Fast eco-evolutionary changes in bacterial genomes after anthropogenic perturbation

Anthropogenic perturbations such as water overexploitation introduce novel selective pressures to the natural environments, impacting on the genomic variability of organisms and thus altering the evolutionary trajectory of its populations. Bad agricultural practices and defective policies in Cuatro Cienegas, Coahuila, Mexico, have strongly impacted its water reservoir, pushing entire hydrological systems to the brink of extinction together with their native populations. Here, we studied the effects of continuous water overexploitation on an environmental aquatic lineage of Pseudomonas otitidis , inhabitant to a particularly affected lagoon of an exhaustively studied system in the middle of the desert, over a 13 year period which encompasses three desiccation events. By comparing the genomes of a population sample from 2003 (original state) and 2015 (perturbed state), we analyzed the demographic history and evolutionary response of this bacterial lineage to the perturbation. Through coalescent simulations, we obtained a demographic model of contraction-expansion-contraction which, alongside an increment in mean Tajima’s D and recombination rate, loss of genetic and nucleotidic variation and a single amino acid under positive selection, points the occurrence of an evolutionary rescue event, possibly potentiated by horizontal gene transfer, where the population nearly went extinct during the first desiccation event but sharply recovered in the second and adapted to its new environment. Furthermore, the gain of phosphorylation, DNA recombination and small-molecule metabolism and loss of biosynthetic and regulation genes on the exclusive accessory genome suggest a functional shift to a more generalist scavenger lifestyle in an environment that went from oligotrophic to nutrient-rich.