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When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis

BACKGROUND: The life cycles of many insect species include an obligatory or facultative diapause stage with arrested development and low metabolic activity as an overwintering strategy. Diapause is characterised by profound physiological changes in endocrine activity, cell proliferation and nutrient...

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Autores principales: Dittmer, Jessica, Brucker, Robert M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8035746/
https://www.ncbi.nlm.nih.gov/pubmed/33836829
http://dx.doi.org/10.1186/s40168-021-01037-6
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author Dittmer, Jessica
Brucker, Robert M.
author_facet Dittmer, Jessica
Brucker, Robert M.
author_sort Dittmer, Jessica
collection PubMed
description BACKGROUND: The life cycles of many insect species include an obligatory or facultative diapause stage with arrested development and low metabolic activity as an overwintering strategy. Diapause is characterised by profound physiological changes in endocrine activity, cell proliferation and nutrient metabolism. However, little is known regarding host-microbiome interactions during diapause, despite the importance of bacterial symbionts for host nutrition and development. In this work, we investigated (i) the role of the microbiome for host nutrient allocation during diapause and (ii) the impact of larval diapause on microbiome dynamics in the parasitoid wasp Nasonia vitripennis, a model organism for host-microbiome interactions. RESULTS: Our results demonstrate that the microbiome is essential for host nutrient allocation during diapause in N. vitripennis, as axenic diapausing larvae had consistently lower glucose and glycerol levels than conventional diapausing larvae, especially when exposed to cold temperature. In turn, microbiome composition was altered in diapausing larvae, potentially due to changes in the surrounding temperature, host nutrient levels and a downregulation of host immune genes. Importantly, prolonged larval diapause had a transstadial effect on the adult microbiome, with unknown consequences for host fitness. Notably, the most dominant microbiome member, Providencia sp., was drastically reduced in adults after more than 4 months of larval diapause, while potential bacterial pathogens increased in abundance. CONCLUSION: This work investigates host-microbiome interactions during a crucial developmental stage, which challenges both the insect host and its microbial associates. The impact of diapause on the microbiome is likely due to several factors, including altered host regulatory mechanisms and changes in the host environment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01037-6.
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spelling pubmed-80357462021-04-12 When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis Dittmer, Jessica Brucker, Robert M. Microbiome Research BACKGROUND: The life cycles of many insect species include an obligatory or facultative diapause stage with arrested development and low metabolic activity as an overwintering strategy. Diapause is characterised by profound physiological changes in endocrine activity, cell proliferation and nutrient metabolism. However, little is known regarding host-microbiome interactions during diapause, despite the importance of bacterial symbionts for host nutrition and development. In this work, we investigated (i) the role of the microbiome for host nutrient allocation during diapause and (ii) the impact of larval diapause on microbiome dynamics in the parasitoid wasp Nasonia vitripennis, a model organism for host-microbiome interactions. RESULTS: Our results demonstrate that the microbiome is essential for host nutrient allocation during diapause in N. vitripennis, as axenic diapausing larvae had consistently lower glucose and glycerol levels than conventional diapausing larvae, especially when exposed to cold temperature. In turn, microbiome composition was altered in diapausing larvae, potentially due to changes in the surrounding temperature, host nutrient levels and a downregulation of host immune genes. Importantly, prolonged larval diapause had a transstadial effect on the adult microbiome, with unknown consequences for host fitness. Notably, the most dominant microbiome member, Providencia sp., was drastically reduced in adults after more than 4 months of larval diapause, while potential bacterial pathogens increased in abundance. CONCLUSION: This work investigates host-microbiome interactions during a crucial developmental stage, which challenges both the insect host and its microbial associates. The impact of diapause on the microbiome is likely due to several factors, including altered host regulatory mechanisms and changes in the host environment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01037-6. BioMed Central 2021-04-09 /pmc/articles/PMC8035746/ /pubmed/33836829 http://dx.doi.org/10.1186/s40168-021-01037-6 Text en © The Author(s) 2021 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
Dittmer, Jessica
Brucker, Robert M.
When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis
title When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis
title_full When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis
title_fullStr When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis
title_full_unstemmed When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis
title_short When your host shuts down: larval diapause impacts host-microbiome interactions in Nasonia vitripennis
title_sort when your host shuts down: larval diapause impacts host-microbiome interactions in nasonia vitripennis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8035746/
https://www.ncbi.nlm.nih.gov/pubmed/33836829
http://dx.doi.org/10.1186/s40168-021-01037-6
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