scholarly journals Adaptive evolution of hybrid bacteria by horizontal gene transfer

2020 ◽  
Author(s):  
Jeffrey J. Power ◽  
Fernanda Pinheiro ◽  
Simone Pompei ◽  
Viera Kovacova ◽  
Melih Yüksel ◽  
...  
Keyword(s):  
Bacillus Subtilis ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Statistical Modeling ◽  
Adaptive Evolution ◽  
Gene Networks ◽  
Evolutionary Dynamics ◽  
Fitness Landscape ◽  
Parallel Evolution ◽  
Evolution Experiment

AbstractHorizontal gene transfer 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 and positive 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.Significance statementIn a parallel evolution experiment, we probe lateral gene transfer between two Bacillus subtilis lineages close to the species boundary. We show that laboratory evolution by horizontal gene transfer can rapidly generate hybrid organisms with broad genomic and functional alterations. By combining genomics, transcriptomics, fitness assays and statistical modeling, we map the selective effects underlying gene transfer. We show that transfer takes place under genome-wide positive and negative selection, generating a net fitness increase in hybrids. The evolutionary dynamics efficiently navigates this fitness landscape, finding viable paths with increasing fraction of transferred genes.

scholarly journals Adaptive evolution of hybrid bacteria by horizontal gene transfer

2021 ◽  
Vol 118 (10) ◽  
pp. e2007873118
Author(s):  
Jeffrey J. Power ◽  
Fernanda Pinheiro ◽  
Simone Pompei ◽  
Viera Kovacova ◽  
Melih Yüksel ◽  
...  
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Adaptive Evolution ◽  
Gene Networks ◽  
Fitness Landscape ◽  
Parallel Evolution ◽  
Rapid Evolution ◽  
Sequence Divergence ◽  
Genomic Analysis ◽  
Stationary Growth Phase

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.

scholarly journals Experimental Evolution of Bacillus subtilis Reveals the Evolutionary Dynamics of Horizontal Gene Transfer and Suggests Adaptive and Neutral Effects

Genetics ◽  
2020 ◽  
Vol 216 (2) ◽  
pp. 543-558
Author(s):  
Shai Slomka ◽  
Itamar Françoise ◽  
Gil Hornung ◽  
Omer Asraf ◽  
Tammy Biniashvili ◽  
...  
Keyword(s):  
Bacillus Subtilis ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Evolutionary Dynamics ◽  
De Novo ◽  
Growth Yield ◽  
Genomic Variation ◽  
Bacterial Populations ◽  
Flagellar Proteins ◽  
Foreign Dna

Tracing evolutionary processes that lead to fixation of genomic variation in wild bacterial populations is a prime challenge in molecular evolution. In particular, the relative contribution of horizontal gene transfer (HGT) vs.de novo mutations during adaptation to a new environment is poorly understood. To gain a better understanding of the dynamics of HGT and its effect on adaptation, we subjected several populations of competent Bacillus subtilis to a serial dilution evolution on a high-salt-containing medium, either with or without foreign DNA from diverse pre-adapted or naturally salt tolerant species. Following 504 generations of evolution, all populations improved growth yield on the medium. Sequencing of evolved populations revealed extensive acquisition of foreign DNA from close Bacillus donors but not from more remote donors. HGT occurred in bursts, whereby a single bacterial cell appears to have acquired dozens of fragments at once. In the largest burst, close to 2% of the genome has been replaced by HGT. Acquired segments tend to be clustered in integration hotspots. Other than HGT, genomes also acquired spontaneous mutations. Many of these mutations occurred within, and seem to alter, the sequence of flagellar proteins. Finally, we show that, while some HGT fragments could be neutral, others are adaptive and accelerate evolution.

scholarly journals Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Polonca Stefanic ◽  
Katarina Belcijan ◽  
Barbara Kraigher ◽  
Rok Kostanjšek ◽  
Joseph Nesme ◽  
...  
Keyword(s):  
Bacillus Subtilis ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Social Interactions ◽  
Recipient Strain ◽  
Donor Strain ◽  
Kin Discrimination ◽  
Defence Mechanisms ◽  
Donor Cells ◽  
Novel Alleles

AbstractBacillus subtilis is a soil bacterium that is competent for natural transformation. Genetically distinct B. subtilis swarms form a boundary upon encounter, resulting in killing of one of the strains. This process is mediated by a fast-evolving kin discrimination (KD) system consisting of cellular attack and defence mechanisms. Here, we show that these swarm antagonisms promote transformation-mediated horizontal gene transfer between strains of low relatedness. Gene transfer between interacting non-kin strains is largely unidirectional, from killed cells of the donor strain to surviving cells of the recipient strain. It is associated with activation of a stress response mediated by sigma factor SigW in the donor cells, and induction of competence in the recipient strain. More closely related strains, which in theory would experience more efficient recombination due to increased sequence homology, do not upregulate transformation upon encounter. This result indicates that social interactions can override mechanistic barriers to horizontal gene transfer. We hypothesize that KD-mediated competence in response to the encounter of distinct neighbouring strains could maximize the probability of efficient incorporation of novel alleles and genes that have proved to function in a genomically and ecologically similar context.

scholarly journals Horizontal Gene Transfer Clarifies Taxonomic Confusion and Promotes the Genetic Diversity and Pathogenicity of Plesiomonas shigelloides

mSystems ◽  
2020 ◽  
Vol 5 (5) ◽  
Author(s):  
Zhiqiu Yin ◽  
Si Zhang ◽  
Yi Wei ◽  
Meng Wang ◽  
Shuangshuang Ma ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Evolutionary Dynamics ◽  
Genomic Analysis ◽  
Comparative Genomic ◽  
Content Type ◽  
Pan Genome ◽  
Long Time ◽  
Taxonomic Confusion

The taxonomic position of P. shigelloides has been the subject of debate for a long time, and until now, the evolutionary dynamics and pathogenesis of P. shigelloides were unclear. In this study, pan-genome analysis indicated extensive genetic diversity and the presence of large and variable gene repertoires. Our results revealed that horizontal gene transfer was the focal driving force for the genetic diversity of the P. shigelloides pan-genome and might have contributed to the emergence of novel properties. Vibrionaceae and Aeromonadaceae were found to be the predominant donor taxa for horizontal genes, which might have caused the taxonomic confusion historically. Comparative genomic analysis revealed the potential of P. shigelloides to cause intestinal and invasive diseases. Our results could advance the understanding of the evolution and pathogenesis of P. shigelloides, particularly in elucidating the role of horizontal gene transfer and investigating virulence-related elements.

scholarly journals Long-term experimental evolution of HIV-1 reveals effects of environment and mutational history

PLoS Biology ◽  
2020 ◽  
Vol 18 (12) ◽  
pp. e3001010
Author(s):  
Eva Bons ◽  
Christine Leemann ◽  
Karin J. Metzner ◽  
Roland R. Regoes
Keyword(s):  
Evolutionary Dynamics ◽  
Fitness Landscape ◽  
Large Population ◽  
Parallel Evolution ◽  
Cell Types ◽  
Drug Pressure ◽  
Evolutionary Paths ◽  
The Impact ◽  
Hiv 1

An often-returning question for not only HIV-1, but also other organisms, is how predictable evolutionary paths are. The environment, mutational history, and random processes can all impact the exact evolutionary paths, but to which extent these factors contribute to the evolutionary dynamics of a particular system is an open question. Especially in a virus like HIV-1, with a large mutation rate and large population sizes, evolution is expected to be highly predictable if the impact of environment and history is low, and evolution is not neutral. We investigated the effect of environment and mutational history by analyzing sequences from a long-term evolution experiment, in which HIV-1 was passaged on 2 different cell types in 8 independent evolutionary lines and 8 derived lines, 4 of which involved a switch of the environment. The experiments lasted for 240–300 passages, corresponding to approximately 400–600 generations or almost 3 years. The sequences show signs of extensive parallel evolution—the majority of mutations that are shared between independent lines appear in both cell types, but we also find that both environment and mutational history significantly impact the evolutionary paths. We conclude that HIV-1 evolution is robust to small changes in the environment, similar to a transmission event in the absence of an immune response or drug pressure. We also find that the fitness landscape of HIV-1 is largely smooth, although we find some evidence for both positive and negative epistatic interactions between mutations.

scholarly journals Environment-dependent fitness gains can be driven by horizontal gene transfer of transporter-encoding genes

2019 ◽  
Vol 116 (12) ◽  
pp. 5613-5622 ◽  
Author(s):  
David S. Milner ◽  
Victoria Attah ◽  
Emily Cook ◽  
Finlay Maguire ◽  
Fiona R. Savory ◽  
...  
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Fitness Landscape ◽  
Single Gene ◽  
Transporter Gene ◽  
Metabolic Potential ◽  
Gene Acquisition ◽  
A Genome ◽  
Complex Polymers ◽  
Encoding Genes

Many microbes acquire metabolites in a “feeding” process where complex polymers are broken down in the environment to their subunits. The subsequent uptake of soluble metabolites by a cell, sometimes called osmotrophy, is facilitated by transporter proteins. As such, the diversification of osmotrophic microorganisms is closely tied to the diversification of transporter functions. Horizontal gene transfer (HGT) has been suggested to produce genetic variation that can lead to adaptation, allowing lineages to acquire traits and expand niche ranges. Transporter genes often encode single-gene phenotypes and tend to have low protein–protein interaction complexity and, as such, are potential candidates for HGT. Here we test the idea that HGT has underpinned the expansion of metabolic potential and substrate utilization via transfer of transporter-encoding genes. Using phylogenomics, we identify seven cases of transporter-gene HGT between fungal phyla, and investigate compatibility, localization, function, and fitness consequences when these genes are expressed inSaccharomyces cerevisiae. Using this approach, we demonstrate that the transporters identified can alter how fungi utilize a range of metabolites, including peptides, polyols, and sugars. We then show, for one model gene, that transporter gene acquisition by HGT can significantly alter the fitness landscape ofS. cerevisiae. We therefore provide evidence that transporter HGT occurs between fungi, alters how fungi can acquire metabolites, and can drive gain in fitness. We propose a “transporter-gene acquisition ratchet,” where transporter repertoires are continually augmented by duplication, HGT, and differential loss, collectively acting to overwrite, fine-tune, and diversify the complement of transporters present in a genome.

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