Gut microbes predominantly act as living beneficial partners rather than raw nutrients
Abstract Animals and their gut microbes mutually benefit their health. Nutrition plays a central role in this, directly influencing both host and microbial fitness and the nature of their interactions. This makes nutritional symbioses a complex and dynamic tri-system of diet-microbiota-host. Despite...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-07-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-38669-7 |
| _version_ | 1827890477003702272 |
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| author | Nuno Filipe da Silva Soares Andrea Quagliariello Seren Yigitturk Maria Elena Martino |
| author_facet | Nuno Filipe da Silva Soares Andrea Quagliariello Seren Yigitturk Maria Elena Martino |
| author_sort | Nuno Filipe da Silva Soares |
| collection | DOAJ |
| description | Abstract Animals and their gut microbes mutually benefit their health. Nutrition plays a central role in this, directly influencing both host and microbial fitness and the nature of their interactions. This makes nutritional symbioses a complex and dynamic tri-system of diet-microbiota-host. Despite recent discoveries on this field, full control over the interplay among these partners is challenging and hinders the resolution of fundamental questions, such as how to parse the gut microbes’ effect as raw nutrition or as symbiotic partners? To tackle this, we made use of the well-characterized Drosophila melanogaster/Lactiplantibacillus plantarum experimental model of nutritional symbiosis to generate a quantitative framework of gut microbes’ effect on the host. By coupling experimental assays and Random Forest analysis, we show that the beneficial effect of L. plantarum strains primarily results from the active relationship as symbionts rather than raw nutrients, regardless of the bacterial strain. Metabolomic analysis of both active and inactive bacterial cells further demonstrated the crucial role of the production of beneficial bacterial metabolites, such as N-acetylated-amino-acids, as result of active bacterial growth and function. Altogether, our results provide a ranking and quantification of the main bacterial features contributing to sustain animal growth. We demonstrate that bacterial activity is the predominant and necessary variable involved in bacteria-mediated benefit, followed by strain-specific properties and the nutritional potential of the bacterial cells. This contributes to elucidate the role of beneficial bacteria and probiotics, creating a broad quantitative framework for host-gut microbiome that can be expanded to other model systems. |
| first_indexed | 2024-03-12T21:10:14Z |
| format | Article |
| id | doaj.art-a47585e0c4a34c65abe32d3f3a5c0ffc |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-12T21:10:14Z |
| publishDate | 2023-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-a47585e0c4a34c65abe32d3f3a5c0ffc2023-07-30T11:14:50ZengNature PortfolioScientific Reports2045-23222023-07-0113111210.1038/s41598-023-38669-7Gut microbes predominantly act as living beneficial partners rather than raw nutrientsNuno Filipe da Silva Soares0Andrea Quagliariello1Seren Yigitturk2Maria Elena Martino3Department of Comparative Biomedicine and Food Science, University of PadovaDepartment of Comparative Biomedicine and Food Science, University of PadovaDepartment of Comparative Biomedicine and Food Science, University of PadovaDepartment of Comparative Biomedicine and Food Science, University of PadovaAbstract Animals and their gut microbes mutually benefit their health. Nutrition plays a central role in this, directly influencing both host and microbial fitness and the nature of their interactions. This makes nutritional symbioses a complex and dynamic tri-system of diet-microbiota-host. Despite recent discoveries on this field, full control over the interplay among these partners is challenging and hinders the resolution of fundamental questions, such as how to parse the gut microbes’ effect as raw nutrition or as symbiotic partners? To tackle this, we made use of the well-characterized Drosophila melanogaster/Lactiplantibacillus plantarum experimental model of nutritional symbiosis to generate a quantitative framework of gut microbes’ effect on the host. By coupling experimental assays and Random Forest analysis, we show that the beneficial effect of L. plantarum strains primarily results from the active relationship as symbionts rather than raw nutrients, regardless of the bacterial strain. Metabolomic analysis of both active and inactive bacterial cells further demonstrated the crucial role of the production of beneficial bacterial metabolites, such as N-acetylated-amino-acids, as result of active bacterial growth and function. Altogether, our results provide a ranking and quantification of the main bacterial features contributing to sustain animal growth. We demonstrate that bacterial activity is the predominant and necessary variable involved in bacteria-mediated benefit, followed by strain-specific properties and the nutritional potential of the bacterial cells. This contributes to elucidate the role of beneficial bacteria and probiotics, creating a broad quantitative framework for host-gut microbiome that can be expanded to other model systems.https://doi.org/10.1038/s41598-023-38669-7 |
| spellingShingle | Nuno Filipe da Silva Soares Andrea Quagliariello Seren Yigitturk Maria Elena Martino Gut microbes predominantly act as living beneficial partners rather than raw nutrients Scientific Reports |
| title | Gut microbes predominantly act as living beneficial partners rather than raw nutrients |
| title_full | Gut microbes predominantly act as living beneficial partners rather than raw nutrients |
| title_fullStr | Gut microbes predominantly act as living beneficial partners rather than raw nutrients |
| title_full_unstemmed | Gut microbes predominantly act as living beneficial partners rather than raw nutrients |
| title_short | Gut microbes predominantly act as living beneficial partners rather than raw nutrients |
| title_sort | gut microbes predominantly act as living beneficial partners rather than raw nutrients |
| url | https://doi.org/10.1038/s41598-023-38669-7 |
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