Primase-polymerases (PrimPols) play divergent functions from DNA replication to DNA repair in all three life domains. In archaea and bacteria, numerous and diverse PPs are encoded by mobile genetic elements (MGEs) and act as the replicases for their MGEs. However, their varying activities and functions are not fully understood. In this study, we characterized a group of PrimPols that are genetically associated with prokaryotic argonaute proteins (pAgos). The pAgo-associated PrimPol (AgaPP) is likely derived from a MGE. AgaPP has polymerase and primase activities and physically interacts with a helicase encoded by its downstream gene, suggesting that they constitute a functional replication module. Further, AgaPP performs translesion DNA synthesis, terminal transfer and microhomology-mediated end joining (MMEJ), showing striking similarity to human DNA repair polymerase θ. AgaPP can promote the MMEJ repair of Cas9-induced double-stranded DNA breaks and increase cell survival post DNA damage in Escherichia coli. In addition, the MMEJ activity of AgaPP can be repurposed to assist DNA assembly in vitro. Together, the findings reveal dual role of AgaPP in both DNA replication and repair.
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