The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids

Abstract

In eukaryotes, mitochondrial DNA (mtDNA) has high rate of nucleotide substitution leading to different mitochondrial haplotypes called mitotypes. However, the impact of mitochondrial genetic variant on phenotypic variation has been poorly considered in microorganisms because mtDNA encodes very few genes compared to nuclear DNA, and also because mitochondrial inheritance is not uniparental. Here we propose original material to unravel mitotype impact on phenotype: we produced interspecific hybrids between S. cerevisiae and S. uvarum species, using fully homozygous diploid parental strains. For two different interspecific crosses involving different parental strains, we recovered 10 independent hybrids per cross, and allowed mtDNA fixation after around 80 generations. We developed PCR-based markers for the rapid discrimination of S. cerevisiae and S. uvarum mitochondrial DNA. For both crosses, we were able to isolate fully isogenic hybrids at the nuclear level, yet possessing either S. cerevisiae mtDNA (Sc-mtDNA) or S. uvarum mtDNA (Su-mtDNA). Under fermentative conditions, the mitotype has no phenotypic impact on fermentation kinetics and products, which was expected since mtDNA are not necessary for fermentative metabolism. Alternatively, under respiratory conditions, hybrids with Sc-mtDNA have higher population growth performance, associated with higher respiratory rate. Indeed, far from the hypothesis that mtDNA variation is neutral, our work shows that mitochondrial polymorphism can have a strong impact on fitness components and hence on the evolutionary fate of the yeast populations. We hypothesize that under fermentative conditions, hybrids may fix stochastically one or the other mt-DNA, while respiratory environments may increase the probability to fix Sc-mtDNA.

Environmental Factors Can Influence Mitochondrial Inheritance in the Saccharomyces Yeast Hybrids

“…Albertin et al [50] and Solieri et al [51] both produced interspecific hybrids between S . cerevisiae and S .…”

“…However, we showed that, for each crossing, there are still hybrids progeny with mtDNA types from both parents after a given number of generations. In Albertin et al [50] and Solieri et al [51], hybrids per cross were recurrent cultured on YPD-agar plates from one colony to a given number of generations. These populations underwent severe bottlenecks during subculturing.…”

A Systems Approach to Elucidate Heterosis of Protein Abundances in Yeast

“…Yeast Strains-Four diploid S. uvarum strains, seven diploid S. cerevisiae strains, and their 55 hybrids produced from a half diallel design (53) were analyzed in this study. Parental strains were derived from strains isolated from different geographical locations and from either natural or food-processing origins (Table I): the S. cerevisiae strains were isolated from diverse media (distillery, enology, oak exudate) to maximize the genetic diversity within this species (54); the S. uvarum strains, originating from grape must or cider fermentation, were chosen to cover a wide part of the genetic diversity of the S. uvarum species (Masneuf-Pomarè de, I., personal communication).…”

“…Construction of the Half Diallel Design-Hybrid construction was performed as described in Albertin et al (53). Briefly, the 11 diploid parental strains were transformed with a cassette containing the HO allele disrupted by a gene of resistance to either G418 (ho::KanR), hygromycin B (ho::HygR), or nourseothricin (ho::NatR).…”

Mitochondria inheritance is a key factor for tolerance to dehydration in wine yeast production

“…) and has a strong impact on growth and respiration rates under aerobic conditions (Albertin et al . ). In contrast, these hybrids displayed similar performance during the fermentation of synthetic grape juice.…”