DNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traits
Abstract Background DNA methylation has been documented to play vital roles in diseases and biological processes. In bovine, little is known about the regulatory roles of DNA methylation alterations on production and health traits, including mastitis. Results Here, we employed whole-genome DNA methy...
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-024-01843-y |
| _version_ | 1827315756339036160 |
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| author | Mengqi Wang Nathalie Bissonnette Mario Laterrière Pier-Luc Dudemaine David Gagné Jean-Philippe Roy Marc-André Sirard Eveline M. Ibeagha-Awemu |
| author_facet | Mengqi Wang Nathalie Bissonnette Mario Laterrière Pier-Luc Dudemaine David Gagné Jean-Philippe Roy Marc-André Sirard Eveline M. Ibeagha-Awemu |
| author_sort | Mengqi Wang |
| collection | DOAJ |
| description | Abstract Background DNA methylation has been documented to play vital roles in diseases and biological processes. In bovine, little is known about the regulatory roles of DNA methylation alterations on production and health traits, including mastitis. Results Here, we employed whole-genome DNA methylation sequencing to profile the DNA methylation patterns of milk somatic cells from sixteen cows with naturally occurring Staphylococcus aureus (S. aureus) subclinical mastitis and ten healthy control cows. We observed abundant DNA methylation alterations, including 3,356,456 differentially methylated cytosines and 153,783 differential methylation haplotype blocks (dMHBs). The DNA methylation in regulatory regions, including promoters, first exons and first introns, showed global significant negative correlations with gene expression status. We identified 6435 dMHBs located in the regulatory regions of differentially expressed genes and significantly correlated with their corresponding genes, revealing their potential effects on transcriptional activities. Genes harboring DNA methylation alterations were significantly enriched in multiple immune- and disease-related pathways, suggesting the involvement of DNA methylation in regulating host responses to S. aureus subclinical mastitis. In addition, we found nine discriminant signatures (differentiates cows with S. aureus subclinical mastitis from healthy cows) representing the majority of the DNA methylation variations related to S. aureus subclinical mastitis. Validation of seven dMHBs in 200 cows indicated significant associations with mammary gland health (SCC and SCS) and milk production performance (milk yield). Conclusions In conclusion, our findings revealed abundant DNA methylation alterations in milk somatic cells that may be involved in regulating mammary gland defense against S. aureus infection. Particularly noteworthy is the identification of seven dMHBs showing significant associations with mammary gland health, underscoring their potential as promising epigenetic biomarkers. Overall, our findings on DNA methylation alterations offer novel insights into the regulatory mechanisms of bovine subclinical mastitis, providing further avenues for the development of effective control measures. Graphical Abstract |
| first_indexed | 2024-04-24T23:02:40Z |
| format | Article |
| id | doaj.art-771011387c3f49418029b7e956702d93 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-24T23:02:40Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-771011387c3f49418029b7e956702d932024-03-17T12:38:21ZengBMCBMC Biology1741-70072024-03-0122112510.1186/s12915-024-01843-yDNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traitsMengqi Wang0Nathalie Bissonnette1Mario Laterrière2Pier-Luc Dudemaine3David Gagné4Jean-Philippe Roy5Marc-André Sirard6Eveline M. Ibeagha-Awemu7Sherbrooke Research and Development Centre, Agriculture and Agri-Food CanadaSherbrooke Research and Development Centre, Agriculture and Agri-Food CanadaQuebec Research and Development Centre, Agriculture and Agri-Food CanadaSherbrooke Research and Development Centre, Agriculture and Agri-Food CanadaQuebec Research and Development Centre, Agriculture and Agri-Food CanadaDepartment of Clinical Sciences, Université de MontréalDepartment of Animal Science, Laval UniversitySherbrooke Research and Development Centre, Agriculture and Agri-Food CanadaAbstract Background DNA methylation has been documented to play vital roles in diseases and biological processes. In bovine, little is known about the regulatory roles of DNA methylation alterations on production and health traits, including mastitis. Results Here, we employed whole-genome DNA methylation sequencing to profile the DNA methylation patterns of milk somatic cells from sixteen cows with naturally occurring Staphylococcus aureus (S. aureus) subclinical mastitis and ten healthy control cows. We observed abundant DNA methylation alterations, including 3,356,456 differentially methylated cytosines and 153,783 differential methylation haplotype blocks (dMHBs). The DNA methylation in regulatory regions, including promoters, first exons and first introns, showed global significant negative correlations with gene expression status. We identified 6435 dMHBs located in the regulatory regions of differentially expressed genes and significantly correlated with their corresponding genes, revealing their potential effects on transcriptional activities. Genes harboring DNA methylation alterations were significantly enriched in multiple immune- and disease-related pathways, suggesting the involvement of DNA methylation in regulating host responses to S. aureus subclinical mastitis. In addition, we found nine discriminant signatures (differentiates cows with S. aureus subclinical mastitis from healthy cows) representing the majority of the DNA methylation variations related to S. aureus subclinical mastitis. Validation of seven dMHBs in 200 cows indicated significant associations with mammary gland health (SCC and SCS) and milk production performance (milk yield). Conclusions In conclusion, our findings revealed abundant DNA methylation alterations in milk somatic cells that may be involved in regulating mammary gland defense against S. aureus infection. Particularly noteworthy is the identification of seven dMHBs showing significant associations with mammary gland health, underscoring their potential as promising epigenetic biomarkers. Overall, our findings on DNA methylation alterations offer novel insights into the regulatory mechanisms of bovine subclinical mastitis, providing further avenues for the development of effective control measures. Graphical Abstracthttps://doi.org/10.1186/s12915-024-01843-yGenome-wide DNA methylation alterationsDNA methylation haplotype blocksDiscriminant signaturesImmune functionsMammary gland healthMilk production |
| spellingShingle | Mengqi Wang Nathalie Bissonnette Mario Laterrière Pier-Luc Dudemaine David Gagné Jean-Philippe Roy Marc-André Sirard Eveline M. Ibeagha-Awemu DNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traits BMC Biology Genome-wide DNA methylation alterations DNA methylation haplotype blocks Discriminant signatures Immune functions Mammary gland health Milk production |
| title | DNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traits |
| title_full | DNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traits |
| title_fullStr | DNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traits |
| title_full_unstemmed | DNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traits |
| title_short | DNA methylation haplotype block signatures responding to Staphylococcus aureus subclinical mastitis and association with production and health traits |
| title_sort | dna methylation haplotype block signatures responding to staphylococcus aureus subclinical mastitis and association with production and health traits |
| topic | Genome-wide DNA methylation alterations DNA methylation haplotype blocks Discriminant signatures Immune functions Mammary gland health Milk production |
| url | https://doi.org/10.1186/s12915-024-01843-y |
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