Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mec

<i>Staphylococcus pseudintermedius</i> is a frequent cause of infections in dogs. Infectious isolates of this coagulase-positive staphylococcal species are often methicillin- and multidrug-resistant, which complicates therapy. In staphylococci, methicillin resistance is encoded by determ...

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Main Authors: Gordon Y. C. Cheung, Ji Hyun Lee, Ryan Liu, Sara D. Lawhon, Ching Yang, Michael Otto
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/13/2/130
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author Gordon Y. C. Cheung
Ji Hyun Lee
Ryan Liu
Sara D. Lawhon
Ching Yang
Michael Otto
author_facet Gordon Y. C. Cheung
Ji Hyun Lee
Ryan Liu
Sara D. Lawhon
Ching Yang
Michael Otto
author_sort Gordon Y. C. Cheung
collection DOAJ
description <i>Staphylococcus pseudintermedius</i> is a frequent cause of infections in dogs. Infectious isolates of this coagulase-positive staphylococcal species are often methicillin- and multidrug-resistant, which complicates therapy. In staphylococci, methicillin resistance is encoded by determinants found on mobile genetic elements called Staphylococcal Chromosome Cassette <i>mec</i> (SCC<i>mec</i>), which, in addition to methicillin resistance factors, sometimes encode additional genes, such as further resistance factors and, rarely, virulence determinants. In this study, we analyzed SCC<i>mec</i> in a collection of infectious methicillin-resistant <i>S. pseudintermedius</i> (MRSP) isolates from predominant lineages in the United States. We found that several lineages characteristically have specific types of SCC<i>mec</i> elements and Agr types and harbor additional factors in their SCC<i>mec</i> elements that may promote virulence or affect DNA uptake. All isolates had SCC<i>mec</i>-encoded restriction–modification (R-M) systems of types I or II, and sequence types (STs) ST84 and ST64 had one type II and one type I R-M system, although the latter lacked a complete methylation enzyme gene. ST68 isolates also had an SCC<i>mec</i>-encoded CRISPR system. ST71 isolates had a <i>psm-mec</i> gene, which, in all but apparently Agr-dysfunctional isolates, produced a PSM-mec peptide toxin, albeit at relatively small amounts. This study gives detailed insight into the composition of SCC<i>mec</i> elements in infectious isolates of <i>S. pseudintermedius</i> and lays the genetic foundation for further efforts directed at elucidating the contribution of identified accessory SCC<i>mec</i> factors in impacting SCC<i>mec</i>-encoded and thus methicillin resistance-associated virulence and resistance to DNA uptake in this leading canine pathogen.
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spelling doaj.art-fb9bd3d64e2f42469e04b87a69e4228f2024-02-23T15:05:00ZengMDPI AGAntibiotics2079-63822024-01-0113213010.3390/antibiotics13020130Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mecGordon Y. C. Cheung0Ji Hyun Lee1Ryan Liu2Sara D. Lawhon3Ching Yang4Michael Otto5Pathogen Molecular Genetics Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), US National Institutes of Health (NIH), Bethesda, MD 20892, USAPathogen Molecular Genetics Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), US National Institutes of Health (NIH), Bethesda, MD 20892, USAPathogen Molecular Genetics Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), US National Institutes of Health (NIH), Bethesda, MD 20892, USADepartment of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843, USADepartment of Veterinary Biomedical Sciences, College of Veterinary Medicine, Long Island University, Brookville, NY 11548, USAPathogen Molecular Genetics Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), US National Institutes of Health (NIH), Bethesda, MD 20892, USA<i>Staphylococcus pseudintermedius</i> is a frequent cause of infections in dogs. Infectious isolates of this coagulase-positive staphylococcal species are often methicillin- and multidrug-resistant, which complicates therapy. In staphylococci, methicillin resistance is encoded by determinants found on mobile genetic elements called Staphylococcal Chromosome Cassette <i>mec</i> (SCC<i>mec</i>), which, in addition to methicillin resistance factors, sometimes encode additional genes, such as further resistance factors and, rarely, virulence determinants. In this study, we analyzed SCC<i>mec</i> in a collection of infectious methicillin-resistant <i>S. pseudintermedius</i> (MRSP) isolates from predominant lineages in the United States. We found that several lineages characteristically have specific types of SCC<i>mec</i> elements and Agr types and harbor additional factors in their SCC<i>mec</i> elements that may promote virulence or affect DNA uptake. All isolates had SCC<i>mec</i>-encoded restriction–modification (R-M) systems of types I or II, and sequence types (STs) ST84 and ST64 had one type II and one type I R-M system, although the latter lacked a complete methylation enzyme gene. ST68 isolates also had an SCC<i>mec</i>-encoded CRISPR system. ST71 isolates had a <i>psm-mec</i> gene, which, in all but apparently Agr-dysfunctional isolates, produced a PSM-mec peptide toxin, albeit at relatively small amounts. This study gives detailed insight into the composition of SCC<i>mec</i> elements in infectious isolates of <i>S. pseudintermedius</i> and lays the genetic foundation for further efforts directed at elucidating the contribution of identified accessory SCC<i>mec</i> factors in impacting SCC<i>mec</i>-encoded and thus methicillin resistance-associated virulence and resistance to DNA uptake in this leading canine pathogen.https://www.mdpi.com/2079-6382/13/2/130<i>Staphylococcus pseudintermedius</i>phenol-soluble modulinPSM-mecSCC<i>mec</i>AgrCRISPR
spellingShingle Gordon Y. C. Cheung
Ji Hyun Lee
Ryan Liu
Sara D. Lawhon
Ching Yang
Michael Otto
Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mec
Antibiotics
<i>Staphylococcus pseudintermedius</i>
phenol-soluble modulin
PSM-mec
SCC<i>mec</i>
Agr
CRISPR
title Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mec
title_full Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mec
title_fullStr Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mec
title_full_unstemmed Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mec
title_short Methicillin Resistance Elements in the Canine Pathogen <i>Staphylococcus pseudintermedius</i> and Their Association with the Peptide Toxin PSM-mec
title_sort methicillin resistance elements in the canine pathogen i staphylococcus pseudintermedius i and their association with the peptide toxin psm mec
topic <i>Staphylococcus pseudintermedius</i>
phenol-soluble modulin
PSM-mec
SCC<i>mec</i>
Agr
CRISPR
url https://www.mdpi.com/2079-6382/13/2/130
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