Mitochondrial Genome Evolution in a Single Protoploid Yeast Species

Department of Genetics, Genomics and Microbiology, University of Strasbourg/Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7156, Strasbourg, France.
G3-Genes Genomes Genetics (Impact Factor: 3.2). 09/2012; 2(9):1103-11. DOI: 10.1534/g3.112.003152
Source: PubMed


Mitochondria are organelles, which play a key role in some essential functions, including respiration, metabolite biosynthesis, ion homeostasis, and apoptosis. The vast numbers of mitochondrial DNA (mtDNA) sequences of various yeast species, which have recently been published, have also helped to elucidate the structural diversity of these genomes. Although a large corpus of data are now available on the diversity of yeast species, little is known so far about the mtDNA diversity in single yeast species. To study the genetic variations occurring in the mtDNA of wild yeast isolates, we performed a genome-wide polymorphism survey on the mtDNA of 18 Lachancea kluyveri (formerly Saccharomyces kluyveri) strains. We determined the complete mt genome sequences of strains isolated from various geographical locations (in North America, Asia, and Europe) and ecological niches (Drosophila, tree exudates, soil). The mt genome of the NCYC 543 reference strain is 51,525 bp long. It contains the same core of genes as Lachancea thermotolerans, the nearest relative to L. kluyveri. To explore the mt genome variations in a single yeast species, we compared the mtDNAs of the 18 isolates. The phylogeny and population structure of L. kluyveri provide clear-cut evidence for the existence of well-defined geographically isolated lineages. Although these genomes are completely syntenic, their size and the intron content were found to vary among the isolates studied. These genomes are highly polymorphic, showing an average diversity of 28.5 SNPs/kb and 6.6 indels/kb. Analysis of the SNP and indel patterns showed the existence of a particularly high overall level of polymorphism in the intergenic regions. The dN/dS ratios obtained are consistent with purifying selection in all these genes, with the noteworthy exception of the VAR1 gene, which gave a very high ratio. These data suggest that the intergenic regions have evolved very fast in yeast mitochondrial genomes.

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    • "Ultimately, we procured a valuable group of sequences for the expansion of intraspecies mt genome comparisons among clades of the Lachancea genus. A Model System for the Analysis of Inter and Intraspecific Diversity: Sister Species of the Lachancea Genus Previous to this work, only one study assessed the intraspecies mt diversity within a single yeast lineage, specifically, among 18 isolates of L. kluyveri (Jung et al. 2012). This species is most closely related to L. thermotolerans and the mt genomes share a variety of features (Talla et al. 2005). "
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    ABSTRACT: The increasing availability of mitochondrial (mt) sequence data from various yeasts provides a tool to study genomic evolution within and between different species. While the genomes from a range of lineages are available, there is a lack of information concerning intraspecific mtDNA diversity. Here, we analyzed the mt genomes of 50 strains from Lachancea thermotolerans, a protoploid yeast species that has been isolated from several locations (Europe, Asia, Australia, South Africa, and North / South America) and ecological sources (fruit, tree exudate, plant material, and grape and agave fermentations). Protein-coding genes from the mtDNA were used to construct a phylogeny, which reflected a similar, yet less resolved topology than the phylogenetic tree of 50 nuclear genes. In comparison to its sister species Lachancea kluyveri, L. thermotolerans has a smaller mt genome. This is due to shorter intergenic regions and fewer introns, of which the latter are only found in COX1. We revealed that L. kluyveri and L. thermotolerans share similar levels of intraspecific divergence concerning the nuclear genomes. However, L. thermotolerans has a more highly conserved mt genome with the coding regions characterized by low rates of nonsynonymous substitution. Thus, in the mt genomes of L. thermotolerans, stronger purifying selection and lower mutation rates potentially shape genome diversity in contract to what was found for L. kluyveri, demonstrating that the factors driving mt genome evolution are different even between closely related species.
    Genome Biology and Evolution 09/2014; 6(10). DOI:10.1093/gbe/evu203 · 4.23 Impact Factor
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    • "To obtain a global view of the genetic variations occurring in the mtDNA within a species, we recently performed a genome-wide polymorphism survey on the mt genome of 18 Lachancea kluyveri (formerly known as Saccharomyces kluyveri) isolates [2]. We generated a comprehensive view of mitochondrial sequence polymorphism in this single species. "
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    ABSTRACT: Yeasts are leading model organisms for mitochondrial genome studies. The explosion of complete sequence of yeast mitochondrial (mt) genomes revealed a wide diversity of organization and structure between species. Recently, genome-wide polymorphism survey on the mt genome of isolates of a single species, Lachancea kluyveri, was also performed. To compare the mitochondrial genome evolution at two hierarchical levels: within and among closely related species, we focused on five species of the Lachancea genus, which are close relatives of L. kluyveri. Hence, we sequenced the complete mt genome of L. dasiensis, L. nothofagi, L. mirantina, L. fantastica and L. meyersii. The phylogeny of the Lachancea genus was explored using these data. Analysis of intra- and interspecific variability across the whole Lachancea genus led to the same conclusions regarding the mitochondrial genome evolution. These genomes exhibit a similar architecture and are completely syntenic. Nevertheless, genome sizes vary considerably because of the variations of the intergenic regions and the intron content, contributing to mitochondrial genome plasticity. The high variability of the intergenic regions stands in contrast to the high level of similarity of protein sequences. Quantification of the selective constraints clearly revealed that most of the mitochondrial genes are under purifying selection in the whole genus.
    PLoS ONE 10/2012; 7(10):e47834. DOI:10.1371/journal.pone.0047834 · 3.23 Impact Factor
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    ABSTRACT: Little is known of the genetic basis of migration despite the ecological benefits migratory species provide to their communities and their rapid global decline due to anthropogenic disturbances in recent years. Using next-generation sequencing of restriction-site-associated DNA (RAD) tags, we genotyped thousands of single nucleotide polymorphisms (SNPs) in two wild populations of migratory steelhead and resident rainbow trout (Oncorhynchus mykiss) from the Pacific Northwest of the United States. One population maintains a connection to the sea, whereas the other population has been sequestered from its access to the ocean for more than 50 years by a hydropower dam. Here we performed a genome-wide association study to identify 504 RAD SNP markers from several genetic regions that were associated with the propensity to migrate both within and between the populations. Our results corroborate those in previous quantitative trait loci studies and provide evidence for additional loci associated with this complex migratory life history. Our results suggest a complex multi-genic basis with several loci of small effect distributed throughout the genome contributing to migration in this species. We also determined that despite being sequestered for decades, the landlocked population continues to harbour genetic variation associated with a migratory life history and ATPase activity. Furthermore, we demonstrate the utility of genotyping-by-sequencing and how RAD-tag SNP data can be readily compared between studies to investigate migration within this species.
    Molecular Ecology 10/2012; 22(11). DOI:10.1111/mec.12082 · 6.49 Impact Factor
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