Localized coevolution between microbial predator and prey alters community-wide gene expression and ecosystem function.

Closely interacting microbial species pairs (e.g., predator and prey) can become coadapted via reciprocal natural selection. A fundamental challenge in evolutionary ecology is to untangle how coevolution in small species groups affects and is affected by biotic interactions in diverse communities. We conducted an experiment with a synthetic 30-species bacterial community where we experimentally manipulated the coevolutionary history of a ciliate predator and one bacterial prey species from the community. Altering the coevolutionary history of the focal prey species had little effect on community structure or carrying capacity in the presence or absence of the coevolved predator. However, community metabolic potential (represented by per-cell ATP concentration) was significantly higher in the presence of both the coevolved focal predator and prey. This ecosystem-level response was mirrored by community-wide transcriptional shifts that resulted in the differential regulation of nutrient acquisition and surface colonization pathways across multiple bacterial species. Our findings show that the disruption of localized coevolution between species pairs can reverberate through community-wide transcriptional networks even while community composition remains largely unchanged. We propose that these altered expression patterns may signal forthcoming evolutionary and ecological change.

Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network.

Mobile genetic elements such as conjugative plasmids are responsible for antibiotic resistance phenotypes in many bacterial pathogens. The ability to conjugate, the presence of antibiotics, and ecological interactions all have a notable role in the persistence of plasmids in bacterial populations. Here, we set out to investigate the contribution of these factors when the conjugation network was disturbed by a plasmid-dependent bacteriophage. Phage alone effectively caused the population to lose plasmids, thus rendering them susceptible to antibiotics. Leakiness of the antibiotic resistance mechanism allowing Black Queen evolution (i.e. a "race to the bottom") was a more significant factor than the antibiotic concentration (lethal vs sublethal) in determining plasmid prevalence. Interestingly, plasmid loss was also prevented by protozoan predation. These results show that outcomes of attempts to resensitize bacterial communities by disrupting the conjugation network are highly dependent on ecological factors and resistance mechanisms. IMPORTANCE Bacterial antibiotic resistance is often a part of mobile genetic elements that move from one bacterium to another. By interfering with the horizontal movement and the maintenance of these elements, it is possible to remove the resistance from the population. Here, we show that a so-called plasmid-dependent bacteriophage causes the initially resistant bacterial population to become susceptible to antibiotics. However, this effect is efficiently countered when the system also contains a predator that feeds on bacteria. Moreover, when the environment contains antibiotics, the survival of resistance is dependent on the resistance mechanism. When bacteria can help their contemporaries to degrade antibiotics, resistance is maintained by only a fraction of the community. On the other hand, when bacteria cannot help others, then all bacteria remain resistant. The concentration of the antibiotic played a less notable role than the antibiotic used. This report shows that the survival of antibiotic resistance in bacterial communities represents a complex process where many factors present in real-life systems define whether or not resistance is actually lost.