The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on development

IntroductionRiptortus pedestris is a destructive pest that threatens multiple leguminous crops in China. The intestinal microbiota plays a crucial role in the growth and reproduction of host insects. However, the composition and function of the gut microbiota at different developmental stages remain...

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Main Authors: Yanbin Wang, Rong Li, Chunjing Wang, Ting Sun, Hongjuan Zhang, Fang Zhao, Jiehui Liu, Yuqiong Hao, Xiansheng Xie
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1517280/full
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author Yanbin Wang
Rong Li
Chunjing Wang
Ting Sun
Hongjuan Zhang
Fang Zhao
Jiehui Liu
Yuqiong Hao
Xiansheng Xie
author_facet Yanbin Wang
Rong Li
Chunjing Wang
Ting Sun
Hongjuan Zhang
Fang Zhao
Jiehui Liu
Yuqiong Hao
Xiansheng Xie
author_sort Yanbin Wang
collection DOAJ
description IntroductionRiptortus pedestris is a destructive pest that threatens multiple leguminous crops in China. The intestinal microbiota plays a crucial role in the growth and reproduction of host insects. However, the composition and function of the gut microbiota at different developmental stages remain unclear.MethodsHere, metagenomic sequencing was performed to clarify the gut microbial diversity and function in 2nd-, 3rd-, 4th-, and 5th- instar nymphs (2 N–5 N) and female adults (FAs) of R. pedestris and the effects of vital gut bacteria on development was detected. The gut bacteria have the stage specificity, indicating their function in the development of R. pedestris.ResultsEnterococcus and Caballerronia were the predominant bacteria present during the development of the 2 N–FAs. In addition, the microbial abundances in the 3 N and 4 N guts were significantly greater than those in the others guts. Furthermore, 5 N harbored the abundant microbiota Burkholderia-Paraburkholderia-Caballeronia. The metabolic pathways were significantly enriched from 2 N to FAs. Carbohydrate metabolism, including glycoside hydrolases (GHs) and glycosyl transferases (GTs), occurs throughout the entire developmental stage. Many antibiotic resistance genes (ARGs) were detected from 2 N to FAs. The bacteria from Pseudomonadota and Bacillota presented a broad spectrum of antibiotic resistance. Excitingly, Burkholderia bacteria eliminated by antibiotic treatment were unable to molt normally, and their lifespan was shortened in nymphs, indicating that the gut microbiota had a significant effect on nymph development.ConclusionIn summary, our results, for the first time, systematically illustrate the abundance and function across the gut microbiota from the different developmental stages of R. pedestris and demonstrate that the genera Burkholderia are crucial during the development of R. pedestris. This study provides the basis for stinkbug management strategies that focus on the pivotal gut microbiota.
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spelling doaj-art-9facd2223893494882867b2793116efd2025-01-28T22:20:09ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011610.3389/fmicb.2025.15172801517280The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on developmentYanbin Wang0Rong Li1Chunjing Wang2Ting Sun3Hongjuan Zhang4Fang Zhao5Jiehui Liu6Yuqiong Hao7Xiansheng Xie8Institute of Wheat Research, Shanxi Agricultural University, Linfen, Shanxi, ChinaInstitute of Wheat Research, Shanxi Agricultural University, Linfen, Shanxi, ChinaCollege of Plant Protection, Shanxi Agricultural University, Taigu, Shanxi, ChinaCollege of Plant Protection, Shanxi Agricultural University, Taigu, Shanxi, ChinaInstitute of Wheat Research, Shanxi Agricultural University, Linfen, Shanxi, ChinaInstitute of Wheat Research, Shanxi Agricultural University, Linfen, Shanxi, ChinaInstitute of Wheat Research, Shanxi Agricultural University, Linfen, Shanxi, ChinaKey Laboratory of Sustainable Dryland Agriculture (Coconstruction by Ministry and Province) Ministry of Agriculture and Rural Affairs, Institute of Wheat Research, Shanxi Agricultural University, Linfen, Shanxi, ChinaInstitute of Wheat Research, Shanxi Agricultural University, Linfen, Shanxi, ChinaIntroductionRiptortus pedestris is a destructive pest that threatens multiple leguminous crops in China. The intestinal microbiota plays a crucial role in the growth and reproduction of host insects. However, the composition and function of the gut microbiota at different developmental stages remain unclear.MethodsHere, metagenomic sequencing was performed to clarify the gut microbial diversity and function in 2nd-, 3rd-, 4th-, and 5th- instar nymphs (2 N–5 N) and female adults (FAs) of R. pedestris and the effects of vital gut bacteria on development was detected. The gut bacteria have the stage specificity, indicating their function in the development of R. pedestris.ResultsEnterococcus and Caballerronia were the predominant bacteria present during the development of the 2 N–FAs. In addition, the microbial abundances in the 3 N and 4 N guts were significantly greater than those in the others guts. Furthermore, 5 N harbored the abundant microbiota Burkholderia-Paraburkholderia-Caballeronia. The metabolic pathways were significantly enriched from 2 N to FAs. Carbohydrate metabolism, including glycoside hydrolases (GHs) and glycosyl transferases (GTs), occurs throughout the entire developmental stage. Many antibiotic resistance genes (ARGs) were detected from 2 N to FAs. The bacteria from Pseudomonadota and Bacillota presented a broad spectrum of antibiotic resistance. Excitingly, Burkholderia bacteria eliminated by antibiotic treatment were unable to molt normally, and their lifespan was shortened in nymphs, indicating that the gut microbiota had a significant effect on nymph development.ConclusionIn summary, our results, for the first time, systematically illustrate the abundance and function across the gut microbiota from the different developmental stages of R. pedestris and demonstrate that the genera Burkholderia are crucial during the development of R. pedestris. This study provides the basis for stinkbug management strategies that focus on the pivotal gut microbiota.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1517280/fullRiptortus pedestrisgut microbiotamicrobial functionantibiotic resistance genesdevelopment
spellingShingle Yanbin Wang
Rong Li
Chunjing Wang
Ting Sun
Hongjuan Zhang
Fang Zhao
Jiehui Liu
Yuqiong Hao
Xiansheng Xie
The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on development
Frontiers in Microbiology
Riptortus pedestris
gut microbiota
microbial function
antibiotic resistance genes
development
title The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on development
title_full The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on development
title_fullStr The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on development
title_full_unstemmed The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on development
title_short The intestinal microbial community and function of Riptortus pedestris at different developmental stages and its effects on development
title_sort intestinal microbial community and function of riptortus pedestris at different developmental stages and its effects on development
topic Riptortus pedestris
gut microbiota
microbial function
antibiotic resistance genes
development
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1517280/full
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