Cargando…
Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line
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 inse...
Autores principales: | , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9195238/ https://www.ncbi.nlm.nih.gov/pubmed/35698170 http://dx.doi.org/10.1186/s40168-022-01291-2 |
_version_ | 1784726925799849984 |
---|---|
author | Wang, Kui Gao, Peiwen Geng, Lili Liu, Chunqin Zhang, Jie Shu, Changlong |
author_facet | Wang, Kui Gao, Peiwen Geng, Lili Liu, Chunqin Zhang, Jie Shu, Changlong |
author_sort | Wang, Kui |
collection | PubMed |
description | 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01291-2. |
format | Online Article Text |
id | pubmed-9195238 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-91952382022-06-15 Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line Wang, Kui Gao, Peiwen Geng, Lili Liu, Chunqin Zhang, Jie Shu, Changlong Microbiome Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01291-2. BioMed Central 2022-06-13 /pmc/articles/PMC9195238/ /pubmed/35698170 http://dx.doi.org/10.1186/s40168-022-01291-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Wang, Kui Gao, Peiwen Geng, Lili Liu, Chunqin Zhang, Jie Shu, Changlong Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line |
title | Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line |
title_full | Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line |
title_fullStr | Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line |
title_full_unstemmed | Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line |
title_short | Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line |
title_sort | lignocellulose degradation in protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9195238/ https://www.ncbi.nlm.nih.gov/pubmed/35698170 http://dx.doi.org/10.1186/s40168-022-01291-2 |
work_keys_str_mv | AT wangkui lignocellulosedegradationinprotaetiabrevitarsislarvaedigestivetractrefiningonatightlydesignedmicrobialfermentationproductionline AT gaopeiwen lignocellulosedegradationinprotaetiabrevitarsislarvaedigestivetractrefiningonatightlydesignedmicrobialfermentationproductionline AT genglili lignocellulosedegradationinprotaetiabrevitarsislarvaedigestivetractrefiningonatightlydesignedmicrobialfermentationproductionline AT liuchunqin lignocellulosedegradationinprotaetiabrevitarsislarvaedigestivetractrefiningonatightlydesignedmicrobialfermentationproductionline AT zhangjie lignocellulosedegradationinprotaetiabrevitarsislarvaedigestivetractrefiningonatightlydesignedmicrobialfermentationproductionline AT shuchanglong lignocellulosedegradationinprotaetiabrevitarsislarvaedigestivetractrefiningonatightlydesignedmicrobialfermentationproductionline |