Experimental determination of evolutionary barriers to horizontal gene transfer
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RESEARCH ARTICLE
Open Access
Experimental determination of evolutionary barriers to horizontal gene transfer Hande Acar Kirit1,2, Mato Lagator3 and Jonathan P. Bollback1*
Abstract Background: Horizontal gene transfer, the acquisition of genes across species boundaries, is a major source of novel phenotypes that enables microbes to rapidly adapt to new environments. How the transferred gene alters the growth – fitness – of the new host affects the success of the horizontal gene transfer event and how rapidly the gene spreads in the population. Several selective barriers – factors that impact the fitness effect of the transferred gene – have been suggested to impede the likelihood of horizontal transmission, however experimental evidence is scarce. The objective of this study was to determine the fitness effects of orthologous genes transferred from Salmonella enterica serovar Typhimurium to Escherichia coli to identify the selective barriers using highly precise experimental measurements. Results: We found that most gene transfers result in strong fitness costs. Previously identified evolutionary barriers — gene function and the number of protein-protein interactions — did not predict the fitness effects of transferred genes. In contrast, dosage sensitivity, gene length, and the intrinsic protein disorder significantly impact the likelihood of a successful horizontal transfer. Conclusion: While computational approaches have been successful in describing long-term barriers to horizontal gene transfer, our experimental results identified previously underappreciated barriers that determine the fitness effects of newly transferred genes, and hence their short-term eco-evolutionary dynamics. Keywords: Horizontal gene transfer, Evolutionary barriers, Gene length, Dosage sensitivity, Distribution of fitness effects
Background Horizontal gene transfer (HGT) is the lateral transfer of genetic material between different individuals and species, and a major driver of evolution in all domains of microbial life [1–3]. HGT has contributed to a stunning array of phenotypic diversity that we observe in nature. As a source of phenotypic novelty, HGT differs from de novo mutations as new adaptive phenotypes can appear faster and sweep through the populations more rapidly, as demonstrated by the mannanase gene of the coffee * Correspondence: [email protected] 1 Institute of Integrative Biology, Functional and Comparative Genomics, University of Liverpool, Liverpool L69 7ZB, UK Full list of author information is available at the end of the article
berry borer beetle, Hypothenemus hampei, which was acquired from bacteria and enabled the beetle to digest the complex sugars in coffee beans, thus turning the beetle into an industrially relevant pest [4]. Similarly, the horizontal acquisition of vancomycin resistance by Staphylococcus aureus [5] and virulence factors by Escherichia coli O104:H4 in the 2011 European outbreak [6] are serious public health concerns. Despite the importance of HGT, we still have a limited understandi
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