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 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.

Evidence for the independent evolution of a rectal complex within the beetle superfamily Scarabaeoidea

“…The ability of Scarabaeoidea species to digest highly resistant material such as lignocellulose is central to this, and relies on the symbiotic bacteria and yeasts within their guts (Ebert et al, 2021; Mishima and Araya, 2016; Shelomi et al, 2019; Tanahashi et al, 2017; Vargas-Asensio et al, 2014). For this reason Protaetia brevitarsis , a member of Cetoniinae farmed as a food source in East Asia, is being investigated for its ability to convert organic waste into fertiliser (Li et al, 2019; Wang et al, 2022). There is evidence from Pachnoda ephippiata (Cetoniinae) that their fresh faeces are rich in ammonia, which is a usable nitrogen source for plants (Li and Brune, 2007).…”

A holobiont approach towards polysaccharide degradation by the highly compartmentalised gut system of the soil-feeding higher termite Labiotermes labralis

“…As in the case of other soil-feeding insects (e.g. the Scarabaeidae beetle; [52]) and soil-feeding termites [7], bacterial biomass present in the soil matrix is hydrolysed, providing essential nutrients to the termite host. In addition, lysozymes excreted from the insect upper digestive tract, including the salivary glands, play a role in immune response [50].…”

“…Expression of the host lysozyme activity in the different gut compartments indicates that termites may simultaneously depend on their gut microbiota as mutualists and exploit them as a food source. In addition to providing essential nutrients to the host [52], a high bacterial biomass turnover could serve other purposes. First, the enzymes released from hydrolysing microbes present in soil or upper gut compartments, constitute a pool of "public goods" helping other microbes to degrade biomass faster [59].…”

A holobiont approach towards polysaccharide degradation by the highly compartmentalised gut system of the soil-feeding higher termite Labiotermes labralis

“…Expression of the host lysozyme activity in the different gut compartments indicates that termites may simultaneously depend on their gut microbiota as mutualists and exploit them as a food source. In addition to providing essential nutrients to the host [51], a high bacterial biomass turnover could serve other purposes. First, the enzymes released from hydrolysing microbes present in soil or upper gut compartments, constitute a pool of "public goods" helping other microbes to degrade biomass faster [59].…”