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Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci

BACKGROUND: In a collaboration between animal and human health care professionals, we assessed the genetic characteristics shared by non-aureus staphylococci (NAS) infecting humans and dairy ewes to investigate their relatedness in a region concentrating half of the total National sheep stock. We ex...

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Autores principales: Azara, Elisa, Longheu, Carla Maria, Attene, Sonia, Sanna, Silvana, Sale, Marco, Addis, Maria Filippa, Tola, Sebastiana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9161600/
https://www.ncbi.nlm.nih.gov/pubmed/35655210
http://dx.doi.org/10.1186/s12917-022-03257-w
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author Azara, Elisa
Longheu, Carla Maria
Attene, Sonia
Sanna, Silvana
Sale, Marco
Addis, Maria Filippa
Tola, Sebastiana
author_facet Azara, Elisa
Longheu, Carla Maria
Attene, Sonia
Sanna, Silvana
Sale, Marco
Addis, Maria Filippa
Tola, Sebastiana
author_sort Azara, Elisa
collection PubMed
description BACKGROUND: In a collaboration between animal and human health care professionals, we assessed the genetic characteristics shared by non-aureus staphylococci (NAS) infecting humans and dairy ewes to investigate their relatedness in a region concentrating half of the total National sheep stock. We examined by PCR 125 ovine and 70 human NAS for biofilm production, pyrogenic toxins, adhesins, autolysins genes, and accessory gene regulator (agr) locus. The microtiter plate assay (MPA) was used for the phenotypic screening of biofilm production. Ovine NAS included S. epidermidis, S. chromogenes, S. haemolyticus, S. simulans, S. caprae, S. warneri, S. saprophyticus, S. intermedius, and S. muscae. Human NAS included S. haemolyticus, S. epidermidis, S. hominis, S. lugdunensis, S. capitis, S. warneri, S. xylosus, S. pasteuri, and S. saprophyticus subsp. bovis. RESULTS: Phenotypically, 41 (32.8%) ovine and 24 (34.3%) human isolates were characterized as biofilm producers. Of the ovine isolates, 12 were classified as biofilm-producing while the remaining 29 as weak biofilm-producing. All 24 human isolates were considered weak biofilm-producing. Few S. epidermidis isolates harbored the icaA/D genes coding for the polysaccharide intercellular adhesin (PIA), while the bhp, aap, and embp genes coding biofilm accumulation proteins were present in both non-producing and biofilm-producing isolates. Fifty-nine sheep NAS (all S. epidermidis, 1 S. chromogenes, and 1 S. haemolyticus) and 27 human NAS (all S. epidermidis and 1 S. warneri) were positive for the agr locus: agr-3se (57.8%) followed by agr-1se (36.8%) predominated in sheep, while agr-1se (65.4%), followed by agr-2se (34.6%) predominated in humans. Concerning virulence genes, 40, 39.2, 47.2%, 52.8, 80 and 43.2% of the sheep isolates carried atlE, aae, sdrF, sdrG, eno and epbS respectively, against 37.1, 42.8, 32.8, 60, 100 and 100% of human isolates. Enterotoxins and tsst were not detected. CONCLUSIONS: Considerable variation in biofilm formation ability was observed among NAS isolates from ovine and human samples. S. epidermidis was the best biofilm producer with the highest prevalence of adhesin-encoding genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12917-022-03257-w.
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spelling pubmed-91616002022-06-03 Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci Azara, Elisa Longheu, Carla Maria Attene, Sonia Sanna, Silvana Sale, Marco Addis, Maria Filippa Tola, Sebastiana BMC Vet Res Research Article BACKGROUND: In a collaboration between animal and human health care professionals, we assessed the genetic characteristics shared by non-aureus staphylococci (NAS) infecting humans and dairy ewes to investigate their relatedness in a region concentrating half of the total National sheep stock. We examined by PCR 125 ovine and 70 human NAS for biofilm production, pyrogenic toxins, adhesins, autolysins genes, and accessory gene regulator (agr) locus. The microtiter plate assay (MPA) was used for the phenotypic screening of biofilm production. Ovine NAS included S. epidermidis, S. chromogenes, S. haemolyticus, S. simulans, S. caprae, S. warneri, S. saprophyticus, S. intermedius, and S. muscae. Human NAS included S. haemolyticus, S. epidermidis, S. hominis, S. lugdunensis, S. capitis, S. warneri, S. xylosus, S. pasteuri, and S. saprophyticus subsp. bovis. RESULTS: Phenotypically, 41 (32.8%) ovine and 24 (34.3%) human isolates were characterized as biofilm producers. Of the ovine isolates, 12 were classified as biofilm-producing while the remaining 29 as weak biofilm-producing. All 24 human isolates were considered weak biofilm-producing. Few S. epidermidis isolates harbored the icaA/D genes coding for the polysaccharide intercellular adhesin (PIA), while the bhp, aap, and embp genes coding biofilm accumulation proteins were present in both non-producing and biofilm-producing isolates. Fifty-nine sheep NAS (all S. epidermidis, 1 S. chromogenes, and 1 S. haemolyticus) and 27 human NAS (all S. epidermidis and 1 S. warneri) were positive for the agr locus: agr-3se (57.8%) followed by agr-1se (36.8%) predominated in sheep, while agr-1se (65.4%), followed by agr-2se (34.6%) predominated in humans. Concerning virulence genes, 40, 39.2, 47.2%, 52.8, 80 and 43.2% of the sheep isolates carried atlE, aae, sdrF, sdrG, eno and epbS respectively, against 37.1, 42.8, 32.8, 60, 100 and 100% of human isolates. Enterotoxins and tsst were not detected. CONCLUSIONS: Considerable variation in biofilm formation ability was observed among NAS isolates from ovine and human samples. S. epidermidis was the best biofilm producer with the highest prevalence of adhesin-encoding genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12917-022-03257-w. BioMed Central 2022-06-02 /pmc/articles/PMC9161600/ /pubmed/35655210 http://dx.doi.org/10.1186/s12917-022-03257-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visithttp://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Azara, Elisa
Longheu, Carla Maria
Attene, Sonia
Sanna, Silvana
Sale, Marco
Addis, Maria Filippa
Tola, Sebastiana
Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci
title Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci
title_full Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci
title_fullStr Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci
title_full_unstemmed Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci
title_short Comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci
title_sort comparative profiling of agr locus, virulence, and biofilm-production genes of human and ovine non-aureus staphylococci
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9161600/
https://www.ncbi.nlm.nih.gov/pubmed/35655210
http://dx.doi.org/10.1186/s12917-022-03257-w
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