Methicillin-resistant and methicillin-susceptible Staphylococcus aureus in French hedgehogs admitted to a wildlife health center

The <i>mecC</i> gene conferring methicillin-resistance has always been found on a SCC<i>mec</i> type XI element and is largely restricted to the few clonal complexes CC130, CC1943, CC425, CC49 and CC599. The occurrence of the <i>mecC</i> gene in many different hosts highlighted its One Health importance, even though European hedgehogs (<i>Erinaceus europaeus</i>) are considered its natural reservoir, most probably because of the selective pressure imposed by beta-lactam-producing dermatophytes (<i>Trichophyton erinacei</i>) that colonize the skin of these mammals. Surprisingly, while the presence of <i>T. erinacei</i> on the French territory has been proven, no <i>mecC</i>-positive methicillin-resistant <i>Staphylococcus aureus</i> (MRSA) isolate has been reported yet from hedgehogs. We thus sampled 139 hedgehogs brought to a wildlife center; 128 were <i>S. aureus</i> carriers and 25 (18.0 %) presented a MRSA isolate, of which 21 (15.1 %) displayed the <i>mecC</i> gene. All 161 <i>S. aureus</i> collected were whole-genome sequenced. The <i>mecC</i>-MRSA belonged to the classical CCs, i.e. CC130, CC1943 and CC49. The majority (98/139, 70.5 %) of the methicillin-susceptible <i>Staphylococcus aureus</i> (MSSA) isolates also belonged to these three CCs. A phylogenetic comparison with <i>mecC</i>-MRSA isolates from all over Europe and New-Zealand showed local adaptations, despite the fact that they all belonged to the same CCs. The acquisition of the SCC<i>mec</i> type XI element by a concomitant MSSA could not be observed in the same animal, but such a transfer might be suggested since identical clones were identified, one MSSA and one MRSA, though in different animals. In parallel, we conducted a detailed analysis of the SCC<i>mec</i> type XI element as well as specific virulence factors (a <i>tst</i> variant and the <i>vwb</i> <sub>SaPI</sub> gene). Results led us to hypothesize that the <i>mecC</i> gene might be acquired through selective pressure of <i>T. erinacei</i> on MSSA, some of which were acquired a long time ago from ruminants and are now colonizing the skin of the hedgehogs.

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Publication Details

Journal
One Health
Published
2024-11-19
DOI
https://doi.org/10.1016/j.onehlt.2024.100938
Citations
7
Primary Topic
Microbial infections and disease research
Type
article
Field-Weighted Citation Impact
2.41

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article

Methicillin-resistant and methicillin-susceptible Staphylococcus aureus in French hedgehogs admitted to a wildlife health center

Marisa Haenni, François Meurens, Antoine Drapeau, Julie Botman et al.
7 citations
One Health
Microbial infections and disease research
2.41
article

Methicillin-resistant and methicillin-susceptible Staphylococcus aureus in French hedgehogs admitted to a wildlife health center

Marisa Haenni, François Meurens, Antoine Drapeau, Julie Botman, Jesper Larsen, Séverine Murri, Philippe Gourlay, Jean-Yves Madec, Pauline François, Caroline M. Lefrère
article en
7 citations

Abstract

The <i>mecC</i> gene conferring methicillin-resistance has always been found on a SCC<i>mec</i> type XI element and is largely restricted to the few clonal complexes CC130, CC1943, CC425, CC49 and CC599. The occurrence of the <i>mecC</i> gene in many different hosts highlighted its One Health importance, even though European hedgehogs (<i>Erinaceus europaeus</i>) are considered its natural reservoir, most probably because of the selective pressure imposed by beta-lactam-producing dermatophytes (<i>Trichophyton erinacei</i>) that colonize the skin of these mammals. Surprisingly, while the presence of <i>T. erinacei</i> on the French territory has been proven, no <i>mecC</i>-positive methicillin-resistant <i>Staphylococcus aureus</i> (MRSA) isolate has been reported yet from hedgehogs. We thus sampled 139 hedgehogs brought to a wildlife center; 128 were <i>S. aureus</i> carriers and 25 (18.0 %) presented a MRSA isolate, of which 21 (15.1 %) displayed the <i>mecC</i> gene. All 161 <i>S. aureus</i> collected were whole-genome sequenced. The <i>mecC</i>-MRSA belonged to the classical CCs, i.e. CC130, CC1943 and CC49. The majority (98/139, 70.5 %) of the methicillin-susceptible <i>Staphylococcus aureus</i> (MSSA) isolates also belonged to these three CCs. A phylogenetic comparison with <i>mecC</i>-MRSA isolates from all over Europe and New-Zealand showed local adaptations, despite the fact that they all belonged to the same CCs. The acquisition of the SCC<i>mec</i> type XI element by a concomitant MSSA could not be observed in the same animal, but such a transfer might be suggested since identical clones were identified, one MSSA and one MRSA, though in different animals. In parallel, we conducted a detailed analysis of the SCC<i>mec</i> type XI element as well as specific virulence factors (a <i>tst</i> variant and the <i>vwb</i> <sub>SaPI</sub> gene). Results led us to hypothesize that the <i>mecC</i> gene might be acquired through selective pressure of <i>T. erinacei</i> on MSSA, some of which were acquired a long time ago from ruminants and are now colonizing the skin of the hedgehogs.

One HealthVol. 19
Université Claude Bernard Lyon 1 (FR), Statens Serum Institut (DK), Cegep de Saint Hyacinthe (CA), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Virologie et Pathologies Humaines (FR), Centre Hospitalier Vétérinaire Frégis (FR), Oniris (FR), Université de Montréal (CA)
Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail
Life in Land
Openalex Percentile: Top 11%
Microbial infections and disease research
2.41
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