Adaptive evolution of hybrid bacteria by horizontal gene transfer

Abstract

9Horizontal gene transfer is an important factor in bacterial evolution that can act across 10 species boundaries. Yet, we know little about rate and genomic targets of cross-lineage 11 gene transfer, and about its effects on the recipient organism's physiology and fitness. 12Here, we address these questions in a parallel evolution experiment with two Bacillus 13 subtilis lineages of 7% sequence divergence. We observe rapid evolution of hybrid 14 organisms: gene transfer swaps ~12% of the core genome in just 200 generations, and 15 60% of core genes are replaced in at least one population. By genomics, transcriptomics, 16fitness assays, and statistical modeling, we show that transfer generates adaptive evolution 17 and functional alterations in hybrids. Specifically, our experiments reveal a strong, 18repeatable fitness increase of evolved populations in the stationary growth phase. By 19 genomic analysis of the transfer statistics across replicate populations, we infer that 20 selection on HGT has a broad genetic basis: 40% of the observed transfers are adaptive. 21At the level of functional gene networks, we find signatures of negative and positive 22 selection, consistent with hybrid incompatibilities and adaptive evolution of network 23 functions. Our results suggest that gene transfer navigates a complex cross-lineage fitness 24 landscape, bridging epistatic barriers along multiple high-fitness paths. 25 26 Significance statement 27In a parallel evolution experiment, we probe lateral gene transfer between two Bacillus subtilis 28 lineages close to the species boundary. We show that laboratory evolution by horizontal gene 29 transfer can rapidly generate hybrid organisms with broad genomic and functional alterations. 30By combining genomics, transcriptomics, fitness assays and statistical modeling, we map the 31 selective effects underlying gene transfer. We show that transfer takes place under genome-32 wide positive and negative selection, generating a net fitness increase in hybrids. The 33 evolutionary dynamics efficiently navigates this fitness landscape, finding viable paths with 34 increasing fraction of transferred genes. 35 36

Whole genome phylogenies reflect the distributions of recombination rates for many bacterial species

“…Just natural selection acts on mutations and thereby shapes the observed patterns of substitutions, selection also undoubtedly strongly acts on recombination events and shapes the recombination patterns that we detect in the core genome alignments. Indeed, strong selection on horizontal transfer events between two B. subtilis strains was recently observed in a laboratory evolution experiment ( Power et al, 2020 ). However, it is currently not clear to what extent the differences in observed recombination rates are shaped mainly by natural selection, for example that due to epistatic interactions only recombinant segments from other strains with similar ‘ecotypes’ are not removed by purifying selection, as suggested by some previous works ( Shapiro et al, 2012 ; Cadillo-Quiroz et al, 2012 ), or that recombination rates may be set mostly by which lineages co-occur at the same geographical location.…”

“…Just natural selection acts on mutations and thereby shapes the observed patterns of substitutions, selection also undoubtedly strongly acts on recombination events and shapes the recombination patterns that we detect in the core genome alignments. Indeed, strong selection on horizontal transfer events between two B. subtilis strains was recently observed in a laboratory evolution experiment (Power et al, 2020). However, it is currently not clear to what extent the differences in observed recombination rates are shaped mainly by natural selection, e.g.…”

The DNA transporter ComEC has metal‐dependent nuclease activity that is important for natural transformation

“…Transformation allows bacteria to acquire adaptively useful genes, to operate a distributed gene pool, and to remove parasitic mobile genetic elements from their genomes (Carvalho et al, 2020;Croucher et al, 2016;Power et al, 2021). In pathogenic bacteria, natural transformation is important for the spread of virulence traits including capsule variation and antibiotic resistance (Chi et al, 2007;Croucher et al, 2011;Domingues et al, 2012;Griffith, 1928).…”