A complete DNA repair system assembled by two endosymbionts restores heat tolerance of the insect host

DNA repair systems are essential to maintain genome integrity and stability. Some obligate endosymbionts that experience long-term symbiosis with the insect hosts, however, have lost their key components for DNA repair. It is largely unexplored how the bacterial endosymbionts cope with the increased demand for mismatch repairs under heat stresses. Here, we showed that ibpA, a small heat shock protein encoded by <i>Buchnera aphidicola</i>, directly interacted with the cytoskeletal actin to prevent its aggregation in bacteriocytes, thus reinforcing the stability of bacteriocytes. However, the succession of 11 adenines in the promoter of <i>ibpA</i> is extremely prone to mismatching error, e.g., a single adenine deletion, which impairs the induction of <i>ibpA</i> under heat stress. Coinfection with a facultative endosymbiont <i>Serratia symbiotica</i> remarkably reduced the mutagenesis rate in the <i>Buchnera</i> genome and potentially prevented a single adenine deletion in <i>ibpA</i> promoter, thereby alleviating the heat vulnerability of aphid bacteriocytes. Furthermore, <i>Serratia</i> encoded mutH, a conserved core protein of prokaryotic DNA mismatch repair (MMR), accessed to <i>Buchnera</i> cells, which complemented <i>Buchnera</i> mutL and mutS in constituting an active MMR. Our findings imply that a full complement of a prokaryotic MMR system assembled by two bacterial endosymbionts contributes significantly to the thermostability of aphid bacteriocytes in an ibpA-dependent manner, furnishing a distinct molecular link among tripartite symbioses in shaping resilience and adaptation of their insect hosts to occupy other ecological niches.