A first characterization of the microbiota-resilience link in swine
Abstract Background The gut microbiome plays a crucial role in understanding complex biological mechanisms, including host resilience to stressors. Investigating the microbiota-resilience link in animals and plants holds relevance in addressing challenges like adaptation of agricultural species to a...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-024-01771-7 |
| _version_ | 1797259173506842624 |
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| author | Enrico Mancin Christian Maltecca Yi Jian Huang Roberto Mantovani Francesco Tiezzi |
| author_facet | Enrico Mancin Christian Maltecca Yi Jian Huang Roberto Mantovani Francesco Tiezzi |
| author_sort | Enrico Mancin |
| collection | DOAJ |
| description | Abstract Background The gut microbiome plays a crucial role in understanding complex biological mechanisms, including host resilience to stressors. Investigating the microbiota-resilience link in animals and plants holds relevance in addressing challenges like adaptation of agricultural species to a warming environment. This study aims to characterize the microbiota-resilience connection in swine. As resilience is not directly observable, we estimated it using four distinct indicators based on daily feed consumption variability, assuming animals with greater intake variation may face challenges in maintaining stable physiological status. These indicators were analyzed both as linear and categorical variables. In our first set of analyses, we explored the microbiota-resilience link using PERMANOVA, α-diversity analysis, and discriminant analysis. Additionally, we quantified the ratio of estimated microbiota variance to total phenotypic variance (microbiability). Finally, we conducted a Partial Least Squares-Discriminant Analysis (PLS-DA) to assess the classification performance of the microbiota with indicators expressed in classes. Results This study offers four key insights. Firstly, among all indicators, two effectively captured resilience. Secondly, our analyses revealed robust relationship between microbial composition and resilience in terms of both composition and richness. We found decreased α-diversity in less-resilient animals, while specific amplicon sequence variants (ASVs) and KEGG pathways associated with inflammatory responses were negatively linked to resilience. Thirdly, considering resilience indicators in classes, we observed significant differences in microbial composition primarily in animals with lower resilience. Lastly, our study indicates that gut microbial composition can serve as a reliable biomarker for distinguishing individuals with lower resilience. Conclusion Our comprehensive analyses have highlighted the host-microbiota and resilience connection, contributing valuable insights to the existing scientific knowledge. The practical implications of PLS-DA and microbiability results are noteworthy. PLS-DA suggests that host-microbiota interactions could be utilized as biomarkers for monitoring resilience. Furthermore, the microbiability findings show that leveraging host-microbiota insights may improve the identification of resilient animals, supporting their adaptive capacity in response to changing environmental conditions. These practical implications offer promising avenues for enhancing animal well-being and adaptation strategies in the context of environmental challenges faced by livestock populations. Video Abstract |
| first_indexed | 2024-04-24T23:05:13Z |
| format | Article |
| id | doaj.art-b8e97635c47e4b058c552f9f61f51545 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-24T23:05:13Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-b8e97635c47e4b058c552f9f61f515452024-03-17T12:32:47ZengBMCMicrobiome2049-26182024-03-0112112610.1186/s40168-024-01771-7A first characterization of the microbiota-resilience link in swineEnrico Mancin0Christian Maltecca1Yi Jian Huang2Roberto Mantovani3Francesco Tiezzi4Department of Agronomy, Animals and Environment, (DAFNAE), Food, Natural Resources, University of PadovaDepartment of Animal Science, North Carolina State UniversitySmithfield Premium GeneticsDepartment of Agronomy, Animals and Environment, (DAFNAE), Food, Natural Resources, University of PadovaDepartment of Agriculture, Food, Environment and Forestry (DAGRI), University of FlorenceAbstract Background The gut microbiome plays a crucial role in understanding complex biological mechanisms, including host resilience to stressors. Investigating the microbiota-resilience link in animals and plants holds relevance in addressing challenges like adaptation of agricultural species to a warming environment. This study aims to characterize the microbiota-resilience connection in swine. As resilience is not directly observable, we estimated it using four distinct indicators based on daily feed consumption variability, assuming animals with greater intake variation may face challenges in maintaining stable physiological status. These indicators were analyzed both as linear and categorical variables. In our first set of analyses, we explored the microbiota-resilience link using PERMANOVA, α-diversity analysis, and discriminant analysis. Additionally, we quantified the ratio of estimated microbiota variance to total phenotypic variance (microbiability). Finally, we conducted a Partial Least Squares-Discriminant Analysis (PLS-DA) to assess the classification performance of the microbiota with indicators expressed in classes. Results This study offers four key insights. Firstly, among all indicators, two effectively captured resilience. Secondly, our analyses revealed robust relationship between microbial composition and resilience in terms of both composition and richness. We found decreased α-diversity in less-resilient animals, while specific amplicon sequence variants (ASVs) and KEGG pathways associated with inflammatory responses were negatively linked to resilience. Thirdly, considering resilience indicators in classes, we observed significant differences in microbial composition primarily in animals with lower resilience. Lastly, our study indicates that gut microbial composition can serve as a reliable biomarker for distinguishing individuals with lower resilience. Conclusion Our comprehensive analyses have highlighted the host-microbiota and resilience connection, contributing valuable insights to the existing scientific knowledge. The practical implications of PLS-DA and microbiability results are noteworthy. PLS-DA suggests that host-microbiota interactions could be utilized as biomarkers for monitoring resilience. Furthermore, the microbiability findings show that leveraging host-microbiota insights may improve the identification of resilient animals, supporting their adaptive capacity in response to changing environmental conditions. These practical implications offer promising avenues for enhancing animal well-being and adaptation strategies in the context of environmental challenges faced by livestock populations. Video Abstracthttps://doi.org/10.1186/s40168-024-01771-7Gut microbiotaPigsResilienceAnimal-health |
| spellingShingle | Enrico Mancin Christian Maltecca Yi Jian Huang Roberto Mantovani Francesco Tiezzi A first characterization of the microbiota-resilience link in swine Microbiome Gut microbiota Pigs Resilience Animal-health |
| title | A first characterization of the microbiota-resilience link in swine |
| title_full | A first characterization of the microbiota-resilience link in swine |
| title_fullStr | A first characterization of the microbiota-resilience link in swine |
| title_full_unstemmed | A first characterization of the microbiota-resilience link in swine |
| title_short | A first characterization of the microbiota-resilience link in swine |
| title_sort | first characterization of the microbiota resilience link in swine |
| topic | Gut microbiota Pigs Resilience Animal-health |
| url | https://doi.org/10.1186/s40168-024-01771-7 |
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