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Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?

BACKGROUND: The insect gut microbiota has been shown to contribute to the host’s digestion, detoxification, development, pathogen resistance, and physiology. However, there is poor information about the ranking of these roles. Most of these results were obtained with cultivable bacteria, whereas the...

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Autores principales: Jing, Tian-Zhong, Qi, Feng-Hui, Wang, Zhi-Ying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7077154/
https://www.ncbi.nlm.nih.gov/pubmed/32178739
http://dx.doi.org/10.1186/s40168-020-00823-y
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author Jing, Tian-Zhong
Qi, Feng-Hui
Wang, Zhi-Ying
author_facet Jing, Tian-Zhong
Qi, Feng-Hui
Wang, Zhi-Ying
author_sort Jing, Tian-Zhong
collection PubMed
description BACKGROUND: The insect gut microbiota has been shown to contribute to the host’s digestion, detoxification, development, pathogen resistance, and physiology. However, there is poor information about the ranking of these roles. Most of these results were obtained with cultivable bacteria, whereas the bacterial physiology may be different between free-living and midgut-colonizing bacteria. In this study, we provided both proteomic and genomic evidence on the ranking of the roles of gut bacteria by investigating the anal droplets from a weevil, Cryptorhynchus lapathi. RESULTS: The gut lumen and the anal droplets showed qualitatively and quantitatively different subsets of bacterial communities. The results of 16S rRNA sequencing showed that the gut lumen is dominated by Proteobacteria and Bacteroidetes, whereas the anal droplets are dominated by Proteobacteria. From the anal droplets, enzymes involved in 31 basic roles that belong to 7 super roles were identified by Q-TOF MS. The cooperation between the weevil and its gut bacteria was determined by reconstructing community pathway maps, which are defined in this study. A score was used to rank the gut bacterial roles. The results from the proteomic data indicate that the most dominant role of gut bacteria is amino acid biosynthesis, followed by protein digestion, energy metabolism, vitamin biosynthesis, lipid digestion, plant secondary metabolite (PSM) degradation, and carbohydrate digestion, while the order from the genomic data is amino acid biosynthesis, vitamin biosynthesis, lipid digestion, energy metabolism, protein digestion, PSM degradation, and carbohydrate digestion. The PCA results showed that the gut bacteria form functional groups from the point of view of either the basic role or super role, and the MFA results showed that there are functional variations among gut bacteria. In addition, the variations between the proteomic and genomic data, analyzed with the HMFA method from the point of view of either the bacterial community or individual bacterial species, are presented. CONCLUSION: The most dominant role of gut bacteria is essential nutrient provisioning, followed by digestion and detoxification. The weevil plays a pioneering role in diet digestion and mainly digests macromolecules into smaller molecules which are then mainly digested by gut bacteria.
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spelling pubmed-70771542020-03-19 Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision? Jing, Tian-Zhong Qi, Feng-Hui Wang, Zhi-Ying Microbiome Research BACKGROUND: The insect gut microbiota has been shown to contribute to the host’s digestion, detoxification, development, pathogen resistance, and physiology. However, there is poor information about the ranking of these roles. Most of these results were obtained with cultivable bacteria, whereas the bacterial physiology may be different between free-living and midgut-colonizing bacteria. In this study, we provided both proteomic and genomic evidence on the ranking of the roles of gut bacteria by investigating the anal droplets from a weevil, Cryptorhynchus lapathi. RESULTS: The gut lumen and the anal droplets showed qualitatively and quantitatively different subsets of bacterial communities. The results of 16S rRNA sequencing showed that the gut lumen is dominated by Proteobacteria and Bacteroidetes, whereas the anal droplets are dominated by Proteobacteria. From the anal droplets, enzymes involved in 31 basic roles that belong to 7 super roles were identified by Q-TOF MS. The cooperation between the weevil and its gut bacteria was determined by reconstructing community pathway maps, which are defined in this study. A score was used to rank the gut bacterial roles. The results from the proteomic data indicate that the most dominant role of gut bacteria is amino acid biosynthesis, followed by protein digestion, energy metabolism, vitamin biosynthesis, lipid digestion, plant secondary metabolite (PSM) degradation, and carbohydrate digestion, while the order from the genomic data is amino acid biosynthesis, vitamin biosynthesis, lipid digestion, energy metabolism, protein digestion, PSM degradation, and carbohydrate digestion. The PCA results showed that the gut bacteria form functional groups from the point of view of either the basic role or super role, and the MFA results showed that there are functional variations among gut bacteria. In addition, the variations between the proteomic and genomic data, analyzed with the HMFA method from the point of view of either the bacterial community or individual bacterial species, are presented. CONCLUSION: The most dominant role of gut bacteria is essential nutrient provisioning, followed by digestion and detoxification. The weevil plays a pioneering role in diet digestion and mainly digests macromolecules into smaller molecules which are then mainly digested by gut bacteria. BioMed Central 2020-03-16 /pmc/articles/PMC7077154/ /pubmed/32178739 http://dx.doi.org/10.1186/s40168-020-00823-y Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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
Jing, Tian-Zhong
Qi, Feng-Hui
Wang, Zhi-Ying
Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?
title Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?
title_full Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?
title_fullStr Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?
title_full_unstemmed Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?
title_short Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?
title_sort most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7077154/
https://www.ncbi.nlm.nih.gov/pubmed/32178739
http://dx.doi.org/10.1186/s40168-020-00823-y
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