Mitochondrial Genome Evolution in a Single Protoploid Yeast Species

Jung, Paul P.; Friedrich, Anne; Reisser, Cyrielle; Hou, Jing; Schacherer, Joseph

doi:10.1534/g3.112.003152

Cited by 44 publications

(51 citation statements)

References 52 publications

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“…The nonsynonymous to synonymous ratio of intraspecific polymorphisms for atp6 (pN/pS = 0.172) was actually higher than that for the rps3/VAR1 excluding indel variations (pN/pS = 0.142), a mitochondrial gene known for intraspecific diversity [19]. Interestingly, this mirrors intraspecific polymorphisms observed for the atp6 gene in L. kluyveri [47], a yeast that evolved before the whole genome duplication. This gene has also been implicated in tests of positive selection in other organisms [60–62].…”

Section: Discussionmentioning

confidence: 92%

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Population structure of mitochondrial genomes in Saccharomyces cerevisiae

2015

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BackgroundRigorous study of mitochondrial functions and cell biology in the budding yeast, Saccharomyces cerevisiae has advanced our understanding of mitochondrial genetics. This yeast is now a powerful model for population genetics, owing to large genetic diversity and highly structured populations among wild isolates. Comparative mitochondrial genomic analyses between yeast species have revealed broad evolutionary changes in genome organization and architecture. A fine-scale view of recent evolutionary changes within S. cerevisiae has not been possible due to low numbers of complete mitochondrial sequences.ResultsTo address challenges of sequencing AT-rich and repetitive mitochondrial DNAs (mtDNAs), we sequenced two divergent S. cerevisiae mtDNAs using a single-molecule sequencing platform (PacBio RS). Using de novo assemblies, we generated highly accurate complete mtDNA sequences. These mtDNA sequences were compared with 98 additional mtDNA sequences gathered from various published collections. Phylogenies based on mitochondrial coding sequences and intron profiles revealed that intraspecific diversity in mitochondrial genomes generally recapitulated the population structure of nuclear genomes. Analysis of intergenic sequence indicated a recent expansion of mobile elements in certain populations. Additionally, our analyses revealed that certain populations lacked introns previously believed conserved throughout the species, as well as the presence of introns never before reported in S. cerevisiae.ConclusionsOur results revealed that the extensive variation in S. cerevisiae mtDNAs is often population specific, thus offering a window into the recent evolutionary processes shaping these genomes. In addition, we offer an effective strategy for sequencing these challenging AT-rich mitochondrial genomes for small scale projects.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1664-4) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 92%

“…Few population genetic investigations on intraspecific mtDNAs in yeasts exist [45–47], and none for Saccharomyces species. To provide a window onto recent evolutionary changes in the mtDNA, we compared the intraspecific genetic variation in mitochondrial genomes from 100 strains of S. cerevisiae.…”

Section: Discussionmentioning

confidence: 99%

Population structure of mitochondrial genomes in Saccharomyces cerevisiae

2015

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“…Previous work found high levels of intraspecific mt genetic diversity within L. kluyveri to be in the intergenic regions (Jung et al 2012). Indeed, in the coding sequence, the SNP density ranged from 0 to 13.96 SNPs/kb, while in the intergenic regions it was 0.31–82.7 SNPs/kb.…”

Section: Resultsmentioning

confidence: 99%

Population Genomic Analysis Reveals Highly Conserved Mitochondrial Genomes in the Yeast Species Lachancea thermotolerans

Freel

Friedrich

Hou

et al. 2014

Genome Biology and Evolution

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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.

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“…However, identical or almost identical mitochondrial genomes have also been reported, for example, in Penicillium isolates from Spain and China, respectively, and may indicate a rapid, global spread of one particular isolate of C. subhashii [103]. On the other hand, the identical mitochondrial genomes are in contrast to studies reporting considerable intra-species variation in size, intron content, and recombination in fungal mitochondrial genomes [104–106]. At present, it is not clear why the C. subhashii mitochondrial genome is so conserved and future studies will have to address the conservation and evolution of the mitochondrial genome in more detail as well as reveal the entire genome sequence of C subhashii as a basis for identifying genes mediating antagonistic functions.…”

Section: Discussionmentioning

confidence: 99%

Competition assays and physiological experiments of soil and phyllosphere yeasts identify Candida subhashii as a novel antagonist of filamentous fungi

et al. 2017

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BackgroundWhile recent advances in next generation sequencing technologies have enabled researchers to readily identify countless microbial species in soil, rhizosphere, and phyllosphere microbiomes, the biological functions of the majority of these species are unknown. Functional studies are therefore urgently needed in order to characterize the plethora of microorganisms that are being identified and to point out species that may be used for biotechnology or plant protection. Here, we used a dual culture assay and growth analyses to characterise yeasts (40 different isolates) and their antagonistic effect on 16 filamentous fungi; comprising plant pathogens, antagonists, and saprophytes.ResultsOverall, this competition screen of 640 pairwise combinations revealed a broad range of outcomes, ranging from small stimulatory effects of some yeasts up to a growth inhibition of more than 80% by individual species. On average, yeasts isolated from soil suppressed filamentous fungi more strongly than phyllosphere yeasts and the antagonistic activity was a species-/isolate-specific property and not dependent on the filamentous fungus a yeast was interacting with. The isolates with the strongest antagonistic activity were Metschnikowia pulcherrima, Hanseniaspora sp., Cyberlindnera sargentensis, Aureobasidium pullulans, Candida subhashii, and Pichia kluyveri. Among these, the soil yeasts (C. sargentensis, A. pullulans, C. subhashii) assimilated and/or oxidized more di-, tri- and tetrasaccharides and organic acids than yeasts from the phyllosphere. Only the two yeasts C. subhashii and M. pulcherrima were able to grow with N-acetyl-glucosamine as carbon source.ConclusionsThe competition assays and physiological experiments described here identified known antagonists that have been implicated in the biological control of plant pathogenic fungi in the past, but also little characterised species such as C. subhashii. Overall, soil yeasts were more antagonistic and metabolically versatile than yeasts from the phyllosphere. Noteworthy was the strong antagonistic activity of the soil yeast C. subhashii, which had so far only been described from a clinical sample and not been studied with respect to biocontrol. Based on binary competition assays and growth analyses (e.g., on different carbon sources, growth in root exudates), C. subhashii was identified as a competitive and antagonistic soil yeast with potential as a novel biocontrol agent against plant pathogenic fungi.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-016-0908-z) contains supplementary material, which is available to authorized users.

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Mitochondrial Genome Evolution in a Single Protoploid Yeast Species

Cited by 44 publications

References 52 publications

Population structure of mitochondrial genomes in Saccharomyces cerevisiae

Population structure of mitochondrial genomes in Saccharomyces cerevisiae

Population Genomic Analysis Reveals Highly Conserved Mitochondrial Genomes in the Yeast Species Lachancea thermotolerans

Competition assays and physiological experiments of soil and phyllosphere yeasts identify Candida subhashii as a novel antagonist of filamentous fungi

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