Availability of public goods shapes the evolution of competing metabolic strategies

Abstract

Tradeoffs provide a rationale for the outcome of natural selection. A prominent example is the negative correlation between the growth rate and the biomass yield in unicellular organisms. This tradeoff leads to a dilemma, where the optimization of growth rate is advantageous for an individual, whereas the optimization of the biomass yield would be advantageous for a population. High-rate strategies are observed in a broad variety of organisms such as Escherichia coli, yeast, and cancer cells. Growth in suspension cultures favors fast-growing organisms, whereas spatial structure is of importance for the evolution of high-yield strategies. Despite this realization, experimental methods to directly select for increased yield are lacking. We here show that the serial propagation of a microbial population in a water-in-oil emulsion allows selection of strains with increased biomass yield. The propagation in emulsion creates a spatially structured environment where the growth-limiting substrate is privatized for populations founded by individual cells. Experimental evolution of several isogenic Lactococcus lactis strains demonstrated the existence of a tradeoff between growth rate and biomass yield as an apparent Pareto front. The underlying mutations altered glucose transport and led to major shifts between homofermentative and heterofermentative metabolism, accounting for the changes in metabolic efficiency. The results demonstrated the impact of privatizing a public good on the evolutionary outcome between competing metabolic strategies. The presented approach allows the investigation of fundamental questions in biology such as the evolution of cooperation, cell-cell interactions, and the relationships between environmental and metabolic constraints.A lthough the existence of tradeoffs in evolution seems to be undisputable, experimental evidence obtained under controlled conditions is scarce. Several examples failed to show tradeoffs (1-4), whereas others could find them (5, 6) or found general but not universal tradeoffs (7,8). A tradeoff between growth rate and growth yield in microbes (9-11) has direct implications for experiments carried out in liquid cultures. This is especially of importance during prolonged cultivations such as laboratory evolution experiments. In suspension, fast-growing variants outcompete slower growing ones at the cost of biomass yield (5). The yield versus rate optimization is governed by a dilemma where fast growth is advantageous from the perspective of an individual cell, whereas slow growth, and therefore high yield, is advantageous from the perspective of a population. This dilemma is consistent with a concept termed the tragedy of the commons (12). It is well described that spatial structure is essential for the selection of high-yield strategies (13-15). The yield/rate tradeoff of microbial growth has been linked to metabolic strategies (11) such as the switch between respiration and fermentation in yeast (9). It is suggested that the underlying cause of this tradeoff is based on...

Global metabolic network reorganization by adaptive mutations allows fast growth of Escherichia coli on glycerol

“…Our results suggest that the GLPK and RPOC strains may preferentially use overflow/fermentation and respiration, respectively, while the DKI has optimized the balance between these processes and biomass yield to achieve a maximum growth rate. These results agree well with known trade-offs between yield and growth rate during the evolutionary process 33,34 .…”

The physiology and ecological implications of efficient growth

“…Isolates with increased growth efficiency relative to the parental strain of L. lactis were observed, yet they typically grew slower than inefficient clones in the population. The clone with the greatest yield and slowest growth rate had a large increase in relative abundance throughout the 28 days of propagation, demonstrating selection favoring efficient growth (Bachmann et al, 2013).…”

Trade-offs between microbial growth phases lead to frequency-dependent and non-transitive selection

“…2B,C), as commonly considered in r/K selection studies [5,7,[12][13][14][15][16][17]. If the mutant has a longer lag time, then having a higher yield will be advantageous since the greater resource efficiency gives the mutant more time to grow exponentially to make up for its late start (Fig.…”

“…Previous work has focused mainly on the possibility of tradeoffs between these traits, especially between exponential growth rate and yield (resource efficiency) in the context of r/K selection [5,7,[12][13][14][15][16][17], as well as between growth rates at low and high concentrations of * To whom correspondence should be addressed.…”