Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line

Abstract

Background The Scarabaeidae insect Protaetia brevitarsis (PB) has recently gained increasing research interest as resource insects, because its larvae can effectively use various organic matter ranging from decaying plant residues to humus and livestock waste and convert those compounds to nonphytotoxic and high humic acid content frass fertilizer, as well as healthy nutritional insect protein sources. Lignocellulose is the main component of PB larvae (PBLs) food sources. PBLs show high lignin and polysaccharide degradation efficiency; however, genome annotation shows that PBLs’ carbohydrate-active enzymes (CAZymes) are not able to complete the lignocellulose degradation process. Therefore, the mechanism by which PBLs efficiently degrade lignocellulose is a worthy issue for further study. Results Here, we used a combined host genomic and gut metagenomic datasets to investigate the lignocellulose degradation activity of PBLs. First, a comprehensive gut gene catalog comprising gut microbial genes and host gut transcriptomic genes was established. The data showed that PBLs 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. Gene annotation revealed PBLs gut microbiome encoded a full spectrum of CAZymes involving in the hydrolysis of lignocellulose (including 39,969 CAZymes), while the host only expressed 33 lignocellulose degradation-related CAZymes in the guts. The PBL hosts provide lignin pretreatment processes via their evolved strong mouthparts as well as a strong alkaline environment in the midgut, which thus complements the lack of laccases in the PBL holobiont. In addition, most of the lignocellulose degradation-related gene sequences in the PBL microbiome were novel, and most of the recovered high-quality genome bins with independent (hemi)cellulose degradation capability from the PBL gut microbiome were novel species. Conclusions This work shows that there is a unique teamwork between PBLs and their gut bacterial flora for efficient lignocellulose degradation. PBLs 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.