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.
Bacterial transformation, a common mechanism of horizontal gene transfer, can speed up adaptive evolution. How its costs and benefits depend on the growth environment is poorly understood. Here, we characterize the distributions of fitness effects (DFE) of transformation in different conditions and test whether they predict in which condition transformation is beneficial. To determine the DFEs, we generate hybrid libraries between the recipient Bacillus subtilis and different donor species and measure the selection coefficient of each hybrid strain. In complex medium, the donor Bacillus vallismortis confers larger fitness effects than the more closely related donor Bacillus spizizenii. For both donors, the DFEs show strong effect beneficial transfers, indicating potential for fast adaptive evolution. While some transfers of B. vallismortis DNA show pleiotropic effects, various transfers are beneficial only under a single growth condition, indicating that the recipient can benefit from a variety of donor genes to adapt to varying growth conditions. We scrutinize the predictive value of the DFEs by laboratory evolution under different growth conditions and show that the DFEs correctly predict the condition at which transformation confers a benefit. We conclude that transformation has a strong potential for speeding up adaptation to varying environments by profiting from a gene pool shared between closely related species.
Bacterial type 4 pili (T4P) are extracellular polymers that serve both as adhesins and molecular motors. Functionally, they are involved in adhesion, colony formation, twitching motility, and horizontal gene transfer. T4P of the human pathogen Neisseria gonorrhoeae have been shown to enhance survivability under treatment with antibiotics or hydrogen peroxide. However, little is known about the effect of external stresses on T4P production and motor properties. Here, we address this question by directly visualizing gonococcal T4P dynamics. We show that in the absence of stress gonococci produce T4P at a remarkably high rate of ∼200 T4P min–1. T4P retraction succeeds elongation without detectable time delay. Treatment with azithromycin or ceftriaxone reduces the T4P production rate. RNA sequencing results suggest that reduced piliation is caused by combined downregulation of the complexes required for T4P extrusion from the cell envelope and cellular energy depletion. Various other stresses including inhibitors of cell wall synthesis and DNA replication, as well as hydrogen peroxide and lactic acid, inhibit T4P production. Moreover, hydrogen peroxide and acidic pH strongly affect pilus length and motor function. In summary, we show that gonococcal T4P are highly dynamic and diverse external stresses reduce piliation despite the protective effect of T4P against some of these stresses.
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
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