Metatranscriptomic analysis uncovers prevalent viral ORFs compatible with mitochondrial translation

RNA viruses are ubiquitous components of the global virosphere, yet
relatively little is known about their genetic diversity or the cellular
mechanisms by which they exploit the biology of their diverse eukaryotic
hosts. A hallmark of (+)ssRNA (positive single-stranded RNA) viruses is
the ability to remodel host endomembranes for their own replication.
However, the subcellular interplay between RNA viruses and host organelles
that harbor gene expression systems, such as mitochondria, is complex and
poorly understood. Here we report the discovery of 763 new virus sequences
belonging to the family Mitoviridae by metatranscriptomic
analysis, the identification of previously uncharacterized mitovirus
clades, and a putative new viral class. With this expanded understanding
of the diversity of mitovirus and encoded RNA-dependent RNA polymerases
(RdRps), we annotate mitovirus-specific protein motifs and identify
hallmarks of mitochondrial translation, including mitochondrion-specific
codons. This study expands the known diversity of mitochondrial viruses
and provides additional evidence that they co-opt mitochondrial biology
for their survival. Metatranscriptomic studies have rapidly expanded the
cadre of known RNA viruses, yet our understanding of how these viruses
navigate the cytoplasmic milieu of their hosts to survive remains poorly
characterized. In this study, we identify and assemble 763 new viral
sequences belonging to the Mitoviridae, a family of (+)ssRNA
viruses thought to interact with and remodel host mitochondria. We exploit
this genetic diversity to identify new clades of Mitoviridae,
annotate clade-specific sequence motifs that distinguish the mitoviral
RdRp, and reveal patterns of RdRp codon usage consistent with translation
on host cell mitoribosomes. These results serve as a foundation for
understanding how mitoviruses co-opt mitochondrial biology for their
proliferation.