Mitochondrial Genome of Phlebia radiata Is the Second Largest (156 kbp) among Fungi and Features Signs of Genome Flexibility and Recent Recombination Events

Abstract

Mitochondria are eukaryotic organelles supporting individual life-style via generation of proton motive force and cellular energy, and indispensable metabolic pathways. As part of genome sequencing of the white rot Basidiomycota species Phlebia radiata, we first assembled its mitochondrial genome (mtDNA). So far, the 156 348 bp mtDNA is the second largest described for fungi, and of considerable size among eukaryotes. The P. radiata mtDNA assembled as single circular dsDNA molecule containing genes for the large and small ribosomal RNAs, 28 transfer RNAs, and over 100 open reading frames encoding the 14 fungal conserved protein subunits of the mitochondrial complexes I, III, IV, and V. Two genes (atp6 and tRNA-IleGAU) were duplicated within 6.1 kbp inverted region, which is a unique feature of the genome. The large mtDNA size, however, is explained by the dominance of intronic and intergenic regions (sum 80% of mtDNA sequence). The intergenic DNA stretches harness short (≤200 nt) repetitive, dispersed and overlapping sequence elements in abundance. Long self-splicing introns of types I and II interrupt eleven of the conserved genes (cox1,2,3; cob; nad1,2,4,4L,5; rnl; rns). The introns embrace a total of 57 homing endonucleases with LAGLIDADGD and GYI-YIG core motifs, which makes P. radiata mtDNA to one of the largest known reservoirs of intron-homing endonucleases. The inverted duplication, intergenic stretches, and intronic features are indications of dynamics and genetic flexibility of the mtDNA, not fully recognized to this extent in fungal mitochondrial genomes previously, thus giving new insights for the evolution of organelle genomes in eukaryotes.

Comparative genomics in plant fungal pathogens (Mycosphaerellaceae): variation in mitochondrial composition due to at least five independent intron invasions

“…We attribute differences in gene order to genomic rearrangements, which could be caused by different processes, such as fusion, fission, recombination, plasmid integration and mobility among mitochondrial genomes (Kawano, Takano and Kuroiwa, 1995). Indeed, plasmid integration appears to have a role in recombination thanks to the presence of long inverted repeats that allows homologous recombination (Salavirta et al, 2014). There are no broad studies comparing mitochondrial gene order among closely related species of fungi.…”

Evidence of extensive intraspecific noncoding reshuffling in a 169-kb mitochondrial genome of a basidiomycetous fungus

“…In Organelle Genome Resources NCBI, only six species are larger than P. noxium (Losada, et al 2014; Mardanov, et al 2014; Kanzi, et al 2016; Nowrousian 2016). Gain of introns have been depicted as the main constituents of the enlargement of fungal mitogenomes (Losada, et al 2014; Mardanov, et al 2014; Salavirta, et al 2014; Kanzi, et al 2016). In the case of Hymenochaetales, three out of the six species hold an impressively high number of introns (table 1).…”

Occurrence of Fungal DNA Contamination in PCR Reagents: Approaches to Control and Decontamination

“…Contaminating DNA from three fungal species, including C. victoriae, M. restricta, and P. radiata, was identified by ITS2 amplicon sequencing and alignment analysis using the GenBank database. P. radiata, a lignin-degrading white-rot fungus that colonizes dead wood in Eurasian and North American forests (19), and C. victoriae, a psychrophilic yeast that was first isolated in the Antarctica (20) but has also been found in samples retrieved in Europe, North and South America, and Asia (21), seem to be widely distributed environmental fungi and may therefore represent common contaminating organisms. In contrast, the presence of M. restricta DNA indicates an anthropogenic origin since this species is associated with the human skin (22).…”