Extensive Horizontal Transfer and Homologous Recombination Generate Highly Chimeric Mitochondrial Genomes in Yeast

Abstract

The frequency of horizontal gene transfer (HGT) in mitochondrial DNA varies substantially. In plants, HGT is relatively common, whereas in animals it appears to be quite rare. It is of considerable importance to understand mitochondrial HGT across the major groups of eukaryotes at a genome-wide level, but so far this has been well studied only in plants. In this study, we generated ten new mitochondrial genome sequences and analyzed 40 mitochondrial genomes from the Saccharomycetaceae to assess the magnitude and nature of mitochondrial HGT in yeasts. We provide evidence for extensive, homologous-recombination-mediated, mitochondrial-to-mitochondrial HGT occurring throughout yeast mitochondrial genomes, leading to genomes that are highly chimeric evolutionarily. This HGT has led to substantial intraspecific polymorphism in both sequence content and sequence divergence, which to our knowledge has not been previously documented in any mitochondrial genome. The unexpectedly high frequency of mitochondrial HGT in yeast may be driven by frequent mitochondrial fusion, relatively low mitochondrial substitution rates and pseudohyphal fusion to produce heterokaryons. These findings suggest that mitochondrial HGT may play an important role in genome evolution of a much broader spectrum of eukaryotes than previously appreciated and that there is a critical need to systematically study the frequency, extent, and importance of mitochondrial HGT across eukaryotes.

Evolutionary restoration of fertility in an interspecies hybrid yeast, by whole-genome duplication after a failed mating-type switch

“…CLIB213 T lacks 2 of the 5 mitochondrial introns that are present in ATCC60483: the omega intron of the large subunit mitochondrial rDNA and intron 2 of COX1 . Intraspecies polymorphism for intron presence/absence and comparable levels of intraspecies mtDNA sequence diversity have been reported in other yeast species [45, 46]. …”

Intraspecific diversity of fission yeast mitochondrial genomes

“…Unlike in animals, where mitogenomes are usually inherited uniparentally, in fungi, biparental transmission of mitogenomes is common and thus allows the recombination between parental mitogenomes (Xu & Li 2015). For budding yeast species belonging to the family Saccharomycetaceae, naturally occurring mitogenome recombination appears to be common (Leducq et al 2017;Peris et al 2017;Wu & Hao 2014;Wu et al 2015). In contrast, we show here that, despite a high level of inter-lineage admixture existing among the S. pombe isolates, inter-lineage recombination of S. pombe mitogenomes has rarely happened.…”

Bakery yeasts, a new model for studies in ecology and evolution

“…All six species have been found in sourdough samples from Asia and Europe, and some of them have also been found in America, Africa, and Australia (Figure a, and see links for interactive maps describing yeast species composition per sourdough http://robdunnlab.com/projects/sourdough/map/ and https://www6.inra.fr/bakery_eng/Results). All of these species' genomes, except for the two Kasachstania species, have been sequenced (Chan, Gan, Ling, & Rashid, ; Goffeau et al, ; Gomez‐Angulo et al, ; Gordon et al, ; Park et al, ; Riley et al, ; Wolfe et al, ; Wu, Buljic, & Hao, ). The distribution of these species did not appear to be correlated with the type of cereal used to make the sourdough (Figure b).…”