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

David S. Milner, Victoria Attah, Emily Cook, Finlay Maguire, Fiona R. Savory, Mark Morrison, Carolin A. Müller, Peter G. Foster, Nicholas J. Talbot, Guy Leonard, Thomas A. Richards

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Abstract

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 in Saccharomyces 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 of S. 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.
Original languageEnglish
Pages (from-to)5613-5622
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America (PNAS)
Volume116
Issue number12
Early online date6 Mar 2019
DOIs
Publication statusPublished - 19 Mar 2019

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