Global Characterization of Fungal Mitogenomes: New Insights on Genomic Diversity and Dynamism of Coding Genes and Accessory Elements

Abstract

Fungi comprise a great diversity of species with distinct ecological functions and lifestyles. Similar to other eukaryotes, fungi rely on interactions with prokaryotes and one of the most important symbiotic events was the acquisition of mitochondria. Mitochondria are organelles found in eukaryotic cells whose main function is to generate energy through aerobic respiration. Mitogenomes (mtDNAs) are double-stranded circular or linear DNA from mitochondria that may contain core genes and accessory elements that can be replicated, transcribed, and independently translated from the nuclear genome. Despite their importance, investigative studies on the diversity of fungal mitogenomes are scarce. Herein, we have evaluated 788 curated fungal mitogenomes available at NCBI database to assess discrepancies and similarities among them and to better understand the mechanisms involved in fungal mtDNAs variability. From a total of 12 fungal phyla, four do not have any representative with available mitogenomes, which highlights the underrepresentation of some groups in the current available data. We selected representative and non-redundant mitogenomes based on the threshold of 90% similarity, eliminating 81 mtDNAs. Comparative analyses revealed considerable size variability of mtDNAs with a difference of up to 260 kb in length. Furthermore, variation in mitogenome length and genomic composition are generally related to the number and length of accessory elements (introns, HEGs, and uORFs). We identified an overall average of 8.0 (0–39) introns, 8.0 (0–100) HEGs, and 8.2 (0–102) uORFs per genome, with high variation among phyla. Even though the length of the core protein-coding genes is considerably conserved, approximately 36.3% of the mitogenomes evaluated have at least one of the 14 core coding genes absent. Also, our results revealed that there is not even a single gene shared among all mitogenomes. Other unusual genes in mitogenomes were also detected in many mitogenomes, such as dpo and rpo, and displayed diverse evolutionary histories. Altogether, the results presented in this study suggest that fungal mitogenomes are diverse, contain accessory elements and are absent of a conserved gene that can be used for the taxonomic classification of the Kingdom Fungi.

From Genome Variation to Molecular Mechanisms: What we Have Learned From Yeast Mitochondrial Genomes?

“…All complete mitogenomes in Saccharomycetaceae encode eight protein genes, seven respiratory-chain protein genes ( atp6 , atp8 , atp9 , cob , cox1 , cox2 , and cox3 ) and one ribosomal protein gene var1 , SSU and LSU rRNAs, and 22–24 tRNAs. This is in contrast with a recent report that “no gene is universally conserved in fungal mitogenomes” ( Fonseca et al, 2021 ). Although it is inevitable that fewer mitochondrial genes are shared when more diverse lineages are included ( Roger et al, 2017 ), the variation of mitogenome sequence quality could have been an important reason for the discrepancy on gene conservation among yeast mitogenomes.…”

“…Although it is inevitable that fewer mitochondrial genes are shared when more diverse lineages are included ( Roger et al, 2017 ), the variation of mitogenome sequence quality could have been an important reason for the discrepancy on gene conservation among yeast mitogenomes. For instance, the two S. cerevisiae mitogenomes (accessions: CM002421 and CP046458 ) reportedly missing atp6 by Fonseca et al (2021) are 22,149 bp (including 13,247 Ns for gaps) and 49,451 bp (517 Ns) in length, respectively, much shorter than the average 82.5 Kb [ranging from 74.2 to 92.2 kb in Xiao et al (2017) ] of S. cerevisiae mitogenomes ( Figure 1 ). The Saccharomycodaceae family has a sole case of gene loss involving a protein gene.…”

De Novo Long-Read Whole-Genome Assemblies and the Comparative Pan-Genome Analysis of Ascochyta Blight Pathogens Affecting Field Pea

“…Rpo-based phylogeny revealed both phyla-specific clades and rpo sequences that are shared between species of different phyla. This diversity of rpo sequences observed in the literature suggests a possible horizontal gene transfer between fungal species [ 203 , 204 , 205 ]. The mitochondrial codon usage for the AB species is similar to that reported for other ascomycete fungi [ 187 ].…”

“…Previous research found that rpo was only found in species belonging to the fungal phyla Ascomycota, Basidiomycota and Chytridiomycota. Although rpo homologs were found in both Ascomycota and Basidiomycota fungal species, this was only in 10% of the Ascomycota species (227) sampled, compared to 57% for Basidiomycota (116) [ 203 ]. This means that P. koolunga is among a small percentage of species within the Ascomycota phylum that harbours an rpo homolog.…”

Exploring Mitogenomes Diversity of Fusarium musae from Banana Fruits and Human Patients

“…Fungal mitochondrial genomes are typically small, circular and double-stranded DNA molecules, with a typical set of mitochondrial genes with identical gene order. Extensive mitochondrial genome comparisons within the fungal kingdom have shown that any gene has a mitochondrial localization in all fungal species [13], suggesting that the use of mitochondrial gene diversity cannot be applied as a universal marker for fungi. Nonetheless, the analysis of mitochondrial diversity can be successfully applied to differentiate species within orders [14] or species [15,16].…”