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

Research output: Contribution to journalArticlepeer-review

32 Citations (Scopus)

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
Volume116
Issue number12
DOIs
Publication statusPublished - 2019

Bibliographical note

Funding Information:
cil Grant BB/N016858/1; and T.A.R. is supported by a Royal Society University Research Fellowship (UF130382). This work is supported mainly by funding from a Philip Leverhulme award from the Leverhulme Trust (PLP-2014-147), with additional support from The Gordon and Betty Moore Foundation (Grant GBMF5514). The University of Exeter OmniLog system and associated operations were supported by a Wellcome Trust Institutional Strategic Support Award WT105618MA.

Funding Information:
ACKNOWLEDGMENTS. We thank Prof. Eckhard Boles for the gift of the Saccharomyces cerevisiae EBY.VW4000 strain; Dr. Cat Gadelha for the p426 GPD sfGFP vector; Prof. Ken Haynes’ laboratory for the S. cerevisiae BY4742 strain and reagents for transformations/Western blots; Dr. Varun Varma for his advice on statistical analyses; and Emma Chapman for her technical assistance. F.M. is supported by a Genome Canada fellowship; C.A.M. is supported by Biotechnology and Biological Sciences Research Coun-

Publisher Copyright:
© 2019 National Academy of Sciences. All Rights Reserved.

ASJC Scopus Subject Areas

  • General

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't

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