Mitochondrial introgression suggests extensive ancestral hybridization events among Saccharomyces species

Abstract

Horizontal gene transfer (HGT) in eukaryotic plastids and mitochondrial genomes is common, and plays an important role in organism evolution. In yeasts, recent mitochondrial HGT has been suggested between S. cerevisiae and S. paradoxus. However, few strains have been explored given the lack of accurate mitochondrial genome annotations. Mitochondrial genome sequences are important to understand how frequent these introgressions occur, and their role in cytonuclear incompatibilities and fitness. Indeed, most of the Bateson-Dobzhansky-Muller genetic incompatibilities described in yeasts are driven by cytonuclear incompatibilities. We herein explored the mitochondrial inheritance of several worldwide distributed wild Saccharomyces species and their hybrids isolated from different sources and geographic origins. We demonstrated the existence of several recombination points in mitochondrial region COX2-ORF1, likely mediated by either the activity of the protein encoded by the ORF1 (F-SceIII) gene, a free-standing homing endonuclease, or mostly facilitated by A+T tandem repeats and regions of integration of GC clusters. These introgressions were shown to occur among strains of the same species and among strains of different species, which suggests a complex model of Saccharomyces evolution that involves several ancestral hybridization events in wild environments.

Genetic Polymorphism in Wine Yeasts: Mechanisms and Methods for Its Detection

“…Similar introgressions were also found in other hybrids (Pérez-Través et al, 2014b; Peris et al, 2014), and a recent study (Peris et al, 2017) demonstrated that these introgressions are very common among Saccharomyces species, which suggests extensive ancestral hybridization events during their evolutionary history.…”

Phylogeography of the wild Lager‐brewing ancestor (Saccharomyces eubayanus) in Patagonia

“…A) were found in Southern Patagonia (Lake La Plata and Glaciares NP sampling sites), which add to a similar case found in the strain CRUB 1975 (yHCT105, from Puyehue) previously reported by Peris and colleagues (). Recombination between Saccharomyces species is common in the mitochondrial genome in both natural and industrial environments (Peris et al ., ,b). We investigated the available COX2 sequences from S. uvarum strains to identify the source of the introgressed region but were unsuccessful because neither S. uvarum population varied in that specific mtDNA region (Supporting Information Fig.…”

“…The mitochondrial gene COX2 (502 bp) (Peris et al, 2014(Peris et al, , 2017a, the nuclear gene DCR1 (859 bp) (Peris et al, 2014) and an intergenic region between the nuclear genes FAR8 and RSF1 (intFR; 547 bp) (Bing et al, 2014) were amplified and sequenced for phylogenetic studies. Sequences were aligned using ClustalW in MEGA 6.0 (Tamura et al, 2013) and corrected manually.…”

Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production

“…Geographical, ecological, and genotypic information of selected Saccharomyces species for generating hybrids, or for conducting the three replicate fermentations in four media conditions at 24 °C, for wild isolates, or 30 °C for synthetic hybridsC2_HXXX: Indicates the COX2 haplotype based on [100] Sch , Scheffersomyces (Pichia) stipitis ; Cp , Clostridium phytofermentans ; Sc , Saccharomyces cerevisiae ; G , generations XYL123 , abbreviation for the SchXYL1 - SchXYL2 - SchXYL3 cassette…”

“…Mitochondrial genomes are displayed in circles , and the color corresponds to the species donor, denoted in the legend. Recombination in Y73 ×  S. mikatae was likely initiated in the COX2 gene, a region previously described as a recombination hotspot due to the presence of the homing endonuclease gene F- Sce III [100] …”