Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apices

ABSTRACT: Staphylococcus hominis, a member of the non-aureus staphylococci (NAS) group, is part of the human and animal microbiota. Although it has been isolated from multiple bovine-associated habitats, its relevance as a cause of bovine mastitis is currently not well described. To successfully col...

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Main Authors: H. Reydams, A. Wuytack, S. Piepers, K. Mertens, F. Boyen, F.N. de Souza, F. Haesebrouck, S. De Vliegher
Format: Article
Language:English
Published: Elsevier 2022-11-01
Series:Journal of Dairy Science
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0022030222006038
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author H. Reydams
A. Wuytack
S. Piepers
K. Mertens
F. Boyen
F.N. de Souza
F. Haesebrouck
S. De Vliegher
author_facet H. Reydams
A. Wuytack
S. Piepers
K. Mertens
F. Boyen
F.N. de Souza
F. Haesebrouck
S. De Vliegher
author_sort H. Reydams
collection DOAJ
description ABSTRACT: Staphylococcus hominis, a member of the non-aureus staphylococci (NAS) group, is part of the human and animal microbiota. Although it has been isolated from multiple bovine-associated habitats, its relevance as a cause of bovine mastitis is currently not well described. To successfully colonize and proliferate in the bovine mammary gland, a bacterial species must be able to acquire iron from host iron-binding proteins. The aims of this study were (1) to assess the genetic diversity of S. hominis isolated from bovine quarter milk, rectal feces, and teat apices, and (2) to investigate the capacity of bovine S. hominis isolates belonging to these different habitats to utilize ferritin and lactoferrin as iron sources. To expand on an available collection of bovine S. hominis isolates (2 from quarter milk, 8 from rectal feces, and 19 from teat apices) from one commercial dairy herd, a subsequent single cross-sectional quarter milk sampling (n = 360) was performed on all lactating cows (n = 90) of the same herd. In total, 514 NAS isolates were recovered and identified by MALDI-TOF mass spectrometry; the 6 most prevalent NAS species were S. cohnii (33.9%), S. sciuri (16.7%), S. haemolyticus (16.3%), S. xylosus (9.6%), S. equorum (9.4%), and S. hominis (3.5%). A random amplified polymorphic DNA (RAPD) analysis was performed on 46 S. hominis isolates (19 from quarter milk, 8 from rectal feces, and 19 from teat apices). Eighteen distinct RAPD fingerprint groups were distinguished although we were unable to detect the presence of the same RAPD type in all 3 habitats. One S. hominis isolate of a distinct RAPD type unique to a specific habitat (8 from quarter milk, 3 from rectal feces, and 4 from teat apices) along with the quality control strain Staphylococcus aureus ATCC 25923 and 2 well-studied Staphylococcus chromogenes isolates (“IM” and “TA”) were included in the phenotypical iron test. All isolates were grown in 4 types of media: iron-rich tryptic soy broth, iron-rich tryptic soy broth deferrated by 2,2'-bipyridyl, and deferrated tryptic soy broth supplemented with human recombinant lactoferrin or equine spleen–derived ferritin. The growth of the different strains was modified by the medium in which they were grown. Staphylococcus chromogenes TA showed significantly lower growth under iron-deprived conditions, and adding an iron supplement (lactoferrin or ferritin) resulted in no improvement in growth; in contrast, growth of S. chromogenes IM was significantly recovered with iron supplementation. Staphylococcus hominis strains from all 3 habitats were able to significantly utilize ferritin but not lactoferrin as an iron source to reverse the growth inhibition, in varying degrees, caused by the chelating agent 2,2'-bipyridyl.
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spelling doaj.art-15243963d0334bec9175b098d52cbc592022-12-22T04:35:43ZengElsevierJournal of Dairy Science0022-03022022-11-0110512999510006Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apicesH. Reydams0A. Wuytack1S. Piepers2K. Mertens3F. Boyen4F.N. de Souza5F. Haesebrouck6S. De Vliegher7M-team and Mastitis and Milk Quality Research Unit, Department of Internal Medicine, Reproduction, and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium; Corresponding authorM-team and Mastitis and Milk Quality Research Unit, Department of Internal Medicine, Reproduction, and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium; Department of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumM-team and Mastitis and Milk Quality Research Unit, Department of Internal Medicine, Reproduction, and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumM-team and Mastitis and Milk Quality Research Unit, Department of Internal Medicine, Reproduction, and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumDepartment of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumVeterinary Clinical Immunology Research Group, Department of Clinical Science, Faculty of Veterinary Medicine and Animal Sciences, University of São Paulo, Prof. Orlando Marques de Paiva Av. 87, São Paulo 05508-270, Brazil; Postgraduate Program in Animal Science, Department of Veterinary Medicine, Federal University of Paraiba, Rodovia PB-079 12, Areia, João Pessoa 58397-000, BrazilDepartment of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumM-team and Mastitis and Milk Quality Research Unit, Department of Internal Medicine, Reproduction, and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, BelgiumABSTRACT: Staphylococcus hominis, a member of the non-aureus staphylococci (NAS) group, is part of the human and animal microbiota. Although it has been isolated from multiple bovine-associated habitats, its relevance as a cause of bovine mastitis is currently not well described. To successfully colonize and proliferate in the bovine mammary gland, a bacterial species must be able to acquire iron from host iron-binding proteins. The aims of this study were (1) to assess the genetic diversity of S. hominis isolated from bovine quarter milk, rectal feces, and teat apices, and (2) to investigate the capacity of bovine S. hominis isolates belonging to these different habitats to utilize ferritin and lactoferrin as iron sources. To expand on an available collection of bovine S. hominis isolates (2 from quarter milk, 8 from rectal feces, and 19 from teat apices) from one commercial dairy herd, a subsequent single cross-sectional quarter milk sampling (n = 360) was performed on all lactating cows (n = 90) of the same herd. In total, 514 NAS isolates were recovered and identified by MALDI-TOF mass spectrometry; the 6 most prevalent NAS species were S. cohnii (33.9%), S. sciuri (16.7%), S. haemolyticus (16.3%), S. xylosus (9.6%), S. equorum (9.4%), and S. hominis (3.5%). A random amplified polymorphic DNA (RAPD) analysis was performed on 46 S. hominis isolates (19 from quarter milk, 8 from rectal feces, and 19 from teat apices). Eighteen distinct RAPD fingerprint groups were distinguished although we were unable to detect the presence of the same RAPD type in all 3 habitats. One S. hominis isolate of a distinct RAPD type unique to a specific habitat (8 from quarter milk, 3 from rectal feces, and 4 from teat apices) along with the quality control strain Staphylococcus aureus ATCC 25923 and 2 well-studied Staphylococcus chromogenes isolates (“IM” and “TA”) were included in the phenotypical iron test. All isolates were grown in 4 types of media: iron-rich tryptic soy broth, iron-rich tryptic soy broth deferrated by 2,2'-bipyridyl, and deferrated tryptic soy broth supplemented with human recombinant lactoferrin or equine spleen–derived ferritin. The growth of the different strains was modified by the medium in which they were grown. Staphylococcus chromogenes TA showed significantly lower growth under iron-deprived conditions, and adding an iron supplement (lactoferrin or ferritin) resulted in no improvement in growth; in contrast, growth of S. chromogenes IM was significantly recovered with iron supplementation. Staphylococcus hominis strains from all 3 habitats were able to significantly utilize ferritin but not lactoferrin as an iron source to reverse the growth inhibition, in varying degrees, caused by the chelating agent 2,2'-bipyridyl.http://www.sciencedirect.com/science/article/pii/S0022030222006038dairy cowmastitisnon-aureus staphylococciiron deprivationStaphylococcus hominis
spellingShingle H. Reydams
A. Wuytack
S. Piepers
K. Mertens
F. Boyen
F.N. de Souza
F. Haesebrouck
S. De Vliegher
Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apices
Journal of Dairy Science
dairy cow
mastitis
non-aureus staphylococci
iron deprivation
Staphylococcus hominis
title Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apices
title_full Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apices
title_fullStr Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apices
title_full_unstemmed Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apices
title_short Genetic diversity and iron metabolism of Staphylococcus hominis isolates originating from bovine quarter milk, rectal feces, and teat apices
title_sort genetic diversity and iron metabolism of staphylococcus hominis isolates originating from bovine quarter milk rectal feces and teat apices
topic dairy cow
mastitis
non-aureus staphylococci
iron deprivation
Staphylococcus hominis
url http://www.sciencedirect.com/science/article/pii/S0022030222006038
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