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.
Highlights
Comparative genomics is a powerful tool for discovering links between phenotypes and genotypes within an evolutionary framework
Our results suggest that the evolution of fructophily may have been part of a process of adaptation to sugar-rich environments, which included a profound remodeling of alcoholic fermentation involving the acquisition of bacterial alcohol dehydrogenases, which turned out to be important for glucose metabolism, and an invertase, which is essential for sucrose assimilation
We previously reported the acquisition of a high-capacity fructose transporter (Ffz1) through horizontal gene transfers (HGT) by the most recent common ancestor (MRCA) of W/S-clade species
Summary
Comparative genomics is a powerful tool for discovering links between phenotypes and genotypes within an evolutionary framework. Available evidence suggests that HGTs are often associated with rapid adaptation to new environments (Cheeseman et al, 2014; Gojkovicet al., 2004; Qiu et al, 2013; Richards et al, 2011; Richards and Talbot, 2013) In line with these findings, we recently reported on the evolutionary history of a unique, highcapacity, specific fructose transporter, Ffz, which is intimately associated with fructophilic metabolism in ascomycetous budding yeasts (subphylum Saccharomycotina) (Goncalves et al, 2016). Fructophily in lactic acid bacteria seems to be linked to redox homeostasis (Endo et al, 2014) In yeasts, it is still unclear how preferential consumption of fructose may be beneficial, partly because unlike fructophilic bacteria, fructophilic yeasts grow vigorously on glucose when it is the only carbon and energy source available (Sousa-Dias et al, 1996; Tofalo et al, 2012). We found a surge of bacterial-derived HGT events in the W/S clade when compared with other lineages in the Saccharomycotina (Marcet-Houben and Gabaldon, 2010), many of which seem to impact redox homeostasis
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