State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China.
Hebei Key Laboratory of Soil Entomology, Cangzhou Academy of Agricultural and Forestry Sciences, Cangzhou, 061001, China.
Microbiome. 2022 Jun 13;10(1):90. doi: 10.1186/s40168-022-01291-2.
The Scarabaeidae insect Protaetia brevitarsis (PB) has recently gained increasing research interest as a resource insect because its larvae can effectively convert decaying organic matter to plant growth-promoting frass with a high humic acid content and produce healthy, nutritional insect protein sources. Lignocellulose is the main component of PB larvae (PBL) feed, but PB genome annotation shows that PBL carbohydrate-active enzymes are not able to complete the lignocellulose degradation process. Thus, the mechanism by which PBL efficiently degrade lignocellulose is worthy of further study.
Herein, we used combined host genomic and gut metagenomic datasets to investigate the lignocellulose degradation activity of PBL, and a comprehensive reference catalog of gut microbial genes and host gut transcriptomic genes was first established. We characterized a gene repertoire comprising highly abundant and diversified lignocellulose-degrading enzymes and demonstrated that there was unique teamwork between PBL and their gut bacterial microbiota for efficient lignocellulose degradation. PBL selectively enriched lignocellulose-degrading microbial species, mainly from Firmicutes and Bacteroidetes, which are capable of producing a broad array of cellulases and hemicellulases, thus playing a major role in lignocellulosic biomass degradation. In addition, most of the lignocellulose degradation-related module sequences in the PBL microbiome were novel. PBL provide organic functional complementarity for lignocellulose degradation via their evolved strong mouthparts, alkaline midgut, and mild stable hindgut microenvironment to facilitate lignocellulosic biomass grinding, dissolving, and symbiotic microbial fermentation, respectively.
This work shows that PBL are a promising model to study lignocellulose degradation, which can provide highly abundant novel enzymes and relevant lignocellulose-degrading bacterial strains for biotechnological biomass conversion industries. The unique teamwork between PBL and their gut symbiotic bacterial microbiota for efficient lignocellulose degradation will expand the knowledge of holobionts and open a new beginning in the theory of holobionts. Video Abstract.
蜣螂科昆虫暗黑金龟 Protaetia brevitarsis（PB）作为一种资源昆虫，其幼虫能有效地将腐烂的有机物转化为具有高腐殖酸含量的植物生长促进粪，并产生健康、有营养的昆虫蛋白源，最近受到越来越多的研究关注。木质纤维素是 PB 幼虫（PBL）饲料的主要成分，但 PB 基因组注释表明，PBL 碳水化合物活性酶不能完成木质纤维素的降解过程。因此，PBL 高效降解木质纤维素的机制值得进一步研究。
本文通过联合宿主基因组和肠道宏基因组数据集来研究 PBL 的木质纤维素降解活性，首次建立了肠道微生物基因和宿主肠道转录组基因的综合参考目录。我们对一个包含高度丰富和多样化木质纤维素降解酶的基因库进行了特征描述，并证明 PBL 与其肠道细菌微生物群之间存在独特的协同作用，以实现高效的木质纤维素降解。PBL 选择性富集木质纤维素降解微生物物种，主要来自厚壁菌门和拟杆菌门，它们能够产生广泛的纤维素酶和半纤维素酶，因此在木质纤维素生物质降解中起着主要作用。此外，PBL 微生物组中大多数与木质纤维素降解相关的模块序列是新的。PBL 通过进化而来的强大口器、碱性中肠和温和稳定的后肠微环境，为木质纤维素降解提供有机功能互补，分别促进木质纤维素生物质的研磨、溶解和共生微生物发酵。
这项工作表明，PBL 是研究木质纤维素降解的一个很有前途的模型，可以为生物技术生物质转化产业提供丰富的新型酶和相关木质纤维素降解细菌菌株。PBL 与其肠道共生细菌微生物群之间高效的木质纤维素降解的独特协同作用将扩展真核生物的知识，并为真核生物理论开辟一个新的开端。视频摘要。
