Abstract
The order Hypocreales (Ascomycota) is composed of ubiquitous and ecologically diverse fungi such as saprobes, biotrophs, and pathogens. Despite their phylogenetic relationship, these species exhibit high variability in biomolecules production, lifestyle, and fitness. The mitochondria play an important role in the fungal biology, providing energy to the cells and regulating diverse processes, such as immune response. In spite of its importance, the mechanisms that shape fungal mitogenomes are still poorly understood. Herein, we investigated the variability and evolution of mitogenomes and its relationship with the divergence time using the order Hypocreales as a study model. We sequenced and annotated for the first time Trichoderma harzianum mitochondrial genome (mtDNA), which was compared to other 34 mtDNAs species that were publicly available. Comparative analysis revealed a substantial structural and size variation on non-coding mtDNA regions, despite the conservation of copy number, length, and structure of protein-coding elements. Interestingly, we observed a highly significant correlation between mitogenome length, and the number and size of non-coding sequences in mitochondrial genome. Among the non-coding elements, group I and II introns and homing endonucleases genes (HEGs) were the main contributors to discrepancies in mitogenomes structure and length. Several intronic sequences displayed sequence similarity among species, and some of them are conserved even at gene position, and were present in the majority of mitogenomes, indicating its origin in a common ancestor. On the other hand, we also identified species-specific introns that advocate for the origin by different mechanisms. Investigation of mitochondrial gene transfer to the nuclear genome revealed that nuclear copies of the nad5 are the most frequent while atp8, atp9, and cox3 could not be identified in any of the nuclear genomes analyzed. Moreover, we also estimated the divergence time of each species and investigated its relationship with coding and non-coding elements as well as with the length of mitogenomes. Altogether, our results demonstrated that introns and HEGs are key elements on mitogenome shaping and its presence on fast-evolving mtDNAs could be mostly explained by its divergence time, although the intron sharing profile suggests the involvement of other mechanisms on the mitochondrial genome evolution, such as horizontal transference.
Highlights
The mitochondrion is an important organelle of eukaryotic cells, involved in multiple processes that are necessary for cell survival and reproduction
The mitogenome of T. harzianum isolate HB324 is a circular DNA molecule of 32,277 bp (Supplementary Text S2), GC content of 27.74%, composed of 14 genes related to the oxidative phosphorylation, 28 genes encoding for transfer RNAs, two ribosomal RNAs [one encoding to the small subunit and other for the large subunit] and the ribosomal gene encoding to rps3 protein
The species T. reesei has the largest mtDNA, even with a smaller number of fragmented genes when compared to T. harzianum (4); the Introns Group I (IGI) size accounts for almost 25% of its genome size
Summary
The mitochondrion is an important organelle of eukaryotic cells, involved in multiple processes that are necessary for cell survival and reproduction. It is responsible for the ATP production, the universal energy-transfer biomolecule in living organisms, through the oxidative phosphorylation pathway. In addition to respiratory metabolism and energy production function, mitochondria is involved in other processes such as senescence during the cell cycle and the maintenance of ion homeostasis (Burger et al, 2003; Basse, 2010; Chatre and Ricchetti, 2013). There are typically multiple copies of the genome, which replicate independently of the nuclear genome and cell cycle (Chatre and Ricchetti, 2013). Most of the mitochondrial genomes are composed of a single circular chromosome, some organisms contain linear mitochondrial genomes made up of multiple subunits (Burger et al, 2003)
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