Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs
ABSTRACT Understanding the mechanisms of microbiome assembly during host development is crucial for successful modulation of the gut microbiome to improve host health and growth. However, results from previous microbial intervention studies to improve swine growth have largely been inconsistent due...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01722-23 |
| _version_ | 1797393575148781568 |
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| author | Wenxuan Dong Nicole Ricker Devin B. Holman Timothy A. Johnson |
| author_facet | Wenxuan Dong Nicole Ricker Devin B. Holman Timothy A. Johnson |
| author_sort | Wenxuan Dong |
| collection | DOAJ |
| description | ABSTRACT Understanding the mechanisms of microbiome assembly during host development is crucial for successful modulation of the gut microbiome to improve host health and growth. However, results from previous microbial intervention studies to improve swine growth have largely been inconsistent due to the constantly changing nature of the gut microbiota and limited longitudinal sampling. Detailed characterization of the swine gut microbiota through meta-analysis allows us to understand the dynamics of microbial community succession, as well as the transient and natural variations between time points and animals. A total of 3,313 fecal microbial communities from over 349 pigs covering 60 time points (from birth to market age) from 14 publications were included in this meta-analysis. Despite differences in animal breeds and management, generalizable patterns of community assembly were identified. Alpha diversity continuously increased during early stages of animal growth and more slowly in the later stages. Beta regression analysis revealed that more microbial taxa were enriched, while fewer were excluded by the gut microbiota. The microbial community structure also changed significantly between days at early ages and became more similar as pigs aged, as revealed by dissimilarity and distance metrics. Dirichlet multinomial mixtures analysis supported gradient microbial clustering in longitudinal pig fecal samples, and we found that the early samples spread to more clusters than those from older pigs. Random forest regression identified 30 operational taxonomic units as potential microbial biomarkers for modeling swine gut microbiota development. External validation showed this model could be generalized to future microbiome studies conducted in suckling and weaning pigs and adds to the toolkit to quantify community succession. IMPORTANCE The swine gut microbiome undergoes an age-dependent assembly pattern with a developmental phase at early ages and a stabilization phase at later ages. Shorter time intervals and a wider range of data sources provided a clearer understanding of the gut microbiota colonization and succession and their associations with pig growth and development. The rapidly changing microbiota of suckling and weaning pigs implies potential time targets for growth and health regulation through gut microbiota manipulation. Since swine gut microbiota development is predictable, swine microbiota age can be calculated and compared between animal treatment groups rather than relying only on static time-matched comparisons. |
| first_indexed | 2024-03-09T00:04:41Z |
| format | Article |
| id | doaj.art-0842362ea6704d8c8137a1b32efd2808 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:04:41Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-0842362ea6704d8c8137a1b32efd28082023-12-12T13:17:21ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.01722-23Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigsWenxuan Dong0Nicole Ricker1Devin B. Holman2Timothy A. Johnson3Department of Animal Sciences, Purdue University , West Lafayette, Indiana, USADepartment of Pathobiology, University of Guelph , Guelph, Ontario, CanadaLacombe Research and Development Centre, Agriculture and Agri-Food Canada , Lacombe, Alberta, CanadaDepartment of Animal Sciences, Purdue University , West Lafayette, Indiana, USAABSTRACT Understanding the mechanisms of microbiome assembly during host development is crucial for successful modulation of the gut microbiome to improve host health and growth. However, results from previous microbial intervention studies to improve swine growth have largely been inconsistent due to the constantly changing nature of the gut microbiota and limited longitudinal sampling. Detailed characterization of the swine gut microbiota through meta-analysis allows us to understand the dynamics of microbial community succession, as well as the transient and natural variations between time points and animals. A total of 3,313 fecal microbial communities from over 349 pigs covering 60 time points (from birth to market age) from 14 publications were included in this meta-analysis. Despite differences in animal breeds and management, generalizable patterns of community assembly were identified. Alpha diversity continuously increased during early stages of animal growth and more slowly in the later stages. Beta regression analysis revealed that more microbial taxa were enriched, while fewer were excluded by the gut microbiota. The microbial community structure also changed significantly between days at early ages and became more similar as pigs aged, as revealed by dissimilarity and distance metrics. Dirichlet multinomial mixtures analysis supported gradient microbial clustering in longitudinal pig fecal samples, and we found that the early samples spread to more clusters than those from older pigs. Random forest regression identified 30 operational taxonomic units as potential microbial biomarkers for modeling swine gut microbiota development. External validation showed this model could be generalized to future microbiome studies conducted in suckling and weaning pigs and adds to the toolkit to quantify community succession. IMPORTANCE The swine gut microbiome undergoes an age-dependent assembly pattern with a developmental phase at early ages and a stabilization phase at later ages. Shorter time intervals and a wider range of data sources provided a clearer understanding of the gut microbiota colonization and succession and their associations with pig growth and development. The rapidly changing microbiota of suckling and weaning pigs implies potential time targets for growth and health regulation through gut microbiota manipulation. Since swine gut microbiota development is predictable, swine microbiota age can be calculated and compared between animal treatment groups rather than relying only on static time-matched comparisons.https://journals.asm.org/doi/10.1128/spectrum.01722-23swine gut microbiomelongitudinaldynamic developmentmicrobiota agecommunity succession |
| spellingShingle | Wenxuan Dong Nicole Ricker Devin B. Holman Timothy A. Johnson Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs Microbiology Spectrum swine gut microbiome longitudinal dynamic development microbiota age community succession |
| title | Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs |
| title_full | Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs |
| title_fullStr | Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs |
| title_full_unstemmed | Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs |
| title_short | Meta-analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs |
| title_sort | meta analysis reveals the predictable dynamic development of the gut microbiota in commercial pigs |
| topic | swine gut microbiome longitudinal dynamic development microbiota age community succession |
| url | https://journals.asm.org/doi/10.1128/spectrum.01722-23 |
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