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Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts
BACKGROUND: Sponges are ancient sessile metazoans, which form with their associated microbial symbionts a complex functional unit called a holobiont. Sponges are a rich source of chemical diversity; however, there is limited knowledge of which holobiont members produce certain metabolites and how th...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8805237/ https://www.ncbi.nlm.nih.gov/pubmed/35105377 http://dx.doi.org/10.1186/s40168-021-01220-9 |
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author | Zhang, Shan Song, Weizhi Nothias, Louis-Félix Couvillion, Sneha P. Webster, Nicole Thomas, Torsten |
author_facet | Zhang, Shan Song, Weizhi Nothias, Louis-Félix Couvillion, Sneha P. Webster, Nicole Thomas, Torsten |
author_sort | Zhang, Shan |
collection | PubMed |
description | BACKGROUND: Sponges are ancient sessile metazoans, which form with their associated microbial symbionts a complex functional unit called a holobiont. Sponges are a rich source of chemical diversity; however, there is limited knowledge of which holobiont members produce certain metabolites and how they may contribute to chemical interactions. To address this issue, we applied non-targeted liquid chromatography tandem mass spectrometry (LC-MS/MS) and gas chromatography mass spectrometry (GC-MS) to either whole sponge tissue or fractionated microbial cells from six different, co-occurring sponge species. RESULTS: Several metabolites were commonly found or enriched in whole sponge tissue, supporting the notion that sponge cells produce them. These include 2-methylbutyryl-carnitine, hexanoyl-carnitine and various carbohydrates, which may be potential food sources for microorganisms, as well as the antagonistic compounds hymenialdisine and eicosatrienoic acid methyl ester. Metabolites that were mostly observed or enriched in microbial cells include the antioxidant didodecyl 3,3′-thiodipropionate, the antagonistic compounds docosatetraenoic acid, and immune-suppressor phenylethylamide. This suggests that these compounds are mainly produced by the microbial members in the sponge holobiont, and are potentially either involved in inter-microbial competitions or in defenses against intruding organisms. CONCLUSIONS: This study shows how different chemical functionality is compartmentalized between sponge hosts and their microbial symbionts and provides new insights into how chemical interactions underpin the function of sponge holobionts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01220-9. |
format | Online Article Text |
id | pubmed-8805237 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-88052372022-02-03 Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan Song, Weizhi Nothias, Louis-Félix Couvillion, Sneha P. Webster, Nicole Thomas, Torsten Microbiome Research BACKGROUND: Sponges are ancient sessile metazoans, which form with their associated microbial symbionts a complex functional unit called a holobiont. Sponges are a rich source of chemical diversity; however, there is limited knowledge of which holobiont members produce certain metabolites and how they may contribute to chemical interactions. To address this issue, we applied non-targeted liquid chromatography tandem mass spectrometry (LC-MS/MS) and gas chromatography mass spectrometry (GC-MS) to either whole sponge tissue or fractionated microbial cells from six different, co-occurring sponge species. RESULTS: Several metabolites were commonly found or enriched in whole sponge tissue, supporting the notion that sponge cells produce them. These include 2-methylbutyryl-carnitine, hexanoyl-carnitine and various carbohydrates, which may be potential food sources for microorganisms, as well as the antagonistic compounds hymenialdisine and eicosatrienoic acid methyl ester. Metabolites that were mostly observed or enriched in microbial cells include the antioxidant didodecyl 3,3′-thiodipropionate, the antagonistic compounds docosatetraenoic acid, and immune-suppressor phenylethylamide. This suggests that these compounds are mainly produced by the microbial members in the sponge holobiont, and are potentially either involved in inter-microbial competitions or in defenses against intruding organisms. CONCLUSIONS: This study shows how different chemical functionality is compartmentalized between sponge hosts and their microbial symbionts and provides new insights into how chemical interactions underpin the function of sponge holobionts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01220-9. BioMed Central 2022-02-01 /pmc/articles/PMC8805237/ /pubmed/35105377 http://dx.doi.org/10.1186/s40168-021-01220-9 Text en © The Author(s) 2022 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 Zhang, Shan Song, Weizhi Nothias, Louis-Félix Couvillion, Sneha P. Webster, Nicole Thomas, Torsten Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts |
title | Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts |
title_full | Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts |
title_fullStr | Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts |
title_full_unstemmed | Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts |
title_short | Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts |
title_sort | comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8805237/ https://www.ncbi.nlm.nih.gov/pubmed/35105377 http://dx.doi.org/10.1186/s40168-021-01220-9 |
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