Mitochondrial genome diversity across the subphylum Saccharomycotina

IntroductionEukaryotic life depends on the functional elements encoded by both the nuclear genome and organellar genomes, such as those contained within the mitochondria. The content, size, and structure of the mitochondrial genome varies across organisms with potentially large implications for phen...

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Main Authors: John F. Wolters, Abigail L. LaBella, Dana A. Opulente, Antonis Rokas, Chris Todd Hittinger
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1268944/full
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author John F. Wolters
Abigail L. LaBella
Abigail L. LaBella
Dana A. Opulente
Dana A. Opulente
Antonis Rokas
Chris Todd Hittinger
author_facet John F. Wolters
Abigail L. LaBella
Abigail L. LaBella
Dana A. Opulente
Dana A. Opulente
Antonis Rokas
Chris Todd Hittinger
author_sort John F. Wolters
collection DOAJ
description IntroductionEukaryotic life depends on the functional elements encoded by both the nuclear genome and organellar genomes, such as those contained within the mitochondria. The content, size, and structure of the mitochondrial genome varies across organisms with potentially large implications for phenotypic variance and resulting evolutionary trajectories. Among yeasts in the subphylum Saccharomycotina, extensive differences have been observed in various species relative to the model yeast Saccharomyces cerevisiae, but mitochondrial genome sampling across many groups has been scarce, even as hundreds of nuclear genomes have become available.MethodsBy extracting mitochondrial assemblies from existing short-read genome sequence datasets, we have greatly expanded both the number of available genomes and the coverage across sparsely sampled clades.ResultsComparison of 353 yeast mitochondrial genomes revealed that, while size and GC content were fairly consistent across species, those in the genera Metschnikowia and Saccharomyces trended larger, while several species in the order Saccharomycetales, which includes S. cerevisiae, exhibited lower GC content. Extreme examples for both size and GC content were scattered throughout the subphylum. All mitochondrial genomes shared a core set of protein-coding genes for Complexes III, IV, and V, but they varied in the presence or absence of mitochondrially-encoded canonical Complex I genes. We traced the loss of Complex I genes to a major event in the ancestor of the orders Saccharomycetales and Saccharomycodales, but we also observed several independent losses in the orders Phaffomycetales, Pichiales, and Dipodascales. In contrast to prior hypotheses based on smaller-scale datasets, comparison of evolutionary rates in protein-coding genes showed no bias towards elevated rates among aerobically fermenting (Crabtree/Warburg-positive) yeasts. Mitochondrial introns were widely distributed, but they were highly enriched in some groups. The majority of mitochondrial introns were poorly conserved within groups, but several were shared within groups, between groups, and even across taxonomic orders, which is consistent with horizontal gene transfer, likely involving homing endonucleases acting as selfish elements.DiscussionAs the number of available fungal nuclear genomes continues to expand, the methods described here to retrieve mitochondrial genome sequences from these datasets will prove invaluable to ensuring that studies of fungal mitochondrial genomes keep pace with their nuclear counterparts.
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spelling doaj.art-e679e5f3a59c4d5aa832bc6d963a8be12023-11-23T11:12:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-11-011410.3389/fmicb.2023.12689441268944Mitochondrial genome diversity across the subphylum SaccharomycotinaJohn F. Wolters0Abigail L. LaBella1Abigail L. LaBella2Dana A. Opulente3Dana A. Opulente4Antonis Rokas5Chris Todd Hittinger6Laboratory of Genetics, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Center for Genomic Science Innovation, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, NC, United StatesDepartment of Biological Sciences, Vanderbilt University, Nashville, TN, United StatesLaboratory of Genetics, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Center for Genomic Science Innovation, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI, United StatesBiology Department, Villanova University, Villanova, PA, United StatesDepartment of Biological Sciences, Vanderbilt University, Nashville, TN, United StatesLaboratory of Genetics, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Center for Genomic Science Innovation, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI, United StatesIntroductionEukaryotic life depends on the functional elements encoded by both the nuclear genome and organellar genomes, such as those contained within the mitochondria. The content, size, and structure of the mitochondrial genome varies across organisms with potentially large implications for phenotypic variance and resulting evolutionary trajectories. Among yeasts in the subphylum Saccharomycotina, extensive differences have been observed in various species relative to the model yeast Saccharomyces cerevisiae, but mitochondrial genome sampling across many groups has been scarce, even as hundreds of nuclear genomes have become available.MethodsBy extracting mitochondrial assemblies from existing short-read genome sequence datasets, we have greatly expanded both the number of available genomes and the coverage across sparsely sampled clades.ResultsComparison of 353 yeast mitochondrial genomes revealed that, while size and GC content were fairly consistent across species, those in the genera Metschnikowia and Saccharomyces trended larger, while several species in the order Saccharomycetales, which includes S. cerevisiae, exhibited lower GC content. Extreme examples for both size and GC content were scattered throughout the subphylum. All mitochondrial genomes shared a core set of protein-coding genes for Complexes III, IV, and V, but they varied in the presence or absence of mitochondrially-encoded canonical Complex I genes. We traced the loss of Complex I genes to a major event in the ancestor of the orders Saccharomycetales and Saccharomycodales, but we also observed several independent losses in the orders Phaffomycetales, Pichiales, and Dipodascales. In contrast to prior hypotheses based on smaller-scale datasets, comparison of evolutionary rates in protein-coding genes showed no bias towards elevated rates among aerobically fermenting (Crabtree/Warburg-positive) yeasts. Mitochondrial introns were widely distributed, but they were highly enriched in some groups. The majority of mitochondrial introns were poorly conserved within groups, but several were shared within groups, between groups, and even across taxonomic orders, which is consistent with horizontal gene transfer, likely involving homing endonucleases acting as selfish elements.DiscussionAs the number of available fungal nuclear genomes continues to expand, the methods described here to retrieve mitochondrial genome sequences from these datasets will prove invaluable to ensuring that studies of fungal mitochondrial genomes keep pace with their nuclear counterparts.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1268944/fullyeastmitochondriaevolutionselectiondiversity
spellingShingle John F. Wolters
Abigail L. LaBella
Abigail L. LaBella
Dana A. Opulente
Dana A. Opulente
Antonis Rokas
Chris Todd Hittinger
Mitochondrial genome diversity across the subphylum Saccharomycotina
Frontiers in Microbiology
yeast
mitochondria
evolution
selection
diversity
title Mitochondrial genome diversity across the subphylum Saccharomycotina
title_full Mitochondrial genome diversity across the subphylum Saccharomycotina
title_fullStr Mitochondrial genome diversity across the subphylum Saccharomycotina
title_full_unstemmed Mitochondrial genome diversity across the subphylum Saccharomycotina
title_short Mitochondrial genome diversity across the subphylum Saccharomycotina
title_sort mitochondrial genome diversity across the subphylum saccharomycotina
topic yeast
mitochondria
evolution
selection
diversity
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1268944/full
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