities, with some fitter and some less fit than the lab strain MG1655. We observed an inverse relationship between competitiveness and the resistance of strains to detergent and antibiotic, consistent with the notion that membrane permeability and competitive fitness are linked by a trade-off between selfpreservation and nutritional competence (SPANC); high permeability has a postulated cost in antibacterial sensitivity whereas a low permeability has a cost in nutrient affinity. Isolates moved along the markedly nonlinear trade-off curve by mutational adaptation; an ECOR strain sensitive to antibacterials and a good competitor was easily converted by mutation into a mutant with higher resistance but poorer competition in the presence of low antibiotic concentrations. Conversely, a resistant ECOR strain changed into a better competitor after a short period of selection under nutrient limitation. In both directions, mutations can affect porin proteins and outer membrane permeability, as indicated by protein analysis, gene sequencing and an independent assay of outer membrane permeability. The extensive, species-wide diversity of E. coli in ecologically important traits can thus be explained as an evolutionary consequence of a SPANC trade-off driven by antagonistic pleiotropy.

Elucidating the Function of the RpoS Regulon

“…The need to express adaptive functions under stress conditions (i.e., those controlled by RpoS) and the ability to scavenge nutrients released from cells during high density stationary phase creates a metabolic dichotomy, which apparently accommodated a single global regulatory system. This dual selective process is termed the self-preservation and nutritional competence, or SPANC balance [51,52]. This idea posits that populations of cells are a type of growth/mutation equilibrium that combines the mutational process with distinct and changing selective forces (e.g., nutritional) -a phenomenon in which rpoS mutations are a common modifier.…”

The form of a trade‐off determines the response to competition

“…). This is a shortcoming because, as recently demonstrated, a mechanistic understanding can explain species‐wide variation in ecologically important traits (Phan & Ferenci ).…”

“…However, even if the existence of a trade-off has been observed we still have little understanding of mechanisms that cause them (Stearns 2000;Tilman 2000;Braendle et al 2011). This is a shortcoming because, as recently demonstrated, a mechanistic understanding can explain species-wide variation in ecologically important traits (Phan & Ferenci 2013).…”

Modeling and Validation of the Ecological Behavior of Wild-Type Listeria monocytogenes and Stress-Resistant Variants

“…The concept of stress resistance as a trade-off for growth has been well described in the literature (14)(15)(16). Specialization on survival often comes at the cost of slower multiplication.…”