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Biology subjects

van Doorn, G. S.

Publications and source records attributed to van Doorn, G. S..

6 recordsLinked to original sources

Temporal resource variation promotes growth equalization through alternative plasticity strategies

Evolutionary theory predicts that fluctuating environments favor adaptations that maximize geometric-mean fitness by reducing variance in performance across conditions. We tested this prediction experimentally by evolving the lactic acid bacterium Lactococcus cremoris on the sugars fructose and galactose in density-controlled chemostats under four resource regimes: constant supply of fructose, constant supply of galactose, a constant mixture of both sugars, and a temporally alternating supply of the two. In the absence of temporal variation, trade-offs between fructose and galactose resulted in evolutionary divergence into a fructose specialist and a galactose specialist. In contrast, adaptation to temporal resource variation equalised growth performance on both sugars by increasing its growth rate on galactose and decreasing it on fructose. Interestingly, performance equalization emerged across replicate populations through distinct resource-transition strategies, indicated by differences in resource affinity and growth recovery on fructose and galactose among strains isolated from the evolved populations. Our results show that temporal resource variation selects for variance-minimizing resource adaptations while adopting multiple resource transition strategies, illustrating how distinct modes of metabolic plasticity can yield convergent fitness outcomes.

evolutionary biology↗

The evolution of a condition-dependent mutation rate enhances evolvability

Empirical studies have demonstrated that mutation rates may change with individual condition, such as in the case of stress-induced mutagenesis. This has led to the hypothesis that condition-dependent (or "plastic") mutation rates could be selectively favoured, as the increased production of new mutants in times of maladaptation enhances evolvability, the ability to undergo adaptive evolution. However, while empirical evidence for condition-dependent mutation rates is accumulating, theoretical models studying their evolution are lacking. Here, we employ an individual-based simulation approach to examine the evolution of condition-dependent mutation rates in a changing environment. We find that condition-dependent mutation rates consistently evolve when the environment changes at an intermediate pace. Furthermore, populations with condition-dependent mutation rates are substantially better adapted to their (changing) environment. Finally, the evolutionary dynamics of condition-dependent mutation rates are both accelerated and destabilised when the mutation rate is self-referential (i.e., when mutator loci affect their own mutation rate). We conclude that condition-dependent mutation rates (and thus evolvability) can readily evolve in changing environments. Significance statementMutation provides the raw material for evolution. Mutation rates thus tune evolvability, the ability to undergo adaptive evolution: if mutation rates are too low, evolution is impeded; if mutation rates are too high, adaptive traits cannot be maintained. Using a theoretical model, we explore the evolution of plastic mutation rates that systematically depend on the condition of the organism and its environment. An example is stress-induced mutagenesis in bacteria, which is implicated in the evolution of antibiotic resistance. We show that plastic mutation rates readily evolve, providing "well-timed" variation specifically when organisms are poorly adapted. Such plastic mutation rates thus facilitate better adaptation to changing environments, and their evolution provides an example of evolvability itself evolving.

evolutionary biology↗

Migration load, competition, and metabolic trade-offs shape spatial divergence through eco-evolutionary dynamics

Evolutionary models predict that trade-offs related to resource utilization promote local specialization and diversification in spatially heterogeneous environments. However, diversification is also influenced by ecological feedback mechanisms - such as frequency-dependent resource use - and their interaction with migration. To investigate how spatial variation affects diversification, we conducted an evolution experiment exposing populations of Lactococcus cremoris to divergent selection on two carbon sources: fructose and galactose. Using a continuous culture system, we partitioned these resources into two isolated patches (allopatry), two patches with constant migration between them (parapatry), and one fully-mixed patch (sympatry). Resource specialization and subsequent phenotypic diversification evolved in all treatments, revealing a metabolic trade-off between fructose and galactose utilization. Compared to treatments without migration, spatial variation produced a distinctive temporal pattern: migration initially delayed specialization on galactose but later accelerated it. This temporal pattern emerged from eco-evolutionary feedbacks operating through two mechanisms: (i) early in the experiment, higher population density in the better-suited fructose patch increased the influx of maladapted immigrants into the galactose patch, slowing local adaptation; however, (ii) as strains adapted locally to galactose, population density increased in the galactose patch and density asymmetries weakened. Simultaneously, the competitive ability of immigrants declined as residents became increasingly specialized in their local resources, progressively reducing the effective migration rate and allowing accelerated divergence. Our experiment demonstrates how the likelihood and tempo of spatial divergence depend on the evolvability of phenotypic trade-offs and their dynamic interaction with migration load and population density.

ecology↗

Community context influences the conjugation efficiency of E. coli

In urinary tract infections different bacteria can live in a polymicrobial community, it is unknown how such community members affect the conjugation rate of uropathogenic Escherichia coli. We investigated the influence of the polymicrobial urinary tract infection (UTI) community context on the conjugation rate of E. coli isolates in artificial urine medium. Pairwise conjugation rate experiments were conducted between a donor E. coli strain containing pOXA-48 and six uropathogenic E. coli isolates in the presence and absence of five community members to elucidate their effect on the rate of conjugation. We found that the basal conjugation rates in the absence of community members are genotype dependent. Interestingly, bacterial interactions have an overall positive effect on E. coli conjugation rates. Particularly Gram-positive enterococcal species were found to enhance the conjugation rates of most uropathogenic E. coli isolates. We hypothesize that the nature and co-culture of the interactions is important for these increased conjugation rates in AUM.

ecology↗

Quorum sensing as a mechanism to harness the wisdom of the crowds

Bacteria release and sense small molecules called autoinducers (AIs) in a process known as quorum sensing (QS). The prevailing interpretation of QS is that by sensing AI concentrations, bacteria estimate population density to regulate the expression of functions that are only beneficial when carried out by a sufficiently large number of cells. However, a major challenge to this interpretation is that the concentration of AIs strongly depends on the environment, often rendering AI-based estimates of cell density unreliable. Here we propose an alternative interpretation of QS, where bacteria, by releasing and sensing AIs, harness social interactions to sense the environment as a collective. As shown by a model, this functionality can explain the evolution of QS, and results from individuals improving their estimation accuracy by pooling many imperfect estimates - analogous to the wisdom of the crowds in decision theory. Importantly, our model reconciles the observed dependence of QS on both population density and the environment and explains why several QS systems regulate the production of private goods.

microbiology↗

Selection for rapid uptake of scarce or fluctuating resource explains vulnerability of glycolysis to imbalance

Glycolysis is a conserved central pathway in energy metabolism that converts glucose to pyruvate with net production of two ATP molecules. Because ATP is produced only in the lower part of glycolysis (LG), preceded by an initial investment of ATP in the upper glycolysis (UG), achieving robust start-up of the pathway upon activation presents a challenge: a sudden increase in glucose concentration can throw a cell into a self-sustaining imbalanced state in which UG outpaces LG, glycolytic intermediates accumulate and the cell is unable to maintain high ATP concentration needed to support cellular functions. Such metabolic imbalance can result in "substrate-accelerated death", a phenomenon observed in prokaryotes and eukaryotes when cells are exposed to an excess of substrate that previously limited growth. Here, we address why evolution has apparently not eliminated such a costly vulnerability and propose that it is a manifestation of an evolutionary trade-off, whereby the glycolysis pathway is adapted to quickly secure scarce or fluctuating resource at the expense of vulnerability in an environment with ample resource. To corroborate this idea, we perform evolutionary simulations of a simplified yeast glycolysis pathway consisting of UG, LG, phosphate transport between a vacuole and a cytosol, and a general ATP demand reaction. The pathway is evolved in constant or fluctuating resource environments by allowing mutations that affect the (maximum) reaction rate constants, reflecting changing expression levels of different glycolytic enzymes. We demonstrate that under limited constant resource, the population evolves to a genotype that is balanced but exhibits strongly imbalanced dynamics under ample resource conditions. Furthermore, when resource availability is fluctuating, the imbalanced phenotype enjoys a fitness advantage over balanced dynamics: when glucose is abundant, imbalanced pathways can quickly accumulate glycolytic intermediate FBP as intracellular storage that is used during periods of starvation to maintain high ATP concentration needed for growth. Our model further predicts that in environments with fluctuating resource, competition for glucose can result in stable coexistence of balanced and imbalanced cells, as well as repeated cycles of population crashes and recoveries that depend on such polymorphism. Overall, we demonstrate the importance of ecological and evolutionary arguments for understanding seemingly maladaptive aspects of cellular metabolism.

systems biology↗