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Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits

BACKGROUND: Heat tolerance is a distinct abiotic factor affecting the distribution and abundance of insects. Gut microbiota can contribute to host fitness, thereby increasing resistance to abiotic stress conditions. In this study, Sarcophaga peregrina is closely associated with human life in ecologi...

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Autores principales: Ren, Lipin, Zhang, Xiangyan, Yang, Fengqin, Jocelin, Ngando Fernand, Shang, Yanjie, Wang, Qing, Liu, Zhuoying, Guo, Yadong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580603/
https://www.ncbi.nlm.nih.gov/pubmed/37848940
http://dx.doi.org/10.1186/s13071-023-05973-0
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author Ren, Lipin
Zhang, Xiangyan
Yang, Fengqin
Jocelin, Ngando Fernand
Shang, Yanjie
Wang, Qing
Liu, Zhuoying
Guo, Yadong
author_facet Ren, Lipin
Zhang, Xiangyan
Yang, Fengqin
Jocelin, Ngando Fernand
Shang, Yanjie
Wang, Qing
Liu, Zhuoying
Guo, Yadong
author_sort Ren, Lipin
collection PubMed
description BACKGROUND: Heat tolerance is a distinct abiotic factor affecting the distribution and abundance of insects. Gut microbiota can contribute to host fitness, thereby increasing resistance to abiotic stress conditions. In this study, Sarcophaga peregrina is closely associated with human life in ecological habits and shows remarkable adaptability to daily and seasonal temperature fluctuations. To date, the role of gut microbiota in S. peregrina response to heat stress and its influence on the host phenotypic variability remain poorly studied. METHODS: We exposed S. peregrina to heat stress at 40 °C for 3 h every day throughout the developmental stages from newly hatched larva to adult, after which gut DNA was extracted from third-instar larvae, early pupal stage, late pupal stage, and newly emerged adults, respectively. Then, 16S rRNA microbial community analyses were performed. RESULTS: Firstly, we analyzed whether heat stress could have an impact on the life history traits of S. peregrina and showed that the growth rate of larvae was higher and the developmental time was significantly shorter after heat stress. We then proposed the role of the gut microbiota in the heat tolerance of S. peregrina, which indicated that the bacterial abundance and community structure changed significantly after heat tolerance. In particular, the relative abundance of Wohlfahrtiimonas and Ignatzschineria was higher in the third-instar larval larvae; the former increased and the latter decreased significantly after heat stress. To further explore the effect of disturbing the microbial community on thermotolerant phenotype, newly hatched larvae were fed with amikacin under heat stress, which indicated that the larval length and the whole developmental cycle was significantly shorter. CONCLUSION: This study indicated that Wohlfahrtiimonas and Ignatzschineria should play an important role in the post-feeding stage under heat stress, but further study is still needed. In general, heat tolerance can affect the gut microbial community structure, which in turn affects the fitness of the host. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05973-0.
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spelling pubmed-105806032023-10-18 Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits Ren, Lipin Zhang, Xiangyan Yang, Fengqin Jocelin, Ngando Fernand Shang, Yanjie Wang, Qing Liu, Zhuoying Guo, Yadong Parasit Vectors Research BACKGROUND: Heat tolerance is a distinct abiotic factor affecting the distribution and abundance of insects. Gut microbiota can contribute to host fitness, thereby increasing resistance to abiotic stress conditions. In this study, Sarcophaga peregrina is closely associated with human life in ecological habits and shows remarkable adaptability to daily and seasonal temperature fluctuations. To date, the role of gut microbiota in S. peregrina response to heat stress and its influence on the host phenotypic variability remain poorly studied. METHODS: We exposed S. peregrina to heat stress at 40 °C for 3 h every day throughout the developmental stages from newly hatched larva to adult, after which gut DNA was extracted from third-instar larvae, early pupal stage, late pupal stage, and newly emerged adults, respectively. Then, 16S rRNA microbial community analyses were performed. RESULTS: Firstly, we analyzed whether heat stress could have an impact on the life history traits of S. peregrina and showed that the growth rate of larvae was higher and the developmental time was significantly shorter after heat stress. We then proposed the role of the gut microbiota in the heat tolerance of S. peregrina, which indicated that the bacterial abundance and community structure changed significantly after heat tolerance. In particular, the relative abundance of Wohlfahrtiimonas and Ignatzschineria was higher in the third-instar larval larvae; the former increased and the latter decreased significantly after heat stress. To further explore the effect of disturbing the microbial community on thermotolerant phenotype, newly hatched larvae were fed with amikacin under heat stress, which indicated that the larval length and the whole developmental cycle was significantly shorter. CONCLUSION: This study indicated that Wohlfahrtiimonas and Ignatzschineria should play an important role in the post-feeding stage under heat stress, but further study is still needed. In general, heat tolerance can affect the gut microbial community structure, which in turn affects the fitness of the host. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05973-0. BioMed Central 2023-10-17 /pmc/articles/PMC10580603/ /pubmed/37848940 http://dx.doi.org/10.1186/s13071-023-05973-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Ren, Lipin
Zhang, Xiangyan
Yang, Fengqin
Jocelin, Ngando Fernand
Shang, Yanjie
Wang, Qing
Liu, Zhuoying
Guo, Yadong
Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits
title Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits
title_full Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits
title_fullStr Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits
title_full_unstemmed Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits
title_short Effects of heat tolerance on the gut microbiota of Sarcophaga peregrina (Diptera: Sarcophagidae) and impacts on the life history traits
title_sort effects of heat tolerance on the gut microbiota of sarcophaga peregrina (diptera: sarcophagidae) and impacts on the life history traits
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580603/
https://www.ncbi.nlm.nih.gov/pubmed/37848940
http://dx.doi.org/10.1186/s13071-023-05973-0
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