Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage

Elife. 2018 Apr 12:7:e33034. doi: 10.7554/eLife.33034.

Abstract

Fructophily is a rare trait that consists of the preference for fructose over other carbon sources. Here, we show that in a yeast lineage (the Wickerhamiella/Starmerella, W/S clade) comprised of fructophilic species thriving in the high-sugar floral niche, the acquisition of fructophily is concurrent with a wider remodeling of central carbon metabolism. Coupling comparative genomics with biochemical and genetic approaches, we gathered ample evidence for the loss of alcoholic fermentation in an ancestor of the W/S clade and subsequent reinstatement through either horizontal acquisition of homologous bacterial genes or modification of a pre-existing yeast gene. An enzyme required for sucrose assimilation was also acquired from bacteria, suggesting that the genetic novelties identified in the W/S clade may be related to adaptation to the high-sugar environment. This work shows how even central carbon metabolism can be remodeled by a surge of HGT events.

Keywords: Starmerella; alcoholic fermentation; evolutionary biology; floral niche; fructophilic yeasts; genomics; horizontal gene transfer; sugar metabolism.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Biological Evolution*
  • Ethanol / metabolism*
  • Fermentation*
  • Fructose / metabolism*
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Gene Transfer, Horizontal*
  • Genome, Fungal
  • Glucose
  • Phylogeny
  • Saccharomycetales / genetics
  • Saccharomycetales / growth & development
  • Saccharomycetales / metabolism*

Substances

  • Bacterial Proteins
  • Fungal Proteins
  • Fructose
  • Ethanol
  • Glucose