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1. Mitochondrial genome diversity across the subphylum Saccharomycotina

   https://doi.org/10.3389/fmicb.2023.1268944  

   Wolters, John F.; LaBella, Abigail L.; Opulente, Dana A.; Rokas, Antonis; Hittinger, Chris Todd (November 2023, Frontiers in Microbiology)

   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 yeastSaccharomyces 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 generaMetschnikowiaandSaccharomycestrended larger, while several species in the order Saccharomycetales, which includesS. 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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2. High mitochondrial mutation rates in Silene are associated with nuclear-mediated changes in mitochondrial physiology

   https://doi.org/10.1098/rsbl.2020.0450  

   Weaver, Ryan J.; Carrion, Gina; Nix, Rachel; Maeda, Gerald P.; Rabinowitz, Samantha; Iverson, Erik N.; Thueson, Kiley; Havird, Justin C. (September 2020, Biology Letters)

   null (Ed.)

   Mitochondrial (mt) respiration depends on proteins encoded both by the mitochondrial and nuclear genomes. Variation in mt-DNA mutation rates exists across eukaryotes, although the functional consequences of elevated mt mutation rates in some lineages remain underexplored. In the angiosperm genus Silene , closely related, ecologically similar species have either ‘fast' or ‘slow' mt-DNA mutation rates. Here, we investigated the functional consequences of elevated mt-DNA mutation rates on mt respiration profiles of Silene mitochondria. Overall levels of respiration were similar among Species. Fast species had lower respiration efficiency than slow species and relied up to 48% more on nuclear-encoded respiratory enzymes alternative oxidase (AOX) and accessory dehydrogenases (DHex), which participate in stress responses in plants. However, not all fast species showed these trends. Respiratory profiles of some enzymes were correlated, most notably AOX and DHex. We conclude that subtle differences in mt physiology among Silene lineages with dramatically different mt mutation rates may underly similar phenotypes at higher levels of biological organization, betraying the consequences of mt mutations. 

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3. Relative rates of evolution of male-beneficial nuclear compensatory mutations and male-harming Mother’s Curse mitochondrial alleles

   https://doi.org/10.1093/evolut/qpad087  

   Dapper, Amy L.; Diegel, Amanda E.; Wade, Michael J. (May 2023, Evolution)

   Abstract Mother’s Curse alleles represent a significant source of potential male fitness defects. The maternal inheritance of mutations with the pattern of sex-specific fitness effects, s♀>0>s♂, allows Mother’s Curse alleles to spread through a population even though they reduce male fitness. Although the mitochondrial genomes of animals contain only a handful of protein-coding genes, mutations in many of these genes have been shown to have a direct effect on male fertility. The evolutionary process of nuclear compensation is hypothesized to counteract the male-limited mitochondrial defects that spread via Mother’s Curse. Here we use population genetic models to investigate the evolution of compensatory autosomal nuclear mutations that act to restore the loss of fitness caused by mitochondrial mutation pressures. We derive the rate of male fitness deterioration by Mother’s Curse and the rate of restoration by nuclear compensatory evolution. We find that the rate of nuclear gene compensation is many times slower than that of its deterioration by cytoplasmic mutation pressure, resulting in a significant lag in the recovery of male fitness. Thus, the numbers of nuclear genes capable of restoring male mitochondrial fitness defects must be large in order to sustain male fitness in the face of mutation pressures. 

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4. Mitonuclear Mismatch is Associated With Increased Male Frequency, Outcrossing, and Male Sperm Size in Experimentally-Evolved C. elegans

   https://doi.org/10.3389/fgene.2022.742272  

   Bever, Brent W.; Dietz, Zachary P.; Sullins, Jennifer A.; Montoya, Ariana M.; Bergthorsson, Ulfar; Katju, Vaishali; Estes, Suzanne (March 2022, Frontiers in Genetics)

   We provide a partial test of the mitonuclear sex hypothesis with the first controlled study of how male frequencies and rates of outcrossing evolve in response to mitonuclear mismatch by allowing replicate lineages of C. elegans nematodes containing either mitochondrial or nuclear mutations of electron transport chain (ETC) genes to evolve under three sexual systems: facultatively outcrossing (wildtype), obligately selfing, and obligately outcrossing. Among facultatively outcrossing lines, we found evolution of increased male frequency in at least one replicate line of all four ETC mutant backgrounds tested—nuclear isp-1 , mitochondrial cox-1 and ctb-1 , and an isp-1 IV; ctb-1M mitonuclear double mutant—and confirmed for a single line set ( cox-1 ) that increased male frequency also resulted in successful outcrossing. We previously found the same result for lines evolved from another nuclear ETC mutant, gas-1 . For several lines in the current experiment, however, male frequency declined to wildtype levels (near 0%) in later generations. Male frequency did not change in lines evolved from a wildtype control strain. Additional phenotypic assays of lines evolved from the mitochondrial cox-1 mutant indicated that evolution of high male frequency was accompanied by evolution of increased male sperm size and mating success with tester females, but that it did not translate into increased mating success with coevolved hermaphrodites. Rather, hermaphrodites’ self-crossed reproductive fitness increased, consistent with sexually antagonistic coevolution. In accordance with evolutionary theory, males and sexual outcrossing may be most beneficial to populations evolving from a state of low ancestral fitness ( gas-1 , as previously reported) and less beneficial or deleterious to those evolving from a state of higher ancestral fitness ( cox-1 ). In support of this idea, the obligately outcrossing fog-2 V; cox-1 M lines exhibited no fitness evolution compared to their ancestor, while facultatively outcrossing lines showed slight upward evolution of fitness, and all but one of the obligately selfing xol-1 X; cox-1 M lines evolved substantially increased fitness—even beyond wildtype levels. This work provides a foundation to directly test the effect of reproductive mode on the evolutionary dynamics of mitonuclear genomes, as well as whether compensatory mutations (nuclear or mitochondrial) can rescue populations from mitochondrial dysfunction. 

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5. Pervasive mitochondrial tRNA gene loss in the clade B of haplosclerid sponges (Porifera, Demospongiae)

   https://doi.org/10.1101/2024.03.04.583380  

   Lavrov, Dennis V; Turner, Thomas L; Vicente, Jan (March 2024, bioRxiv)

   <bold>Abstract</bold> Mitochondrial tRNA gene loss and cytosolic tRNA import to mitochondria are two common phenomena in mitochondrial biology, but their importance is often under-appreciated in animals. This is because most bilaterally symmetrical animals (Bilateria) encode a complete set of tRNAs needed for mitochondrial translation. By contrast, studies of mitochondrial genomes in non-bilaterian animals have shown a reduced tRNA gene content in several lineages, necessitating tRNA import. Interestingly, in most of these lineages tRNA gene content appears to be set early in the evolution of the group and conserved thereafter. Here we demonstrate that Clade B of Haplosclerid Sponges (CBHS) represent an exception to this pattern. We determined mt-genome sequences for eight species from this group and analyzed them with six that had been previously available. In addition, we determined mt-genome sequences for two species of haploslerid sponges outside the CBHS and used them with eight previously available sequences as outgroups. We found that tRNA gene content varied widely among CBHS species: from three in an undescribedHaliclonaspecies (Haliclona sp. TLT785) to 25 inXestospongia mutaandX. testudinaria. Furthermore, we found that all CBHS species outside the genusXestospongialackedatp9, while some also lackedatp8. Analysis of nuclear sequences fromNiphates digitalisrevealed that bothatp8andatp9had transferred to the nuclear genome, while the absence of mt-tRNA genes represented their genuine loss. Overall, CBHS can be a useful animal system to study mt-tRNA genes loss, mitochondrial import of cytosolic tRNA, and the impact of both of these processes on mitochondrial evolution. Significance statementIt is generally believed that the gene content is stable in animal mitochondrial (mt) DNA. Indeed, mtDNA in most bilaterally symmetrical animals encompasses a conserved set of 37 genes coding for 13 proteins, two rRNAs and 22 tRNAs. By contrast, mtDNA in non-bilaterian animals shows more variation in mt gene content, in particular in the number of tRNA genes. However, most of this variation occurs between major non-bilaterian lineages. Here we demonstrate that a group of demosponges called Clade B of Haplosclerid Sponges (CBHS) represents a fascinating exception to this pattern, with species experiencing recurrent losses of up to 22 mt-tRNA genes. We argue that this group constitutes a promising system to investigate the effects of tRNA gene loss on evolution of mt-genomes as well as mitochondrial tRNA import machinery. 

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