Performance, genomic rearrangements and signatures of adaptive
evolution: lessons from fermentative yeasts.
Abstract
The capacity of some yeasts to extract energy from single sugars,
generating CO2 and ethanol (=fermentation), even in the presence of
oxygen is known as the Crabtree effect. This phenomenon represents an
important adaptation as it allowed the utilization of the ecological
niche given by modern fruits, an abundant source of food that emerged in
the terrestrial environment in the Cretaceous. However, identifying the
evolutionary events that triggered fermentative capacity in Crabtree
positive species is challenging, as microorganisms do not leave fossil
evidence. Thus, key innovations should be inferred based only on traits
measured under culture conditions. Here, we reanalyzed data form a
common-garden experiment where several proxies of fermentative capacity
were recorded in Crabtree positive and negative species, representing
yeast’s phylogenetic diversity. In particular, we applied the
“lasso-OU” algorithm which detects points of adaptive shifts, provided
trait values representing a given performance measure. We tested whether
multiple events or a single event explains the actual fermentative
capacity of yeasts. According to the lasso-OU procedure, evolutionary
changes in the three proxies of fermentative capacity that we considered
(i.e., glycerol production, ethanol yield and respiratory quotient) are
consistent with a single evolutionary episode (a whole-genomic
duplication, WGD), instead of a series of small genomic rearrangements.
Thus, the WGD appears as the key event behind the diversification of
fermentative yeasts, which by increasing gene dosage and maximized their
capacity of energy extraction for exploiting the new ecological niche
provided by single sugars.