Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitis
Abstract Background Mastitis caused by multiple factors remains one of the most common and costly disease of the dairy industry. Multi-omics approaches enable the comprehensive investigation of the complex interactions between multiple layers of information to provide a more holistic view of disease...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2024-03-01
|
| Series: | Journal of Animal Science and Biotechnology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40104-024-00996-8 |
| _version_ | 1797259092110082048 |
|---|---|
| author | Mengqi Wang Naisu Yang Mario Laterrière David Gagné Faith Omonijo Eveline M. Ibeagha-Awemu |
| author_facet | Mengqi Wang Naisu Yang Mario Laterrière David Gagné Faith Omonijo Eveline M. Ibeagha-Awemu |
| author_sort | Mengqi Wang |
| collection | DOAJ |
| description | Abstract Background Mastitis caused by multiple factors remains one of the most common and costly disease of the dairy industry. Multi-omics approaches enable the comprehensive investigation of the complex interactions between multiple layers of information to provide a more holistic view of disease pathogenesis. Therefore, this study investigated the genomic and epigenomic signatures and the possible regulatory mechanisms underlying subclinical mastitis by integrating RNA sequencing data (mRNA and lncRNA), small RNA sequencing data (miRNA) and DNA methylation sequencing data of milk somatic cells from 10 healthy cows and 20 cows with naturally occurring subclinical mastitis caused by Staphylococcus aureus or Staphylococcus chromogenes. Results Functional investigation of the data sets through gene set analysis uncovered 3458 biological process GO terms and 170 KEGG pathways with altered activities during subclinical mastitis, provided further insights into subclinical mastitis and revealed the involvement of multi-omics signatures in the altered immune responses and impaired mammary gland productivity during subclinical mastitis. The abundant genomic and epigenomic signatures with significant alterations related to subclinical mastitis were observed, including 30,846, 2552, 1276 and 57 differential methylation haplotype blocks (dMHBs), differentially expressed genes (DEGs), lncRNAs (DELs) and miRNAs (DEMs), respectively. Next, 5 factors presenting the principal variation of differential multi-omics signatures were identified. The important roles of Factor 1 (DEG, DEM and DEL) and Factor 2 (dMHB and DEM), in the regulation of immune defense and impaired mammary gland functions during subclinical mastitis were revealed. Each of the omics within Factors 1 and 2 explained about 20% of the source of variation in subclinical mastitis. Also, networks of important functional gene sets with the involvement of multi-omics signatures were demonstrated, which contributed to a comprehensive view of the possible regulatory mechanisms underlying subclinical mastitis. Furthermore, multi-omics integration enabled the association of the epigenomic regulatory factors (dMHBs, DELs and DEMs) of altered genes in important pathways, such as ‘Staphylococcus aureus infection pathway’ and ‘natural killer cell mediated cytotoxicity pathway’, etc., which provides further insights into mastitis regulatory mechanisms. Moreover, few multi-omics signatures (14 dMHBs, 25 DEGs, 18 DELs and 5 DEMs) were identified as candidate discriminant signatures with capacity of distinguishing subclinical mastitis cows from healthy cows. Conclusion The integration of genomic and epigenomic data by multi-omics approaches in this study provided a better understanding of the molecular mechanisms underlying subclinical mastitis and identified multi-omics candidate discriminant signatures for subclinical mastitis, which may ultimately lead to the development of more effective mastitis control and management strategies. |
| first_indexed | 2024-04-24T23:03:56Z |
| format | Article |
| id | doaj.art-a4175590e217413db2d214922bdc66a0 |
| institution | Directory Open Access Journal |
| issn | 2049-1891 |
| language | English |
| last_indexed | 2024-04-24T23:03:56Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Animal Science and Biotechnology |
| spelling | doaj.art-a4175590e217413db2d214922bdc66a02024-03-17T12:34:16ZengBMCJournal of Animal Science and Biotechnology2049-18912024-03-0115112110.1186/s40104-024-00996-8Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitisMengqi Wang0Naisu Yang1Mario Laterrière2David Gagné3Faith Omonijo4Eveline M. Ibeagha-Awemu5Agriculture and Agri-Food Canada, Sherbrooke Research and Development CentreDepartment of Animal Science, Université LavalQuebec Research and Development Centre, Agriculture and Agri-Food CanadaQuebec Research and Development Centre, Agriculture and Agri-Food CanadaAgriculture and Agri-Food Canada, Sherbrooke Research and Development CentreAgriculture and Agri-Food Canada, Sherbrooke Research and Development CentreAbstract Background Mastitis caused by multiple factors remains one of the most common and costly disease of the dairy industry. Multi-omics approaches enable the comprehensive investigation of the complex interactions between multiple layers of information to provide a more holistic view of disease pathogenesis. Therefore, this study investigated the genomic and epigenomic signatures and the possible regulatory mechanisms underlying subclinical mastitis by integrating RNA sequencing data (mRNA and lncRNA), small RNA sequencing data (miRNA) and DNA methylation sequencing data of milk somatic cells from 10 healthy cows and 20 cows with naturally occurring subclinical mastitis caused by Staphylococcus aureus or Staphylococcus chromogenes. Results Functional investigation of the data sets through gene set analysis uncovered 3458 biological process GO terms and 170 KEGG pathways with altered activities during subclinical mastitis, provided further insights into subclinical mastitis and revealed the involvement of multi-omics signatures in the altered immune responses and impaired mammary gland productivity during subclinical mastitis. The abundant genomic and epigenomic signatures with significant alterations related to subclinical mastitis were observed, including 30,846, 2552, 1276 and 57 differential methylation haplotype blocks (dMHBs), differentially expressed genes (DEGs), lncRNAs (DELs) and miRNAs (DEMs), respectively. Next, 5 factors presenting the principal variation of differential multi-omics signatures were identified. The important roles of Factor 1 (DEG, DEM and DEL) and Factor 2 (dMHB and DEM), in the regulation of immune defense and impaired mammary gland functions during subclinical mastitis were revealed. Each of the omics within Factors 1 and 2 explained about 20% of the source of variation in subclinical mastitis. Also, networks of important functional gene sets with the involvement of multi-omics signatures were demonstrated, which contributed to a comprehensive view of the possible regulatory mechanisms underlying subclinical mastitis. Furthermore, multi-omics integration enabled the association of the epigenomic regulatory factors (dMHBs, DELs and DEMs) of altered genes in important pathways, such as ‘Staphylococcus aureus infection pathway’ and ‘natural killer cell mediated cytotoxicity pathway’, etc., which provides further insights into mastitis regulatory mechanisms. Moreover, few multi-omics signatures (14 dMHBs, 25 DEGs, 18 DELs and 5 DEMs) were identified as candidate discriminant signatures with capacity of distinguishing subclinical mastitis cows from healthy cows. Conclusion The integration of genomic and epigenomic data by multi-omics approaches in this study provided a better understanding of the molecular mechanisms underlying subclinical mastitis and identified multi-omics candidate discriminant signatures for subclinical mastitis, which may ultimately lead to the development of more effective mastitis control and management strategies.https://doi.org/10.1186/s40104-024-00996-8Candidate discriminant multi-omics signatureGeneLong non-coding RNAMethylation haplotype blockMicroRNAMulti-omics integration |
| spellingShingle | Mengqi Wang Naisu Yang Mario Laterrière David Gagné Faith Omonijo Eveline M. Ibeagha-Awemu Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitis Journal of Animal Science and Biotechnology Candidate discriminant multi-omics signature Gene Long non-coding RNA Methylation haplotype block MicroRNA Multi-omics integration |
| title | Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitis |
| title_full | Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitis |
| title_fullStr | Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitis |
| title_full_unstemmed | Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitis |
| title_short | Multi-omics integration identifies regulatory factors underlying bovine subclinical mastitis |
| title_sort | multi omics integration identifies regulatory factors underlying bovine subclinical mastitis |
| topic | Candidate discriminant multi-omics signature Gene Long non-coding RNA Methylation haplotype block MicroRNA Multi-omics integration |
| url | https://doi.org/10.1186/s40104-024-00996-8 |
| work_keys_str_mv | AT mengqiwang multiomicsintegrationidentifiesregulatoryfactorsunderlyingbovinesubclinicalmastitis AT naisuyang multiomicsintegrationidentifiesregulatoryfactorsunderlyingbovinesubclinicalmastitis AT mariolaterriere multiomicsintegrationidentifiesregulatoryfactorsunderlyingbovinesubclinicalmastitis AT davidgagne multiomicsintegrationidentifiesregulatoryfactorsunderlyingbovinesubclinicalmastitis AT faithomonijo multiomicsintegrationidentifiesregulatoryfactorsunderlyingbovinesubclinicalmastitis AT evelinemibeaghaawemu multiomicsintegrationidentifiesregulatoryfactorsunderlyingbovinesubclinicalmastitis |