Decomposers play an important role in the biogeochemical cycle. Protaetia brevitarsis larvae (PBLs) can transform wastes into frass rich in humic acid (HA) and microorganisms, which may increase the disease resistance of plants and promote plant growth. Beyond HA, the microorganisms may also contribute to the biostimulant activity. To address this hypothesis, we investigated the potential microbial community in the PBL frass samples and elucidated their functions of disease resistance and plant growth promotion. High-throughput sequencing analysis of four PBL-relevant samples showed that their frass can influence the microbial community of the surrounding environment. Further analysis showed that there were many microorganisms beneficial to agriculture, such as Bacillus. Therefore, culturable Bacillus microbes were isolated from frass, and 16S rDNA gene analysis showed that Bacillus subtilis was the dominant species. In addition, some Bacillus microorganisms isolated from the PBL frass had antibacterial activities against pathogenic fungi. The plant growth promotion pot experiment also proved that some strains promote plant growth. In conclusion, this study demonstrated that the microorganisms in the PBL frass are conducive to colonizing the surrounding organic matrix, which will help beneficial microbes to increase the disease resistance of plants and promote plant growth.

Background 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. Results 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. Conclusions 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.

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.