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Peer-reviewedCC BYIMeta

Domesticated bacterial origin genes regulate homeostasis of the insect gut microbiome and empower adaptation

  • Zhenjia Zhang1,2,3
  • Yubo Zhang2
  • Kun Zhao2
  • Guangyuan Cheng1
  • Zhihao Lu2
  • Dongju Wang4
  • Yiqun Liu5
  • Jianguo Wu1
  • Liying Wang2
  • Lisheng Zhang6
  • Xinhai Ye7
  • Li Yu4
2 more authors
  • Wei Zhang2,8,9,10,11
  • Yi Li1
11 affiliations
  1. 1State Key Laboratory of Agricultural and Forestry Biosecurity, Vector‐borne Virus Research Center Fujian Agriculture and Forestry University Fuzhou China
  2. 2State Key Laboratory of Gene Function and Modulation Research, School of Life Sciences Peking University Beijing China
  3. 3College of Grassland Science and Technology China Agricultural University Beijing China
  4. 4The State Key Laboratory of Membrane Biology Tsinghua University‐Peking University Joint Centre for Life Sciences, Beijing Frontier Research Center for Biological Structure, School of Life Sciences, Tsinghua University Beijing China
  5. 5National Center for Protein Science and Core Facilities at School of Life Sciences Peking University Beijing China
  6. 6Key Laboratory of Natural Enemy Insects of Ministry of Agriculture and Rural Affairs, State Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant Protection, Chinese Academy of Agricultural Sciences Beijing China
  7. 7College of Advanced Agriculture Sciences Zhejiang A&F University Hangzhou China
  8. 8Peking‐Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies Peking University Beijing China
  9. 9Institute of Ecology Peking University Beijing China
  10. 10Peking University Chengdu Academy for Advanced Interdisciplinary Biotechnologies Chengdu China
  11. 11Medog Biodiversity Observation and Research Station of Xizang Autonomous Region Nyingchi China
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Abstract

Sap‐sucking insects, represented by the globally distributed leafhoppers, have evolved a wide range of adaptive traits and play multiple ecological roles. However, their successful survival strategies in nature remain poorly understood. To explore the adaptive mechanisms of sap‐sucking insects, we established a research system using three representative leafhopper species from the same family and found that they have acquired multiple cholesterol‐dependent cytolysins (CDCs) derived from gram‐positive bacterial genes. Furthermore, we demonstrated that these CDCs have been domesticated and co‐evolved with leafhoppers, ultimately participating in various life activities of the host. Specifically, some CDCs exhibit high cytotoxicity, are specifically expressed in the egg serosa, and affect the feeding behaviors of leafhopper predators; others show non‐cytotoxic activity, are specifically expressed in the gut, and may regulate leafhopper growth and development by potentially maintaining the homeostasis of the leafhopper gut microbiome. This study uncovers leafhoppers as a paradigm for understanding how organisms can borrow microbial innovations to address ecological challenges and thrive as agricultural pests. It provides a comprehensive perspective to bridge the genotypes of acquired genes with the phenotypes of adaptive traits and demonstrates how homologous genes from donor organisms undergo functional differentiation in recipient hosts, enabling them to exploit new ecological niches. By decoding these mechanisms, we not only gain fundamental insights into evolutionary processes but also develop powerful strategies for sustainable pest management.

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Cite

BibTeXRIS
BibTeX
@article{zhang2026domesticated,
  title = {{Domesticated bacterial origin genes regulate homeostasis of the insect gut microbiome and empower adaptation}},
  author = {Zhenjia Zhang and Yubo Zhang and Kun Zhao and Guangyuan Cheng and Zhihao Lu and Dongju Wang and Yiqun Liu and Jianguo Wu and Liying Wang and Lisheng Zhang and Xinhai Ye and Li Yu and Wei Zhang and Yi Li},
  journal = {IMeta},
  year = {2026},
  month = oct,
  doi = {10.1002/imt2.70179},
  url = {https://europepmc.org/article/PMC/PMC13670155},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Domesticated bacterial origin genes regulate homeostasis of the insect gut microbiome and empower adaptation
AU  - Zhenjia Zhang
AU  - Yubo Zhang
AU  - Kun Zhao
AU  - Guangyuan Cheng
AU  - Zhihao Lu
AU  - Dongju Wang
AU  - Yiqun Liu
AU  - Jianguo Wu
AU  - Liying Wang
AU  - Lisheng Zhang
AU  - Xinhai Ye
AU  - Li Yu
AU  - Wei Zhang
AU  - Yi Li
PY  - 2026
DA  - 2026/10/15
JO  - IMeta
DO  - 10.1002/imt2.70179
UR  - https://europepmc.org/article/PMC/PMC13670155
AB  - Sap‐sucking insects, represented by the globally distributed leafhoppers, have evolved a wide range of adaptive traits and play multiple ecological roles. However, their successful survival strategies in nature remain poorly understood. To explore the adaptive mechanisms of sap‐sucking insects, we established a research system using three representative leafhopper species from the same family and found that they have acquired multiple cholesterol‐dependent cytolysins (CDCs) derived from gram‐positive bacterial genes. Furthermore, we demonstrated that these CDCs have been domesticated and co‐evolved with leafhoppers, ultimately participating in various life activities of the host. Specifically, some CDCs exhibit high cytotoxicity, are specifically expressed in the egg serosa, and affect the feeding behaviors of leafhopper predators; others show non‐cytotoxic activity, are specifically expressed in the gut, and may regulate leafhopper growth and development by potentially maintaining the homeostasis of the leafhopper gut microbiome. This study uncovers leafhoppers as a paradigm for understanding how organisms can borrow microbial innovations to address ecological challenges and thrive as agricultural pests. It provides a comprehensive perspective to bridge the genotypes of acquired genes with the phenotypes of adaptive traits and demonstrates how homologous genes from donor organisms undergo functional differentiation in recipient hosts, enabling them to exploit new ecological niches. By decoding these mechanisms, we not only gain fundamental insights into evolutionary processes but also develop powerful strategies for sustainable pest management.
SN  - 2770-5986
SN  - 2770-596X
ER  -