Dissecting an ancient stress resistance trait syndrome in the compost yeastKluyveromyces marxianus

Abstract

AbstractIn the search to understand how evolution builds new traits, ancient events are often the hardest to dissect. Species-unique traits pose a particular challenge for geneticists—cases in which a character arose long ago and, in the modern day, is conserved within a species, distinguishing it from reproductively isolated relatives. In this work, we have developed the budding yeast genusKluyveromycesas a model for mechanistic dissection of trait variation across species boundaries. Phenotypic profiling revealed robust heat and chemical-stress tolerance phenotypes that distinguished the compost yeastK. marxianusfrom the rest of the clade. We used culture-based, transcriptomic, and genetic approaches to characterize the metabolic requirements of theK. marxianustrait syndrome. We then generated a population-genomic resource forK. marxianusand harnessed it in molecular-evolution analyses, which found hundreds of housekeeping genes with evidence for adaptive protein variation unique to this species. Our data support a model in which, in the distant past,K. marxianusunderwent a vastly complex remodeling of its proteome to achieve stress resistance. Such a polygenic architecture, involving nucleotide-level allelic variation on a massive scale, is consistent with theoretical models of the mechanisms of long-term adaptation, and suggests principles of broad relevance for interspecies trait genetics.