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Except for the presence of base excision repair (BER) and two double\u2010strand break repair (DSBR) proteins in mitochondria, the mechanisms for preservation of mtDNA integrity during traversal of the parasite through different cell types and environments in the mosquito vector and mammalian host are not characterized. We identified two putative organellar exonucleases in\n                    <jats:italic>Plasmodium falciparum<\/jats:italic>\n                    ,\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit1<\/jats:sub>\n                    and\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit2<\/jats:sub>\n                    , with homologs present only within certain alveolates. Immunofluorescence localization and chromatin immunoprecipitation experiments using antibodies generated against recombinant proteins showed that they are localized to the mitochondrion.\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit1<\/jats:sub>\n                    and\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit2<\/jats:sub>\n                    demonstrated specificity for different DNA substrates;\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit1<\/jats:sub>\n                    cleaved ssDNA in both polarities, while\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit2<\/jats:sub>\n                    was a bipolar exonuclease on dsDNA with 3\u2032\u20105\u2032 exonuclease activity on ssDNA. The mismatch repair (MMR) protein\n                    <jats:italic>Pf<\/jats:italic>\n                    MutS, which carries an additional endonuclease domain, was localized in the mitochondria and interacted with\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit2<\/jats:sub>\n                    in pull\u2010down assays.\n                    <jats:italic>Pf<\/jats:italic>\n                    Exo\n                    <jats:sub>mit2<\/jats:sub>\n                    also interacted with the mitochondria\u2010targeted DSBR protein\n                    <jats:italic>Pf<\/jats:italic>\n                    Rad51, suggesting that it is a component of both MMR and DSBR pathways. When Exo\n                    <jats:sub>mit1<\/jats:sub>\n                    expression in the rodent parasite\n                    <jats:italic>P. berghei<\/jats:italic>\n                    was silenced in sporozoites via conditional mutagenesis,\n                    <jats:italic>Pb<\/jats:italic>\n                    Exo\n                    <jats:sub>mit1<\/jats:sub>\n                    conditional knockout sporozoites invaded hepatocytes and developed in the liver, but could not transition to the blood stage.\n                    <jats:italic>Pb<\/jats:italic>\n                    Exo\n                    <jats:sub>mit1<\/jats:sub>\n                    localized to the mitochondria in liver stages as well, indicating that its ssDNA exonuclease function in mtDNA processing in the liver impacted establishment of blood\u2010stage infection.\n                  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