Horizontal transfer of tRNA genes to mitochondrial plasmids facilitates gene loss from fungal mitochondrial DNA

Abstract

Fungal and plant mitochondria are known to exchange DNA with retroviral plasmids. Transfer of plasmid DNA to the organellar genome is best known and occurs through wholesale insertion of the plasmid. Less well known is the transfer of organellar DNA to plasmids, in particular tRNA genes. Presently, it is unknown whether fungal plasmids can adopt mitochondrial functions such as tRNA production through horizontal gene transfer. In this paper, we studied the exchange of DNA between fungal linear plasmids and fungal mtDNA, mainly focusing on the basidiomycete family Lyophyllaceae. We report at least six independent transfers of complete tRNA genes to fungal plasmids. Furthermore, we discovered two independent cases of loss of a tRNA gene from a fungal mitochondrial genome following transfer of such a gene to a linear mitochondrial plasmid. We propose that loss of a tRNA gene from mtDNA following its transfer to a plasmid creates a mutualistic dependency of the host mtDNA on the plasmid. We also find that tRNA genes transferred to plasmids encode codons that occur at the lowest frequency in the host mitochondrial genomes, possibly due to a higher number of unused transcripts. We discuss the potential consequences of mtDNA transfer to plasmids for both the host mtDNA and the plasmid.

A cryptic plastid and a novel mitochondrial plasmid inLeucomyxa plasmidiferagen. and sp. nov. (Ochrophyta) push the frontiers of organellar biology

“…Furthermore, the acceptor stem has only six rather than canonical seven paired nucleotides, lacking the top pair. It is noteworthy that tRNA genes were previously identified in some fungal and plant mitochondrial plasmids, and that in some cases the gene for the respective tRNA species has been lost from the mitogenome of the same organism, indicating dependence of the mitochondrial translation on the plasmid-specified tRNA (Nieuwenhuis et al 2023). The only essential tRNA species lacking a corresponding gene in the Leuc.…”

Insights into Fungal Mitochondrial Genomes and Inheritance Based on Current Findings from Yeast-like Fungi

“…Interestingly, some mitochondrial plasmids, which contain ORFs of reverse transcriptase or DNA/RNA polymerase and exist in the mitochondria of fungi, have the ability to integrate either wholly or partially into the mitochondrial genome of their host, thus becoming a kind of mobile element. Evidence of the transfer of gene fragments and tRNA fragments between mitochondrial plasmids and mitochondrial genomes has been found in some species of Neurospora, Podospora, Agaricus, Termitomyces, and Moniliophthora [58][59][60][61][62]. Surprisingly, the occurrence of DNA fragment transfer between mitochondrial plasmids and mitochondrial genomes has been found to be associated with fungal growth and aging in Neurospora and Podospora [63,64].…”

“…The replication mechanism of fungal mtDNA is mainly studied in yeast, whereas it is less understood than in humans [58][59][60][61][62]. Except for the similar mechanism of RNAprimed replication in humans, yeast has developed alternative ways by coupling recombination and rolling circle replication [63,64].…”