Evolutionary crowdsourcing: alignment of fitness landscapes allows cross-species adaptation of a horizontally transferred gene

Abstract

Genes that undergo horizontal gene transfer (HGT) evolve in different genomic backgrounds as they move between hosts, in contrast to genes that evolve under strict vertical inheritance. Despite the ubiquity of HGT in microbial communities, the effects of host-switching on gene evolution have been understudied. Here, we present a novel framework to examine the consequences of host-switching on gene evolution by probing the existence and form of host-dependent mutational effects. We started exploring the effects of HGT on gene evolution by focusing on an antibiotic resistance gene (encoding a beta-lactamase) commonly found on conjugative plasmids in Enterobacteriaceae pathogens. By reconstructing the resistance landscape for a small set of mutationally connected alleles in three enteric species (Escherichia coli, Salmonella enterica, and Klebsiella pneumoniae), we uncovered that the landscape topographies were largely aligned with very low levels of host-dependent mutational effects. By simulating gene evolution with and without HGT using the species-specific empirical landscapes, we found that evolutionary outcomes were similar despite HGT. These findings suggest that the adaptive evolution of a mobile gene in one species can translate to adaptation in another species. In such a case, vehicles of cross-species HGT such as plasmids enable a distributed form of genetic evolution across a bacterial community, where species can crowdsource adaptation from other community members. The role of evolutionary crowdsourcing on the evolution of bacteria merits further investigation.

Adaptive and pleiotropic effects of evolution in synonymous sugar environments

“…al. reported that shifting hosts may aid adaptation of a gene, which are blocked due to epistatic interactions in the native host 40 . Our results point at similar roadblocks to adaptation posed by the environment, and indicate how minute changes in the environment can help overcome them.…”

Visualizing and quantifying structural diversity around mobile resistance genes

“…First, nucleotide-level variation in the mobile gene itself does indeed appear to be a 'slow' molecular clock compared to the much faster rates of rearrangements in flanking regions. Even single SNVs can change the hydrolytic profile of betalactamases, for example in the well-studied evolution of bla TEM-1 [21,22], including specifically while on MGEs [23,24], so this variation should not generally be taken as a neutral clock. However, this nevertheless suggests a quantitative connection between mutational and non-mutational evolution that could be fruitful for further exploration.…”