Zhang Yuxin, Tu Chengjie, Bai Jianyang, Li Xiayu, Sun Ziyue, Xu Letian
State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan 430062, China.
Anhui Province Key Laboratory of Forest Resources and Silviculture, Anhui Province Laboratory of Microbial Control, Engineering Research Center of Fungal Biotechnology, Ministry of Education, School of Forestry and Landscape Architecture, Anhui Agricultural University, Hefei 230036, China.
Proc Natl Acad Sci U S A. 2025 Jan 7;122(1):e2415717122. doi: 10.1073/pnas.2415717122. Epub 2024 Dec 30.
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 (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 ( and ). 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 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.
细菌向昆虫的水平基因转移（HGT）已有广泛报道，且常与昆虫的适应性和多样化相关。然而，关于HGT赋予的代谢调节如何使物种适应周围环境的有力证据仍然匮乏。饮食特化是动物采用的一种重要生态策略，用于减少对有限资源的种间和种内竞争。叶甲（鞘翅目）成虫优先取食新叶；然而，我们发现它们会选择性地在成熟叶片上产卵，从而在成虫和幼虫之间建立了明显的饮食生态位分离。基于从头组装的染色体水平基因组，我们鉴定出两个具有纤维素降解潜力的水平转移基因，属于糖基水解酶48家族（ 和 ）。HGTs的原核表达证实了这两个基因的纤维素降解能力。与野生型幼虫相比，敲低GH48显著阻碍了以成熟叶片为食的幼虫的生长和存活率，而成虫未观察到类似影响。补充表达GH48的细菌弥补了这两个基因的敲低，并恢复了幼虫对成熟叶片的适应性。综上所述，我们的结果突出了两个纤维素降解HGTs赋予 幼虫的优势和代谢增强作用，使它们能够在富含纤维素的成熟叶片上发育，并强调了HGTs在促进叶甲适应植物方面的不可或缺的作用。
