Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs

Abstract Background The true bugs (Heteroptera) occupy nearly all of the known ecological niches of insects. Among them, as a group containing more than 30,000 species, the phytophagous true bugs are making increasing impacts on agricultural and forestry ecosystems. Previous studies proved that symb...

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Published in:Microbiome
Main Authors: Zi-Wen Yang, Jiu-Yang Luo, Yu Men, Zhi-Hui Liu, Zi-Kai Zheng, Yan-Hui Wang, Qiang Xie
Format: Article
Language:English
Published: BMC 2023-11-01
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Online Access:https://doi.org/10.1186/s40168-023-01702-y
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author Zi-Wen Yang
Jiu-Yang Luo
Yu Men
Zhi-Hui Liu
Zi-Kai Zheng
Yan-Hui Wang
Qiang Xie
author_facet Zi-Wen Yang
Jiu-Yang Luo
Yu Men
Zhi-Hui Liu
Zi-Kai Zheng
Yan-Hui Wang
Qiang Xie
author_sort Zi-Wen Yang
collection DOAJ
container_title Microbiome
description Abstract Background The true bugs (Heteroptera) occupy nearly all of the known ecological niches of insects. Among them, as a group containing more than 30,000 species, the phytophagous true bugs are making increasing impacts on agricultural and forestry ecosystems. Previous studies proved that symbiotic bacteria play important roles in these insects in fitting various habitats. However, it is still obscure about the evolutionary and ecological patterns of the microorganisms of phytophagous true bugs as a whole with comprehensive taxon sampling. Results Here, in order to explore the symbiotic patterns between plant-feeding true bugs and their symbiotic microorganisms, 209 species belonging to 32 families of 9 superfamilies had been sampled, which covered all the major phytophagous families of true bugs. The symbiotic microbial communities were surveyed by full-length 16S rRNA gene and ITS amplicons respectively for bacteria and fungi using the PacBio platform. We revealed that hosts mainly affect the dominant bacteria of symbiotic microbial communities, while habitats generally influence the subordinate ones. Thereafter, we carried out the ancestral state reconstruction of the dominant bacteria and found that dramatic replacements of dominant bacteria occurred in the early Cretaceous and formed newly stable symbiotic relationships accompanying the radiation of insect families. In contrast, the symbiotic fungi were revealed to be horizontally transmitted, which makes fungal communities distinctive in different habitats but not significantly related to hosts. Conclusions Host and habitat determine microbial communities of plant-feeding true bugs in different roles. The symbiotic bacterial communities are both shaped by host and habitat but in different ways. Nevertheless, the symbiotic fungal communities are mainly influenced by habitat but not host. These findings shed light on a general framework for future microbiome research of phytophagous insects. Video Abstract
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spelling doaj-art-997ac64e72f449c19a56426f3e6a2d182025-08-19T22:12:26ZengBMCMicrobiome2049-26182023-11-0111111210.1186/s40168-023-01702-yDifferent roles of host and habitat in determining the microbial communities of plant-feeding true bugsZi-Wen Yang0Jiu-Yang Luo1Yu Men2Zhi-Hui Liu3Zi-Kai Zheng4Yan-Hui Wang5Qiang Xie6School of Life Sciences, State Key Laboratory of Biocontrol, Sun Yat-sen UniversitySchool of Life Sciences, State Key Laboratory of Biocontrol, Sun Yat-sen UniversitySchool of Life Sciences, Zhaoqing UniversitySchool of Life Sciences, State Key Laboratory of Biocontrol, Sun Yat-sen UniversitySchool of Life Sciences, State Key Laboratory of Biocontrol, Sun Yat-sen UniversitySchool of Life Sciences, State Key Laboratory of Biocontrol, Sun Yat-sen UniversitySchool of Life Sciences, State Key Laboratory of Biocontrol, Sun Yat-sen UniversityAbstract Background The true bugs (Heteroptera) occupy nearly all of the known ecological niches of insects. Among them, as a group containing more than 30,000 species, the phytophagous true bugs are making increasing impacts on agricultural and forestry ecosystems. Previous studies proved that symbiotic bacteria play important roles in these insects in fitting various habitats. However, it is still obscure about the evolutionary and ecological patterns of the microorganisms of phytophagous true bugs as a whole with comprehensive taxon sampling. Results Here, in order to explore the symbiotic patterns between plant-feeding true bugs and their symbiotic microorganisms, 209 species belonging to 32 families of 9 superfamilies had been sampled, which covered all the major phytophagous families of true bugs. The symbiotic microbial communities were surveyed by full-length 16S rRNA gene and ITS amplicons respectively for bacteria and fungi using the PacBio platform. We revealed that hosts mainly affect the dominant bacteria of symbiotic microbial communities, while habitats generally influence the subordinate ones. Thereafter, we carried out the ancestral state reconstruction of the dominant bacteria and found that dramatic replacements of dominant bacteria occurred in the early Cretaceous and formed newly stable symbiotic relationships accompanying the radiation of insect families. In contrast, the symbiotic fungi were revealed to be horizontally transmitted, which makes fungal communities distinctive in different habitats but not significantly related to hosts. Conclusions Host and habitat determine microbial communities of plant-feeding true bugs in different roles. The symbiotic bacterial communities are both shaped by host and habitat but in different ways. Nevertheless, the symbiotic fungal communities are mainly influenced by habitat but not host. These findings shed light on a general framework for future microbiome research of phytophagous insects. Video Abstracthttps://doi.org/10.1186/s40168-023-01702-yPhytophagous true bugsAmplicon sequencingSymbiotic bacteriaSymbiotic fungiMicrobial communityThird-generation sequencing
spellingShingle Zi-Wen Yang
Jiu-Yang Luo
Yu Men
Zhi-Hui Liu
Zi-Kai Zheng
Yan-Hui Wang
Qiang Xie
Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs
Phytophagous true bugs
Amplicon sequencing
Symbiotic bacteria
Symbiotic fungi
Microbial community
Third-generation sequencing
title Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs
title_full Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs
title_fullStr Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs
title_full_unstemmed Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs
title_short Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs
title_sort different roles of host and habitat in determining the microbial communities of plant feeding true bugs
topic Phytophagous true bugs
Amplicon sequencing
Symbiotic bacteria
Symbiotic fungi
Microbial community
Third-generation sequencing
url https://doi.org/10.1186/s40168-023-01702-y
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