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Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens

Carrion beetles, Nicrophorus vespilloides, are reared on decomposing carrion where larvae are exposed to high populations of carcass‐derived bacteria. Larvae do not become colonized with these bacteria but instead are colonized with the gut microbiome of their parents, suggesting that bacteria in th...

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Autores principales: Wang, Yin, Rozen, Daniel E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792511/
https://www.ncbi.nlm.nih.gov/pubmed/29435240
http://dx.doi.org/10.1002/ece3.3589
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author Wang, Yin
Rozen, Daniel E.
author_facet Wang, Yin
Rozen, Daniel E.
author_sort Wang, Yin
collection PubMed
description Carrion beetles, Nicrophorus vespilloides, are reared on decomposing carrion where larvae are exposed to high populations of carcass‐derived bacteria. Larvae do not become colonized with these bacteria but instead are colonized with the gut microbiome of their parents, suggesting that bacteria in the beetle microbiome outcompete the carcass‐derived species for larval colonization. Here, we test this hypothesis and quantify the fitness consequences of colonization with different bacterial symbionts. First, we show that beetles colonized by their endogenous microbiome produce heavier broods than those colonized with carcass‐bacteria. Next, we show that bacteria from the endogenous microbiome, including Providencia rettgeri and Morganella morganii, are better colonizers of the beetle gut and can outcompete nonendogenous species, including Serratia marcescens and Escherichia coli, during in vivo competition. Finally, we find that Providencia and Morganella provide beetles with colonization resistance against Serratia and thereby reduce Serratia‐induced larval mortality. This effect is eliminated in larvae first colonized by Serratia, suggesting that while competition within the larval gut is determined by priority effects, these effects are less important for Serratia‐induced mortality. Our work suggests that an unappreciated benefit of parental care in N. vespilloides is the social transmission of the microbiome from parents to offspring.
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spelling pubmed-57925112018-02-12 Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens Wang, Yin Rozen, Daniel E. Ecol Evol Original Research Carrion beetles, Nicrophorus vespilloides, are reared on decomposing carrion where larvae are exposed to high populations of carcass‐derived bacteria. Larvae do not become colonized with these bacteria but instead are colonized with the gut microbiome of their parents, suggesting that bacteria in the beetle microbiome outcompete the carcass‐derived species for larval colonization. Here, we test this hypothesis and quantify the fitness consequences of colonization with different bacterial symbionts. First, we show that beetles colonized by their endogenous microbiome produce heavier broods than those colonized with carcass‐bacteria. Next, we show that bacteria from the endogenous microbiome, including Providencia rettgeri and Morganella morganii, are better colonizers of the beetle gut and can outcompete nonendogenous species, including Serratia marcescens and Escherichia coli, during in vivo competition. Finally, we find that Providencia and Morganella provide beetles with colonization resistance against Serratia and thereby reduce Serratia‐induced larval mortality. This effect is eliminated in larvae first colonized by Serratia, suggesting that while competition within the larval gut is determined by priority effects, these effects are less important for Serratia‐induced mortality. Our work suggests that an unappreciated benefit of parental care in N. vespilloides is the social transmission of the microbiome from parents to offspring. John Wiley and Sons Inc. 2018-01-05 /pmc/articles/PMC5792511/ /pubmed/29435240 http://dx.doi.org/10.1002/ece3.3589 Text en © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Wang, Yin
Rozen, Daniel E.
Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens
title Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens
title_full Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens
title_fullStr Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens
title_full_unstemmed Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens
title_short Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens
title_sort gut microbiota in the burying beetle, nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792511/
https://www.ncbi.nlm.nih.gov/pubmed/29435240
http://dx.doi.org/10.1002/ece3.3589
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