Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics use
IntroductionPost-weaning diarrhoea (PWD) is a multifactorial disease that affects piglets after weaning, contributing to productive and economic losses. Its control includes the use of in-feed prophylactic antibiotics and therapeutic zinc oxide (ZnO), treatments that, since 2022, are no longer permi...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-02-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2024.1354449/full |
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| author | Juan M. Ortiz Sanjuán Juan M. Ortiz Sanjuán Edgar G. Manzanilla Edgar G. Manzanilla Raúl Cabrera-Rubio Raúl Cabrera-Rubio Fiona Crispie Fiona Crispie Paul D. Cotter Paul D. Cotter Paul D. Cotter Juan J. Garrido Daniel Ekhlas Daniel Ekhlas Lorcan O’Neill Lorcan O’Neill Héctor Argüello |
| author_facet | Juan M. Ortiz Sanjuán Juan M. Ortiz Sanjuán Edgar G. Manzanilla Edgar G. Manzanilla Raúl Cabrera-Rubio Raúl Cabrera-Rubio Fiona Crispie Fiona Crispie Paul D. Cotter Paul D. Cotter Paul D. Cotter Juan J. Garrido Daniel Ekhlas Daniel Ekhlas Lorcan O’Neill Lorcan O’Neill Héctor Argüello |
| author_sort | Juan M. Ortiz Sanjuán |
| collection | DOAJ |
| description | IntroductionPost-weaning diarrhoea (PWD) is a multifactorial disease that affects piglets after weaning, contributing to productive and economic losses. Its control includes the use of in-feed prophylactic antibiotics and therapeutic zinc oxide (ZnO), treatments that, since 2022, are no longer permitted in the European Union due to spread of antimicrobial resistance genes and pollution of soil with heavy metals. A dysbiosis in the microbiota has been suggested as a potential risk factor of PWD onset. Understanding pig’s microbiota development around weaning and its changes in response to ZnO and antibiotics is crucial to develop feasible alternatives to prophylactic and metaphylactic antimicrobial use.MethodsThis study used shotgun metagenomic sequencing to investigate the environmental and faecal microbiota on 10 farms using (Treated) or not using (ZnO-free) in-feed antibiotics and ZnO during the first 14 days post-weaning (dpw). Environmental samples from clean pens were collected at weaning day (0dpw), and faecal samples at 0, 7 and 14dpw. Diarrhoeic faecal samples were collected at 7dpw when available.ResultsThe analysis of data revealed that the faecal microbiota composition and its functionality was impacted by the sampling time point (microbiota maturation after weaning) but not by the farm environment. Treatment with antibiotics and ZnO showed no effects on diversity indices while the analyses of microbiota taxonomic and functional profiles revealed increased abundance of taxa and metabolic functions associated with Phascolarctobacterium succinatutens or different species of Prevotella spp. on the Treated farms, and with Megasphaera elsdenii and Escherichia coli on the ZnO-free farms. The analysis of diarrhoea samples revealed that the treatment favoured the microbiota transition or maturation from 0dpw to 14dpw in Treated farms, resembling the composition of healthy animals, when compared to diarrhoea from ZnO-free farms, which were linked in composition to 0dpw samples.DiscussionThe results provide a comprehensive overview of the beneficial effects of ZnO and antibiotics in PWD in the microbiota transition after weaning, preventing the overgrowth of pathogens such as pathogenic E. coli and revealing the key aspects in microbiota maturation that antibiotics or ZnO alternatives should fulfil. |
| first_indexed | 2024-03-08T05:12:36Z |
| format | Article |
| id | doaj.art-e35e271c08394960897ea47ac3758f6f |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-03-08T05:12:36Z |
| publishDate | 2024-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-e35e271c08394960897ea47ac3758f6f2024-02-07T05:34:27ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882024-02-011410.3389/fcimb.2024.13544491354449Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics useJuan M. Ortiz Sanjuán0Juan M. Ortiz Sanjuán1Edgar G. Manzanilla2Edgar G. Manzanilla3Raúl Cabrera-Rubio4Raúl Cabrera-Rubio5Fiona Crispie6Fiona Crispie7Paul D. Cotter8Paul D. Cotter9Paul D. Cotter10Juan J. Garrido11Daniel Ekhlas12Daniel Ekhlas13Lorcan O’Neill14Lorcan O’Neill15Héctor Argüello16Pig Development Department, Teagasc Grassland Research and Innovation Centre, Moorepark, Cork, IrelandGrupo de Genómica y Mejora Animal, Departamento de Genética, Facultad de Veterinaria, Universidad de Córdoba, Córdoba, SpainPig Development Department, Teagasc Grassland Research and Innovation Centre, Moorepark, Cork, IrelandSchool of Veterinary Medicine, University College Dublin, Dublin, IrelandTeagasc Food Research Centre, Moorepark, Cork, IrelandAPC Microbiome Institute Science Foundation Ireland (SFI) Research Centre, University College Cork, Cork, IrelandTeagasc Food Research Centre, Moorepark, Cork, IrelandAPC Microbiome Institute Science Foundation Ireland (SFI) Research Centre, University College Cork, Cork, IrelandTeagasc Food Research Centre, Moorepark, Cork, IrelandAPC Microbiome Institute Science Foundation Ireland (SFI) Research Centre, University College Cork, Cork, IrelandVistaMilk Science Foundation Ireland (SFI) Research Centre, Cork, IrelandGrupo de Genómica y Mejora Animal, Departamento de Genética, Facultad de Veterinaria, Universidad de Córdoba, Córdoba, SpainPig Development Department, Teagasc Grassland Research and Innovation Centre, Moorepark, Cork, IrelandSchool of Veterinary Medicine, University College Dublin, Dublin, IrelandPig Development Department, Teagasc Grassland Research and Innovation Centre, Moorepark, Cork, IrelandSchool of Veterinary Medicine, University College Dublin, Dublin, IrelandDepartamento de Sanidad Animal, Facultad de Veterinaria, Universidad de León, León, SpainIntroductionPost-weaning diarrhoea (PWD) is a multifactorial disease that affects piglets after weaning, contributing to productive and economic losses. Its control includes the use of in-feed prophylactic antibiotics and therapeutic zinc oxide (ZnO), treatments that, since 2022, are no longer permitted in the European Union due to spread of antimicrobial resistance genes and pollution of soil with heavy metals. A dysbiosis in the microbiota has been suggested as a potential risk factor of PWD onset. Understanding pig’s microbiota development around weaning and its changes in response to ZnO and antibiotics is crucial to develop feasible alternatives to prophylactic and metaphylactic antimicrobial use.MethodsThis study used shotgun metagenomic sequencing to investigate the environmental and faecal microbiota on 10 farms using (Treated) or not using (ZnO-free) in-feed antibiotics and ZnO during the first 14 days post-weaning (dpw). Environmental samples from clean pens were collected at weaning day (0dpw), and faecal samples at 0, 7 and 14dpw. Diarrhoeic faecal samples were collected at 7dpw when available.ResultsThe analysis of data revealed that the faecal microbiota composition and its functionality was impacted by the sampling time point (microbiota maturation after weaning) but not by the farm environment. Treatment with antibiotics and ZnO showed no effects on diversity indices while the analyses of microbiota taxonomic and functional profiles revealed increased abundance of taxa and metabolic functions associated with Phascolarctobacterium succinatutens or different species of Prevotella spp. on the Treated farms, and with Megasphaera elsdenii and Escherichia coli on the ZnO-free farms. The analysis of diarrhoea samples revealed that the treatment favoured the microbiota transition or maturation from 0dpw to 14dpw in Treated farms, resembling the composition of healthy animals, when compared to diarrhoea from ZnO-free farms, which were linked in composition to 0dpw samples.DiscussionThe results provide a comprehensive overview of the beneficial effects of ZnO and antibiotics in PWD in the microbiota transition after weaning, preventing the overgrowth of pathogens such as pathogenic E. coli and revealing the key aspects in microbiota maturation that antibiotics or ZnO alternatives should fulfil.https://www.frontiersin.org/articles/10.3389/fcimb.2024.1354449/fullantimicrobialenvironmentmicrobiomepigletspost-weaning diarrheaweaning |
| spellingShingle | Juan M. Ortiz Sanjuán Juan M. Ortiz Sanjuán Edgar G. Manzanilla Edgar G. Manzanilla Raúl Cabrera-Rubio Raúl Cabrera-Rubio Fiona Crispie Fiona Crispie Paul D. Cotter Paul D. Cotter Paul D. Cotter Juan J. Garrido Daniel Ekhlas Daniel Ekhlas Lorcan O’Neill Lorcan O’Neill Héctor Argüello Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics use Frontiers in Cellular and Infection Microbiology antimicrobial environment microbiome piglets post-weaning diarrhea weaning |
| title | Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics use |
| title_full | Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics use |
| title_fullStr | Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics use |
| title_full_unstemmed | Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics use |
| title_short | Fine-tuning of post-weaning pig microbiome structure and functionality by in-feed zinc oxide and antibiotics use |
| title_sort | fine tuning of post weaning pig microbiome structure and functionality by in feed zinc oxide and antibiotics use |
| topic | antimicrobial environment microbiome piglets post-weaning diarrhea weaning |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2024.1354449/full |
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