Phage origin of mitochondrion-localized family A DNA polymerases in kinetoplastids and diplonemids

Mitochondria retain their own genomes as other bacterial
endosymbiont-derived organelles. Nevertheless, no protein for DNA
replication and repair is encoded in any mitochondrial genomes (mtDNAs)
assessed to date, suggesting the nucleus primarily governs the maintenance
of mtDNA. As the proteins of diverse evolutionary origins occupy a large
proportion of the current mitochondrial proteomes, we anticipate finding
the same evolutionary trend in the nucleus-encoded machinery for mtDNA
maintenance. Indeed, none of the DNA polymerases (DNAPs) in the
mitochondrial endosymbiont, a putative α-proteobacterium, seemingly had
been inherited by their descendants (mitochondria), as none of the known
types of mitochondrion-localized DNAP showed a specific affinity to the
α-proteobacterial DNAPs. Nevertheless, we currently have no concrete idea
of how and when the known types of mitochondrion-localized DNAPs emerged.
We here explored the origins of mitochondrion-localized DNAPs after the
improvement of the samplings of DNAPs from bacteria and phages/viruses.
Past studies revealed that a set of mitochondrion-localized DNAPs in
kinetoplastids and diplonemids, namely PolIB, PolIC, PolID, PolI-Perk1/2,
and PolI-dipl (henceforth designated collectively as “PolIBCD+”) have
emerged from a single DNAP. In this study, we recovered an intimate
connection between PolIBCD+ and the DNAPs found in a particular group of
phages. Thus, the common ancestor of kinetoplastids and diplonemids most
likely converted a laterally acquired phage DNAP into a
mitochondrion-localized DNAP that was ancestral to PolIBCD+. The phage
origin of PolIBCD+ hints at a potentially large contribution of proteins
acquired via non-vertical processes to the machinery for mtDNA maintenance
in kinetoplastids and diplonemids.