Metabolic enhancement contributed by horizontal gene transfer is essential for dietary specialization in leaf beetles

• 成果类型: Article
• 署名作者: Zhang, Yuxin; Tu, Chengjie; Bai, Jianyang; Li, Xiayu; Sun, Ziyue; Xu, Letian
• 署名单位: Hubei University; Anhui Agricultural University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9475
• DOI: 10.1073/pnas.2415717122
• 发表日期: 2025-01-07
• 关键词: enemy-free space; larval performance; host preference; oviposition; adaptation; EVOLUTION; herbivory; alignment; bacteria; TREE

摘要

Horizontal gene transfer (HGT) from bacteria to insects is widely reported and often associated with the adaptation and diversification of insects. However, compelling evidence demonstrating how HGT- conferred metabolic adjustments enable species to adapt to surrounding environment remains scarce. Dietary specialization is an important ecological strategy adopted by animals to reduce inter- and intraspecific competition for limited resources. Adults of the leaf beetle Plagiodera versicolora (Coleoptera) preferentially consume new leaves; nevertheless, we found that they selectively oviposit on mature leaves, thereby establishing a distinct dietary niche separation between adults and larvae. Based on the de novo assembled chromosome- level genome, we identified two horizontally transferred genes with cellulose degradation potential, belonging to the glycosyl hydrolase 48 family ( GH48- 1 and GH48-2). Prokaryotic expression of the HGTs confirmed the cellulose degradation capability of the two genes. Knockdown of GH48 significantly hampered the growth and survival rate of larvae feeding on mature leaves compared to wild- type larvae, with no similar effect observed in adults. Replenishing the GH48- expressing bacteria compensated for the knockdown of these two genes and recurred larval adaptability to mature leaves. Taken together, our results highlight the advantage and metabolic enhancement conferred by the two cellulose- degrading HGTs in P. versicolora larvae, enabling their development on cellulose- enriched mature leaves and underscoring the indispensable role of HGTs in facilitating the adaptation of leaf beetles to plants.