An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions
ABSTRACT: Udder cleft dermatitis (UCD) is a skin condition affecting the anterior parts of the udder in dairy cattle. In the present study, we aimed to shed light on the microbiota in severe UCD lesions versus healthy udder skin by putting forward a taxonomic and functional profile based on a virule...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-05-01
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| Series: | Journal of Dairy Science |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0022030223020179 |
| _version_ | 1827277924691083264 |
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| author | A.S. Vermeersch M. Ali Y. Gansemans F. Van Nieuwerburgh R. Ducatelle P. Geldhof D. Deforce J. Callens G. Opsomer |
| author_facet | A.S. Vermeersch M. Ali Y. Gansemans F. Van Nieuwerburgh R. Ducatelle P. Geldhof D. Deforce J. Callens G. Opsomer |
| author_sort | A.S. Vermeersch |
| collection | DOAJ |
| description | ABSTRACT: Udder cleft dermatitis (UCD) is a skin condition affecting the anterior parts of the udder in dairy cattle. In the present study, we aimed to shed light on the microbiota in severe UCD lesions versus healthy udder skin by putting forward a taxonomic and functional profile based on a virulence factor analysis. Through shotgun metagenomic sequencing, we found a high proportion of bacteria in addition to a low abundance of archaea. A distinct clustering of healthy udder skin versus UCD lesion samples was shown by applying principal component analysis and (sparse) partial least squares analysis on the metagenomic data. Proteobacteria, Bacillota, and Actinomycetota were among the most abundant phyla in healthy udder skin samples. In UCD samples, Bacteroidota was the most abundant phylum. At genus level, Bifidobacterium spp. had the highest relative abundance in healthy skin samples, whereas Porphyromonas spp. and Corynebacterium spp. had the highest relative abundance in UCD samples. In the differential abundance analysis, Porphyromonas spp. and Bacteroides spp. were significantly differentially abundant in UCD samples, whereas Bifidobacterium spp., Staphylococcus sp. AntiMn-1, and Staphylococcus equorum were more commonly found in healthy samples. Moreover, the abundance of several treponeme phylotypes was significantly higher in lesion samples. The streptococcal cysteine protease speB was among the most abundant virulence factors present in severe UCD lesions, while a plethora of virulence factors such as the antitoxin relB were downregulated, possibly contributing to creating the ideal wound climate for the dysbiotic community. Network analysis showed healthy lesion samples had a large network ofpositive, correlations between the abundances of beneficial species such as Aerococcus urinaeequi and Bifidobacterium angulatum, indicating that the healthy skin microbiome forms an active protective bacterial network, which is disrupted in case of UCD. In UCD samples, a smaller microbial network mainly consisting of positive correlations between the abundances of Bacteroides fragilis and anaerobic Bacteroidota was exposed. Moreover, a high correlation between the taxonomic data and virulence factors was revealed, concurrently with 2 separate networks of microbes and virulence factors. One network, matching with the taxonomic findings in the healthy udder skin samples, showcased a community of harmless or beneficial bacteria, such as Bifidobacterium spp. and Butyrivibrio proteoclasticus, associated with hcnB, hcnC, relB, glyoxalase, and cupin 2. The other network, corresponding to UCD samples, consisted of pathogenic or facultative pathogenic and mainly anaerobic bacteria such as Treponema spp., Mycoplasmopsis spp., and bovine gammaherpesvirus 4, that correlated with virulence factors SpvB, fhaB, and haemagglutination activity domain–associated factor. Our results point toward a dysbiotic community with a notable decrease in diversity and evenness, with a loss of normal skin inhabitants and innocuous or useful species making way for predominantly anaerobic, facultative pathogens. The shift in the abundance of virulence factors such as fhaB and SpvB could play a role in the manifestation of a local micro-environment favorable to the microbiome associated with udder skin lesions. Lastly, the presence of specific networks between microbial species, and between microbes and virulence factors was shown. |
| first_indexed | 2024-04-24T07:44:31Z |
| format | Article |
| id | doaj.art-55fc01c9efbe44e99fffa55bb4d347e1 |
| institution | Directory Open Access Journal |
| issn | 0022-0302 |
| language | English |
| last_indexed | 2024-04-24T07:44:31Z |
| publishDate | 2024-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Journal of Dairy Science |
| spelling | doaj.art-55fc01c9efbe44e99fffa55bb4d347e12024-04-19T04:16:17ZengElsevierJournal of Dairy Science0022-03022024-05-01107532193234An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesionsA.S. Vermeersch0M. Ali1Y. Gansemans2F. Van Nieuwerburgh3R. Ducatelle4P. Geldhof5D. Deforce6J. Callens7G. Opsomer8Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium; Corresponding authorLaboratory of Pharmaceutical Biotechnology, Faculty of Pharmaceutical Sciences, Ghent University, 9000 Ghent, BelgiumLaboratory of Pharmaceutical Biotechnology, Faculty of Pharmaceutical Sciences, Ghent University, 9000 Ghent, BelgiumLaboratory of Pharmaceutical Biotechnology, Faculty of Pharmaceutical Sciences, Ghent University, 9000 Ghent, BelgiumDepartment of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumDepartment of Translational Physiology, Infectiology and Public Health, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumLaboratory of Pharmaceutical Biotechnology, Faculty of Pharmaceutical Sciences, Ghent University, 9000 Ghent, BelgiumDierengezondheidszorg Vlaanderen, 8820 Torhout, BelgiumDepartment of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumABSTRACT: Udder cleft dermatitis (UCD) is a skin condition affecting the anterior parts of the udder in dairy cattle. In the present study, we aimed to shed light on the microbiota in severe UCD lesions versus healthy udder skin by putting forward a taxonomic and functional profile based on a virulence factor analysis. Through shotgun metagenomic sequencing, we found a high proportion of bacteria in addition to a low abundance of archaea. A distinct clustering of healthy udder skin versus UCD lesion samples was shown by applying principal component analysis and (sparse) partial least squares analysis on the metagenomic data. Proteobacteria, Bacillota, and Actinomycetota were among the most abundant phyla in healthy udder skin samples. In UCD samples, Bacteroidota was the most abundant phylum. At genus level, Bifidobacterium spp. had the highest relative abundance in healthy skin samples, whereas Porphyromonas spp. and Corynebacterium spp. had the highest relative abundance in UCD samples. In the differential abundance analysis, Porphyromonas spp. and Bacteroides spp. were significantly differentially abundant in UCD samples, whereas Bifidobacterium spp., Staphylococcus sp. AntiMn-1, and Staphylococcus equorum were more commonly found in healthy samples. Moreover, the abundance of several treponeme phylotypes was significantly higher in lesion samples. The streptococcal cysteine protease speB was among the most abundant virulence factors present in severe UCD lesions, while a plethora of virulence factors such as the antitoxin relB were downregulated, possibly contributing to creating the ideal wound climate for the dysbiotic community. Network analysis showed healthy lesion samples had a large network ofpositive, correlations between the abundances of beneficial species such as Aerococcus urinaeequi and Bifidobacterium angulatum, indicating that the healthy skin microbiome forms an active protective bacterial network, which is disrupted in case of UCD. In UCD samples, a smaller microbial network mainly consisting of positive correlations between the abundances of Bacteroides fragilis and anaerobic Bacteroidota was exposed. Moreover, a high correlation between the taxonomic data and virulence factors was revealed, concurrently with 2 separate networks of microbes and virulence factors. One network, matching with the taxonomic findings in the healthy udder skin samples, showcased a community of harmless or beneficial bacteria, such as Bifidobacterium spp. and Butyrivibrio proteoclasticus, associated with hcnB, hcnC, relB, glyoxalase, and cupin 2. The other network, corresponding to UCD samples, consisted of pathogenic or facultative pathogenic and mainly anaerobic bacteria such as Treponema spp., Mycoplasmopsis spp., and bovine gammaherpesvirus 4, that correlated with virulence factors SpvB, fhaB, and haemagglutination activity domain–associated factor. Our results point toward a dysbiotic community with a notable decrease in diversity and evenness, with a loss of normal skin inhabitants and innocuous or useful species making way for predominantly anaerobic, facultative pathogens. The shift in the abundance of virulence factors such as fhaB and SpvB could play a role in the manifestation of a local micro-environment favorable to the microbiome associated with udder skin lesions. Lastly, the presence of specific networks between microbial species, and between microbes and virulence factors was shown.http://www.sciencedirect.com/science/article/pii/S0022030223020179udder cleft dermatitiscattlemetagenomicsshotgun sequencing |
| spellingShingle | A.S. Vermeersch M. Ali Y. Gansemans F. Van Nieuwerburgh R. Ducatelle P. Geldhof D. Deforce J. Callens G. Opsomer An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions Journal of Dairy Science udder cleft dermatitis cattle metagenomics shotgun sequencing |
| title | An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions |
| title_full | An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions |
| title_fullStr | An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions |
| title_full_unstemmed | An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions |
| title_short | An in-depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions |
| title_sort | in depth investigation of the microbiota and its virulence factors associated with severe udder cleft dermatitis lesions |
| topic | udder cleft dermatitis cattle metagenomics shotgun sequencing |
| url | http://www.sciencedirect.com/science/article/pii/S0022030223020179 |
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