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Microbiome-assisted carrion preservation aids larval development in a burying beetle
The ability to feed on a wide range of diets has enabled insects to diversify and colonize specialized niches. Carrion, for example, is highly susceptible to microbial decomposers, but is kept palatable several days after an animal’s death by carrion-feeding insects. Here we show that the burying be...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6217399/ https://www.ncbi.nlm.nih.gov/pubmed/30322931 http://dx.doi.org/10.1073/pnas.1812808115 |
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author | Shukla, Shantanu P. Plata, Camila Reichelt, Michael Steiger, Sandra Heckel, David G. Kaltenpoth, Martin Vilcinskas, Andreas Vogel, Heiko |
author_facet | Shukla, Shantanu P. Plata, Camila Reichelt, Michael Steiger, Sandra Heckel, David G. Kaltenpoth, Martin Vilcinskas, Andreas Vogel, Heiko |
author_sort | Shukla, Shantanu P. |
collection | PubMed |
description | The ability to feed on a wide range of diets has enabled insects to diversify and colonize specialized niches. Carrion, for example, is highly susceptible to microbial decomposers, but is kept palatable several days after an animal’s death by carrion-feeding insects. Here we show that the burying beetle Nicrophorus vespilloides preserves carrion by preventing the microbial succession associated with carrion decomposition, thus ensuring a high-quality resource for their developing larvae. Beetle-tended carcasses showed no signs of degradation and hosted a microbial community containing the beetles’ gut microbiota, including the yeast Yarrowia. In contrast, untended carcasses showed visual and olfactory signs of putrefaction, and their microbial community consisted of endogenous and soil-originating microbial decomposers. This regulation of the carcass’ bacterial and fungal community and transcriptomic profile was associated with lower concentrations of putrescine and cadaverine (toxic polyamines associated with carcass putrefaction) and altered levels of proteases, lipases, and free amino acids. Beetle-tended carcasses develop a biofilm-like matrix housing the yeast, which, when experimentally removed, leads to reduced larval growth. Thus, tended carcasses hosted a mutualistic microbial community that promotes optimal larval development, likely through symbiont-mediated extraintestinal digestion and detoxification of carrion nutrients. The adaptive preservation of carrion coordinated by the beetles and their symbionts demonstrates a specialized resource-management strategy through which insects modify their habitats to enhance fitness. |
format | Online Article Text |
id | pubmed-6217399 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-62173992018-11-06 Microbiome-assisted carrion preservation aids larval development in a burying beetle Shukla, Shantanu P. Plata, Camila Reichelt, Michael Steiger, Sandra Heckel, David G. Kaltenpoth, Martin Vilcinskas, Andreas Vogel, Heiko Proc Natl Acad Sci U S A Biological Sciences The ability to feed on a wide range of diets has enabled insects to diversify and colonize specialized niches. Carrion, for example, is highly susceptible to microbial decomposers, but is kept palatable several days after an animal’s death by carrion-feeding insects. Here we show that the burying beetle Nicrophorus vespilloides preserves carrion by preventing the microbial succession associated with carrion decomposition, thus ensuring a high-quality resource for their developing larvae. Beetle-tended carcasses showed no signs of degradation and hosted a microbial community containing the beetles’ gut microbiota, including the yeast Yarrowia. In contrast, untended carcasses showed visual and olfactory signs of putrefaction, and their microbial community consisted of endogenous and soil-originating microbial decomposers. This regulation of the carcass’ bacterial and fungal community and transcriptomic profile was associated with lower concentrations of putrescine and cadaverine (toxic polyamines associated with carcass putrefaction) and altered levels of proteases, lipases, and free amino acids. Beetle-tended carcasses develop a biofilm-like matrix housing the yeast, which, when experimentally removed, leads to reduced larval growth. Thus, tended carcasses hosted a mutualistic microbial community that promotes optimal larval development, likely through symbiont-mediated extraintestinal digestion and detoxification of carrion nutrients. The adaptive preservation of carrion coordinated by the beetles and their symbionts demonstrates a specialized resource-management strategy through which insects modify their habitats to enhance fitness. National Academy of Sciences 2018-10-30 2018-10-15 /pmc/articles/PMC6217399/ /pubmed/30322931 http://dx.doi.org/10.1073/pnas.1812808115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Shukla, Shantanu P. Plata, Camila Reichelt, Michael Steiger, Sandra Heckel, David G. Kaltenpoth, Martin Vilcinskas, Andreas Vogel, Heiko Microbiome-assisted carrion preservation aids larval development in a burying beetle |
title | Microbiome-assisted carrion preservation aids larval development in a burying beetle |
title_full | Microbiome-assisted carrion preservation aids larval development in a burying beetle |
title_fullStr | Microbiome-assisted carrion preservation aids larval development in a burying beetle |
title_full_unstemmed | Microbiome-assisted carrion preservation aids larval development in a burying beetle |
title_short | Microbiome-assisted carrion preservation aids larval development in a burying beetle |
title_sort | microbiome-assisted carrion preservation aids larval development in a burying beetle |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6217399/ https://www.ncbi.nlm.nih.gov/pubmed/30322931 http://dx.doi.org/10.1073/pnas.1812808115 |
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