Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>

ABSTRACT Methicillin-resistant Staphylococcus pseudintermedius (MRSP) is a major cause of soft tissue infections in dogs and occasionally infects humans. Hypervirulent multidrug-resistant (MDR) MRSP clones have emerged globally. The sequence types ST71 and ST68, the major epidemic clones of Europe a...

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Autores principales:	Michael R. Brooks, Lyan Padilla-Vélez, Tarannum A. Khan, Azaan A. Qureshi, Jason B. Pieper, Carol W. Maddox, Md Tauqeer Alam
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Staphylococcus antibiotic resistance bacteriophage evolution drug resistance evolution genetic competence genomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dc492914b3d64ffca4c4a7ffe85d13cc
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spelling	oai:doaj.org-article:dc492914b3d64ffca4c4a7ffe85d13cc2021-12-02T18:39:47ZProphage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>10.1128/mSystems.00684-192379-5077https://doaj.org/article/dc492914b3d64ffca4c4a7ffe85d13cc2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00684-19https://doaj.org/toc/2379-5077ABSTRACT Methicillin-resistant Staphylococcus pseudintermedius (MRSP) is a major cause of soft tissue infections in dogs and occasionally infects humans. Hypervirulent multidrug-resistant (MDR) MRSP clones have emerged globally. The sequence types ST71 and ST68, the major epidemic clones of Europe and North America, respectively, have spread to other regions. The genetic factors underlying the success of these clones have not been investigated thoroughly. Here, we performed a comprehensive genomic analysis of 371 S. pseudintermedius isolates to dissect the differences between major clonal lineages. We show that the prevalence of genes associated with antibiotic resistance, virulence, prophages, restriction-modification (RM), and CRISPR/Cas systems differs significantly among MRSP clones. The isolates with GyrA+GrlA mutations, conferring fluoroquinolone resistance, carry more of these genes than those without GyrA+GrlA mutations. ST71 and ST68 clones carry lineage-specific prophages with genes that are likely associated with their increased fitness and virulence. We have discovered that a prophage, SpST71A, is inserted within the comGA gene of the late competence operon comG in the ST71 lineage. A functional comG is essential for natural genetic competence, which is one of the major modes of horizontal gene transfer (HGT) in bacteria. The RM and CRISPR/Cas systems, both major genetic barriers to HGT, are also lineage specific. Clones harboring CRISPR/Cas or a prophage-disrupted comG exhibited less genetic diversity and lower rates of recombination than clones lacking these systems. After Listeria monocytogenes, this is the second example of prophage-mediated competence disruption reported in any bacteria. These findings are important for understanding the evolution and clonal expansion of MDR MRSP clones. IMPORTANCE Staphylococcus pseudintermedius is a bacterium responsible for clinically important infections in dogs and can infect humans. In this study, we performed genomic analysis of 371 S. pseudintermedius isolates to understand the evolution of antibiotic resistance and virulence in this organism. The analysis covered significant reported clones, including ST71 and ST68, the major epidemic clones of Europe and North America, respectively. We show that the prevalence of genes associated with antibiotic resistance, virulence, prophages, and horizontal gene transfer differs among clones. ST71 and ST68 carry prophages with novel virulence and antibiotic resistance genes. Importantly, site-specific integration of a prophage, SpST71A, has led to the disruption of the genetic competence operon comG in ST71 clone. A functional comG is essential for the natural uptake of foreign DNA and thus plays an important role in the evolution of bacteria. This study provides insight into the emergence and evolution of antibiotic resistance and virulence in S. pseudintermedius, which may help in efforts to combat this pathogen.Michael R. BrooksLyan Padilla-VélezTarannum A. KhanAzaan A. QureshiJason B. PieperCarol W. MaddoxMd Tauqeer AlamAmerican Society for MicrobiologyarticleStaphylococcusantibiotic resistancebacteriophage evolutiondrug resistance evolutiongenetic competencegenomicsMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Staphylococcus antibiotic resistance bacteriophage evolution drug resistance evolution genetic competence genomics Microbiology QR1-502
spellingShingle	Staphylococcus antibiotic resistance bacteriophage evolution drug resistance evolution genetic competence genomics Microbiology QR1-502 Michael R. Brooks Lyan Padilla-Vélez Tarannum A. Khan Azaan A. Qureshi Jason B. Pieper Carol W. Maddox Md Tauqeer Alam Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
description	ABSTRACT Methicillin-resistant Staphylococcus pseudintermedius (MRSP) is a major cause of soft tissue infections in dogs and occasionally infects humans. Hypervirulent multidrug-resistant (MDR) MRSP clones have emerged globally. The sequence types ST71 and ST68, the major epidemic clones of Europe and North America, respectively, have spread to other regions. The genetic factors underlying the success of these clones have not been investigated thoroughly. Here, we performed a comprehensive genomic analysis of 371 S. pseudintermedius isolates to dissect the differences between major clonal lineages. We show that the prevalence of genes associated with antibiotic resistance, virulence, prophages, restriction-modification (RM), and CRISPR/Cas systems differs significantly among MRSP clones. The isolates with GyrA+GrlA mutations, conferring fluoroquinolone resistance, carry more of these genes than those without GyrA+GrlA mutations. ST71 and ST68 clones carry lineage-specific prophages with genes that are likely associated with their increased fitness and virulence. We have discovered that a prophage, SpST71A, is inserted within the comGA gene of the late competence operon comG in the ST71 lineage. A functional comG is essential for natural genetic competence, which is one of the major modes of horizontal gene transfer (HGT) in bacteria. The RM and CRISPR/Cas systems, both major genetic barriers to HGT, are also lineage specific. Clones harboring CRISPR/Cas or a prophage-disrupted comG exhibited less genetic diversity and lower rates of recombination than clones lacking these systems. After Listeria monocytogenes, this is the second example of prophage-mediated competence disruption reported in any bacteria. These findings are important for understanding the evolution and clonal expansion of MDR MRSP clones. IMPORTANCE Staphylococcus pseudintermedius is a bacterium responsible for clinically important infections in dogs and can infect humans. In this study, we performed genomic analysis of 371 S. pseudintermedius isolates to understand the evolution of antibiotic resistance and virulence in this organism. The analysis covered significant reported clones, including ST71 and ST68, the major epidemic clones of Europe and North America, respectively. We show that the prevalence of genes associated with antibiotic resistance, virulence, prophages, and horizontal gene transfer differs among clones. ST71 and ST68 carry prophages with novel virulence and antibiotic resistance genes. Importantly, site-specific integration of a prophage, SpST71A, has led to the disruption of the genetic competence operon comG in ST71 clone. A functional comG is essential for the natural uptake of foreign DNA and thus plays an important role in the evolution of bacteria. This study provides insight into the emergence and evolution of antibiotic resistance and virulence in S. pseudintermedius, which may help in efforts to combat this pathogen.
format	article
author	Michael R. Brooks Lyan Padilla-Vélez Tarannum A. Khan Azaan A. Qureshi Jason B. Pieper Carol W. Maddox Md Tauqeer Alam
author_facet	Michael R. Brooks Lyan Padilla-Vélez Tarannum A. Khan Azaan A. Qureshi Jason B. Pieper Carol W. Maddox Md Tauqeer Alam
author_sort	Michael R. Brooks
title	Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_short	Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_full	Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_fullStr	Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_full_unstemmed	Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_sort	prophage-mediated disruption of genetic competence in <named-content content-type="genus-species">staphylococcus pseudintermedius</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/dc492914b3d64ffca4c4a7ffe85d13cc
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Prophage-Mediated Disruption of Genetic Competence in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>

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