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Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species

Mammalian chemosignals—or scent marks—are characterized by astounding chemical diversity, reflecting both complex biochemical pathways that produce them and rich information exchange with conspecifics. The microbiome of scent glands was thought to play prominent role in the chemical signal synthesis...

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Autores principales: Zhou, Wenliang, Qi, Dunwu, Swaisgood, Ronald R., Wang, Le, Jin, Yipeng, Wu, Qi, Wei, Fuwen, Nie, Yonggang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245644/
https://www.ncbi.nlm.nih.gov/pubmed/33568789
http://dx.doi.org/10.1038/s41396-021-00905-1
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author Zhou, Wenliang
Qi, Dunwu
Swaisgood, Ronald R.
Wang, Le
Jin, Yipeng
Wu, Qi
Wei, Fuwen
Nie, Yonggang
author_facet Zhou, Wenliang
Qi, Dunwu
Swaisgood, Ronald R.
Wang, Le
Jin, Yipeng
Wu, Qi
Wei, Fuwen
Nie, Yonggang
author_sort Zhou, Wenliang
collection PubMed
description Mammalian chemosignals—or scent marks—are characterized by astounding chemical diversity, reflecting both complex biochemical pathways that produce them and rich information exchange with conspecifics. The microbiome of scent glands was thought to play prominent role in the chemical signal synthesis, with diverse microbiota metabolizing glandular products to produce odorants that may be used as chemosignals. Here, we use gas chromatography–mass spectrometry and metagenomic shotgun sequencing to explore this phenomenon in the anogenital gland secretions (AGS) of the giant panda (Ailuropoda melanoleuca). We find that this gland contains a diverse community of fermentative bacteria with enzymes that support metabolic pathways (e.g., lipid degradation) for the productions of volatile odorants specialized for chemical communication. We found quantitative and qualitative differences in the microbiota between AGS and digestive tract, a finding which was mirrored by differences among chemical compounds that could be used for olfactory communication. Volatile chemical compounds were more diverse and abundant in AGS than fecal samples, and our evidence suggests that metabolic pathways have been specialized for the synthesis of chemosignals for communication. The panda’s microbiome is rich with genes coding for enzymes that participate in the fermentation pathways producing chemical compounds commonly deployed in mammalian chemosignals. These findings illuminate the poorly understood phenomena involved in the role of symbiotic bacteria in the production of chemosignals.
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spelling pubmed-82456442021-07-20 Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species Zhou, Wenliang Qi, Dunwu Swaisgood, Ronald R. Wang, Le Jin, Yipeng Wu, Qi Wei, Fuwen Nie, Yonggang ISME J Article Mammalian chemosignals—or scent marks—are characterized by astounding chemical diversity, reflecting both complex biochemical pathways that produce them and rich information exchange with conspecifics. The microbiome of scent glands was thought to play prominent role in the chemical signal synthesis, with diverse microbiota metabolizing glandular products to produce odorants that may be used as chemosignals. Here, we use gas chromatography–mass spectrometry and metagenomic shotgun sequencing to explore this phenomenon in the anogenital gland secretions (AGS) of the giant panda (Ailuropoda melanoleuca). We find that this gland contains a diverse community of fermentative bacteria with enzymes that support metabolic pathways (e.g., lipid degradation) for the productions of volatile odorants specialized for chemical communication. We found quantitative and qualitative differences in the microbiota between AGS and digestive tract, a finding which was mirrored by differences among chemical compounds that could be used for olfactory communication. Volatile chemical compounds were more diverse and abundant in AGS than fecal samples, and our evidence suggests that metabolic pathways have been specialized for the synthesis of chemosignals for communication. The panda’s microbiome is rich with genes coding for enzymes that participate in the fermentation pathways producing chemical compounds commonly deployed in mammalian chemosignals. These findings illuminate the poorly understood phenomena involved in the role of symbiotic bacteria in the production of chemosignals. Nature Publishing Group UK 2021-02-10 2021-07 /pmc/articles/PMC8245644/ /pubmed/33568789 http://dx.doi.org/10.1038/s41396-021-00905-1 Text en © The Author(s) 2021 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Zhou, Wenliang
Qi, Dunwu
Swaisgood, Ronald R.
Wang, Le
Jin, Yipeng
Wu, Qi
Wei, Fuwen
Nie, Yonggang
Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
title Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
title_full Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
title_fullStr Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
title_full_unstemmed Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
title_short Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
title_sort symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245644/
https://www.ncbi.nlm.nih.gov/pubmed/33568789
http://dx.doi.org/10.1038/s41396-021-00905-1
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