Adaptive evolution of hybrid bacteria by horizontal gene transfer

Abstract

Horizontal gene transfer (HGT) is an important factor in bacterial evolution that can act across species boundaries. Yet, we know little about rate and genomic targets of cross-lineage gene transfer and about its effects on the recipient organism's physiology and fitness. Here, we address these questions in a parallel evolution experiment with two Bacillus subtilis lineages of 7% sequence divergence. We observe rapid evolution of hybrid organisms: gene transfer swaps ∼12% of the core genome in just 200 generations, and 60% of core genes are replaced in at least one population. By genomics, transcriptomics, fitness assays, and statistical modeling, we show that transfer generates adaptive evolution and functional alterations in hybrids. Specifically, our experiments reveal a strong, repeatable fitness increase of evolved populations in the stationary growth phase. By genomic analysis of the transfer statistics across replicate populations, we infer that selection on HGT has a broad genetic basis: 40% of the observed transfers are adaptive. At the level of functional gene networks, we find signatures of negative, positive, and epistatic selection, consistent with hybrid incompatibilities and adaptive evolution of network functions. Our results suggest that gene transfer navigates a complex cross-lineage fitness landscape, bridging epistatic barriers along multiple high-fitness paths.

Revisiting Antibiotic Resistance: Mechanistic Foundations to Evolutionary Outlook

“…Previously, HGT was proposed to occur in only some bacteria. However, whole-genome sequencing in various species has confirmed the pervasiveness and the dominant role of this mechanism over spontaneous mutations in bacterial evolution [ 128 , 129 ]. It is estimated that at least 60% of prokaryotic genes have undergone HGT [ 130 ].…”

“…Among various mechanisms of HGT, the acquisition of multidrug resistance through recombination—i.e., natural transformation—could bring more evolutionary benefits to the bacterial populations [ 132 , 133 , 134 ]. First, recombination can integrate single or multiple DNA fragments into the recipient’s chromosomes [ 128 , 135 ]. This process increases genetic variation in the populations and thus potentiates the adaptation to further environmental changes [ 131 ].…”

Microbial adaptive evolution

“…Demonstrating that horizontal gene transfer can promote fitness, Power et al co-cultured two B. subtilis strains that had 7% DNA sequence difference over multiple rounds of growth and stationary phase (Power et al, 2021 ). They observed the rapid emergence of hybrid organisms with gene transfer swaps of approximately 12% of the core genome in just 200 generations and 60% of core genes replaced in at least one population.…”

Insight into the antibacterial resistance of graphdiyne functionalized by silver nanoparticles

“…These antimicrobials combat bacteria by interacting with special intracellular targets via chemical ways, which easily induce the resistance in bacteria 4 . What is worse, the horizontal gene transfer between bacteria can further accelerate the propagation of resistance, causing the novel antibiotics quickly to fail 5,6 . Therefore, there is an urgent need to develop novel alternatives to combat the growing menace of pathogenic bacteria.…”