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

• 成果类型: Article
• 署名作者: Ling, Xiaoyu; Guo, Huijuan; Di, Jian; Xie, Liqiang; Zhu-Salzman, Keyan; Ge, Feng; Zhao, Zihua; Sun, Yucheng
• 署名单位: Chinese Academy of Sciences; Institute of Zoology, CAS; Chinese Academy of Sciences; University of Chinese Academy of Sciences, CAS; Texas A&M University System; Texas A&M University College Station; Shandong Academy of Agricultural Sciences; China Agricultural University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-8543
• DOI: 10.1073/pnas.2415651121
• 发表日期: 2024-12-13
• 关键词: sequence determinants; thermal tolerance; escherichia-coli; mismatch repair; pea aphid; in-vivo; EVOLUTION; gene; expression; promoter

摘要

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 Buchnera aphidicola, 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 ibpA is extremely prone to mismatching error, e.g., a single adenine deletion, which impairs the induction of ibpA under heat stress. Coinfection with a facultative endosymbiont Serratia symbiotica remarkably reduced the mutagenesis rate in the Buchnera genome and potentially prevented a single adenine deletion in ibpA promoter, thereby alleviating the heat vulnerability of aphid bacteriocytes. Furthermore, Serratia encoded mutH, a conserved core protein of prokaryotic DNA mismatch repair (MMR), accessed to Buchnera cells, which complemented Buchnera mutt 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.