Abstract
Predator impacts on prey diversity are often studied among higher organisms over short periods, but microbial predator-prey systems allow examination of prey-diversity dynamics over evolutionary timescales. We previously showed that Escherichia coli commonly evolved minority mucoid phenotypes in response to predation by the bacterial predator Myxococcus xanthus by one time point of a coevolution experiment now named MyxoEE-6. Here we examine mucoid frequencies across several MyxoEE-6 timepoints to discriminate between the hypotheses that mucoids were increasing to fixation, stabilizing around equilibrium frequencies, or heading to loss toward the end of MyxoEE-6. In four focal coevolved prey populations, mucoids rose rapidly early in the experiment and then fluctuated within detectable minority frequency ranges through the end of MyxoEE-6, generating frequency dynamics suggestive of negative frequency-dependent selection. However, a competition experiment between mucoid and non-mucoid clones found a predation-specific advantage of the mucoid clone that was insensitive to frequency over the examined range, leaving the mechanism that maintains minority mucoidy unresolved. The advantage of mucoidy under predation was found to be associated with reduced population size after growth (productivity) in the absence of predators, suggesting a tradeoff between productivity and resistance to predation that we hypothesize may reverse mucoid vs non-mucoid fitness ranks within each MyxoEE-6 cycle. We also found that mucoidy was associated with diverse colony phenotypes and diverse candidate mutations primarily localized in the exopolysaccharide operon yjbEFGH. Collectively, our results show that selection from predatory bacteria can generate apparently stable sympatric phenotypic polymorphisms within coevolving prey populations and also allopatric diversity across populations by selecting for diverse mutations and colony phenotypes associated with mucoidy. More broadly, our results suggest that myxobacterial predation increases long-term diversity within natural microbial communities.
Highlights
IntroductionPrey face the dual challenges of optimizing their own acquisition and use of resources for growth and reproduction while avoiding being killed or injured by predators
Predation is one of the most common forms of inter-specific antagonism [1]
In a predator-prey coevolution experiment with Escherichia coli as prey and the myxobacterium Myxococcus xanthus as predator recently named MyxoEE-6 [22], we previously showed that coevolving prey were under selection both for parallel losses of function in a prey outer-membrane protein (OmpT) and favoring the increase of genotypes that generate a mucoid-colony phenotype [23]
Summary
Prey face the dual challenges of optimizing their own acquisition and use of resources for growth and reproduction while avoiding being killed or injured by predators This dilemma has been shown to play an important role in the ecology and evolution of diverse prey species, including among plants [2], animals [3] and microorganisms [4]. Several studies have shown that over short time periods, microbial predators can elicit phenotypic responses providing resistance against predatory killing. These include filamentation [10], biofilm formation [11], sporulation [12] and production of various extracellular compounds [13] (reviewed in detail in [14]).
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