Wolters John F, LaBella Abigail L, Opulente Dana A, Rokas Antonis, Hittinger Chris Todd
Laboratory 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 States.
Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, NC, United States.
Front Microbiol. 2023 Nov 23;14:1268944. doi: 10.3389/fmicb.2023.1268944. eCollection 2023.
Eukaryotic 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 , but mitochondrial genome sampling across many groups has been scarce, even as hundreds of nuclear genomes have become available.
By 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.
Comparison of 353 yeast mitochondrial genomes revealed that, while size and GC content were fairly consistent across species, those in the genera and trended larger, while several species in the order Saccharomycetales, which includes , 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.
As 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.
真核生物的生命依赖于核基因组和细胞器基因组（如线粒体中的基因组）所编码的功能元件。线粒体基因组的内容、大小和结构在不同生物中存在差异，这可能对表型变异和由此产生的进化轨迹产生重大影响。在子囊菌亚门的酵母中，相对于模式酵母，已在各种物种中观察到广泛差异，但即使已有数百个核基因组可用，许多类群中线粒体基因组的采样仍然很少。
通过从现有的短读长基因组序列数据集中提取线粒体组装序列，我们极大地扩展了可用基因组的数量以及稀疏采样分支的覆盖范围。
对353个酵母线粒体基因组的比较表明，虽然物种间的大小和GC含量相当一致，但毕赤酵母属和德巴利酵母属的线粒体基因组倾向于更大，而包括酿酒酵母在内的酵母目几个物种的GC含量较低。大小和GC含量的极端例子分散在整个亚门中。所有线粒体基因组都共享一组核心的蛋白质编码基因，用于复合体III、IV和V，但它们在是否存在线粒体编码的典型复合体I基因方面存在差异。我们将复合体I基因的丢失追溯到酵母目和酵母球菌目祖先中的一个重大事件，但我们也在发夫酵母目、毕赤酵母目和双足酵母目中观察到了几次独立的丢失事件。与基于较小规模数据集的先前假设相反，蛋白质编码基因进化速率的比较显示，需氧发酵（克奈特/瓦伯格阳性）酵母中不存在进化速率升高的偏向。线粒体内含子分布广泛，但在某些类群中高度富集。大多数线粒体内含子在类群内保守性较差，但有几个在类群内、类群间甚至跨分类目共享，这与水平基因转移一致，可能涉及作为自私元件的归巢内切酶。
随着可用真菌核基因组数量的持续增加，本文所述的从这些数据集中检索线粒体基因组序列的方法对于确保真菌线粒体基因组的研究与其核基因组研究同步将被证明具有极高价值。
