The evolutionary history of Saccharomyces species inferred from completed mitochondrial genomes and revision in the ‘yeast mitochondrial genetic code’

Abstract

The yeast Saccharomyces are widely used to test ecological and evolutionary hypotheses. A large number of nuclear genomic DNA sequences are available, but mitochondrial genomic data are insufficient. We completed mitochondrial DNA (mtDNA) sequencing from Illumina MiSeq reads for all Saccharomyces species. All are circularly mapped molecules decreasing in size with phylogenetic distance from Saccharomyces cerevisiae but with similar gene content including regulatory and selfish elements like origins of replication, introns, free-standing open reading frames or GC clusters. Their most profound feature is species-specific alteration in gene order. The genetic code slightly differs from well-established yeast mitochondrial code as GUG is used rarely as the translation start and CGA and CGC code for arginine. The multilocus phylogeny, inferred from mtDNA, does not correlate with the trees derived from nuclear genes. mtDNA data demonstrate that Saccharomyces cariocanus should be assigned as a separate species and Saccharomyces bayanus CBS 380T should not be considered as a distinct species due to mtDNA nearly identical to Saccharomyces uvarum mtDNA. Apparently, comparison of mtDNAs should not be neglected in genomic studies as it is an important tool to understand the origin and evolutionary history of some yeast species.

Discordant evolution of mitochondrial and nuclear yeast genomes at population level

“…Recent report suggested that the alteration of the gene order within yeast genera could be related to the mitochondrial genome size (Sulo et al 2017). While the Lachancea and Yarrowia clades, with mitochondrial genome less than 50 kb, show high synteny across species (Friedrich et al 2012;Gaillardin et al 2012), the Saccharomyces clade (mitochondrial genome size > 65 kb) is more prone to rearrangements (Sulo et al 2017). Indeed structural rearrangements were also detected in the mitochondrial genome of S. paradoxus (Yue et al 2017).…”

Mitochondrial Genome Variation Affects Multiple Respiration and Nonrespiration Phenotypes in Saccharomyces cerevisiae

“…The mitochondrial genome sequences of 128 strains in 8 Saccharomyces species (Foury et al 1998;Fritsch et al 2014;Strope et al 2015;Leducq et al 2017;Sulo et al 2017) were screened for ATP6 and ENS2 gene sequences. Evolutionary histories of these genes were inferred by using the maximum likelihood (ML) method, using MEGA6 (Tamura et al 2013).…”

“…We searched the mitochondrial genome sequences of seven other Saccharomyces species (Leducq et al 2017;Sulo et al 2017) and identified ens2 sequences in Saccharomyces arboricola and Saccharomyces paradoxus ( Figure 2). Similar to S. cerevisiae ( Figure 3 and Table S6), ENS2 was located immediately downstream of ATP6 in S. arboricola (two of two strains) as well as in some S. paradoxus (9 of 25) strains; there was evidence of ENS2 introgression (Figure 1, Figure S1, and Figure S2).…”

“…The three S. cerevisiae ENS2 groups (A, B, and 1399), ens2 sequence presence/absence, the two classes of Ens2 site-specific endonuclease recognition sequences, and the three most highly oligomycin phenotypeassociated SNPs coincided with the six S. cerevisiae ATP6 groups (Figure 2, Figure S1, Figure S2, and Table S6). Finally, we searched the recently published mitochondrial genome sequences of seven other Saccharomyces species (Leducq et al 2017;Sulo et al 2017) for ATP6 and constructed phylogenies. We identified three S. paradoxus ATP6 groups (S. paradoxus groups 1, 2, and 3).…”

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

“…The intronless S. cerevisiae COX1 and S. uvarum COB alleles showed better respiratory growth at 37°C than wild-type S. cerevisiae mtDNA, suggesting a dominant negative role of introns in the hybrid. In Saccharomyces, the number and presence of mitochondrial introns is variable between species (Sulo et al 2017). This contrasts with high conservation of mitochondrial protein coding sequences, which show over 90% sequence identity between S. cerevisiae and S. uvarum, much higher than the 80% average of nuclear-encoded genes (Kellis et al 2003).…”