Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>

ABSTRACT Staphylococcus pseudintermedius is a major canine pathogen but also occasionally colonizes and infects humans. Multidrug-resistant methicillin-resistant S. pseudintermedius (MDR MRSP) strains have emerged globally, making treatment and control of this pathogen challenging. Sequence type 71...

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Autores principales:	Alem Zukancic, Mubin A. Khan, Sumayya J. Gurmen, Quinn M. Gliniecki, Dayna L. Moritz-Kinkade, Carol W. Maddox, Md Tauqeer Alam
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Staphylococcus antibiotic resistance genomics horizontal gene transfer Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/02b9388c932a43c191f7f5d13874d3b2
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spelling	oai:doaj.org-article:02b9388c932a43c191f7f5d13874d3b22021-11-15T15:30:59ZStaphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>10.1128/mSphere.00666-202379-5042https://doaj.org/article/02b9388c932a43c191f7f5d13874d3b22020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00666-20https://doaj.org/toc/2379-5042ABSTRACT Staphylococcus pseudintermedius is a major canine pathogen but also occasionally colonizes and infects humans. Multidrug-resistant methicillin-resistant S. pseudintermedius (MDR MRSP) strains have emerged globally, making treatment and control of this pathogen challenging. Sequence type 71 (ST71), ST68, and ST45 are the most widespread and successful MDR MRSP clones. The potential genetic factors underlying the clonal success of these and other predominant clones remain unknown. Characterization of the pangenome, lineage-associated accessory genes, and genes acquired through horizontal gene transfer from other bacteria is important for identifying such factors. Here, we analyzed genome sequence data from 622 S. pseudintermedius isolates to investigate the evolution of pathogenicity across lineages. We show that the predominant clones carry one or more lineage-associated virulence genes. The gene encoding staphylococcal protein A (SpA), a key virulence factor involved in immune evasion and a potential vaccine antigen, is deleted in 62% of isolates. Most importantly, we have discovered that the spa locus is a hot spot for recombination and horizontal gene transfer in S. pseudintermedius, where genes related to restriction modification, prophage immunity, mercury resistance, and nucleotide and carbohydrate metabolism have been acquired in different lineages. Our study also establishes that ST45 is composed of two distinct sublineages that differ in their accessory gene content and virulence potential. Collectively, this study reports several previously undetected lineage-associated genetic factors that may have a role in the clonal success of the major MDR MRSP clones. These data provide a framework for future experimental studies on S. pseudintermedius pathogenesis and for developing novel therapeutics against this pathogen. IMPORTANCE Staphylococcus pseudintermedius is a major canine pathogen but can also occasionally infect humans. Identification of genetic factors contributing to the virulence and clonal success of multidrug-resistant S. pseudintermedius clones is critical for the development of therapeutics against this pathogen. Here, we characterized the genome sequences of a global collection of 622 S. pseudintermedius isolates. We show that all major clones, besides carrying core virulence genes, which are present in all strains, carry one or more lineage-specific genes. Many of these genes have been acquired from other bacterial species through a horizontal gene transfer mechanism. Importantly, we have discovered that the staphylococcal protein A gene (spa), a widely used marker for molecular typing of S. pseudintermedius strains and a potential vaccine candidate antigen, is deleted in 62% of strains. Furthermore, the spa locus in S. pseudintermedius acts as a reservoir to accumulate lineage-associated genes with adaptive functions.Alem ZukancicMubin A. KhanSumayya J. GurmenQuinn M. GlinieckiDayna L. Moritz-KinkadeCarol W. MaddoxMd Tauqeer AlamAmerican Society for MicrobiologyarticleStaphylococcusantibiotic resistancegenomicshorizontal gene transferMicrobiologyQR1-502ENmSphere, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Staphylococcus antibiotic resistance genomics horizontal gene transfer Microbiology QR1-502
spellingShingle	Staphylococcus antibiotic resistance genomics horizontal gene transfer Microbiology QR1-502 Alem Zukancic Mubin A. Khan Sumayya J. Gurmen Quinn M. Gliniecki Dayna L. Moritz-Kinkade Carol W. Maddox Md Tauqeer Alam Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
description	ABSTRACT Staphylococcus pseudintermedius is a major canine pathogen but also occasionally colonizes and infects humans. Multidrug-resistant methicillin-resistant S. pseudintermedius (MDR MRSP) strains have emerged globally, making treatment and control of this pathogen challenging. Sequence type 71 (ST71), ST68, and ST45 are the most widespread and successful MDR MRSP clones. The potential genetic factors underlying the clonal success of these and other predominant clones remain unknown. Characterization of the pangenome, lineage-associated accessory genes, and genes acquired through horizontal gene transfer from other bacteria is important for identifying such factors. Here, we analyzed genome sequence data from 622 S. pseudintermedius isolates to investigate the evolution of pathogenicity across lineages. We show that the predominant clones carry one or more lineage-associated virulence genes. The gene encoding staphylococcal protein A (SpA), a key virulence factor involved in immune evasion and a potential vaccine antigen, is deleted in 62% of isolates. Most importantly, we have discovered that the spa locus is a hot spot for recombination and horizontal gene transfer in S. pseudintermedius, where genes related to restriction modification, prophage immunity, mercury resistance, and nucleotide and carbohydrate metabolism have been acquired in different lineages. Our study also establishes that ST45 is composed of two distinct sublineages that differ in their accessory gene content and virulence potential. Collectively, this study reports several previously undetected lineage-associated genetic factors that may have a role in the clonal success of the major MDR MRSP clones. These data provide a framework for future experimental studies on S. pseudintermedius pathogenesis and for developing novel therapeutics against this pathogen. IMPORTANCE Staphylococcus pseudintermedius is a major canine pathogen but can also occasionally infect humans. Identification of genetic factors contributing to the virulence and clonal success of multidrug-resistant S. pseudintermedius clones is critical for the development of therapeutics against this pathogen. Here, we characterized the genome sequences of a global collection of 622 S. pseudintermedius isolates. We show that all major clones, besides carrying core virulence genes, which are present in all strains, carry one or more lineage-specific genes. Many of these genes have been acquired from other bacterial species through a horizontal gene transfer mechanism. Importantly, we have discovered that the staphylococcal protein A gene (spa), a widely used marker for molecular typing of S. pseudintermedius strains and a potential vaccine candidate antigen, is deleted in 62% of strains. Furthermore, the spa locus in S. pseudintermedius acts as a reservoir to accumulate lineage-associated genes with adaptive functions.
format	article
author	Alem Zukancic Mubin A. Khan Sumayya J. Gurmen Quinn M. Gliniecki Dayna L. Moritz-Kinkade Carol W. Maddox Md Tauqeer Alam
author_facet	Alem Zukancic Mubin A. Khan Sumayya J. Gurmen Quinn M. Gliniecki Dayna L. Moritz-Kinkade Carol W. Maddox Md Tauqeer Alam
author_sort	Alem Zukancic
title	Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_short	Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_full	Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_fullStr	Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_full_unstemmed	Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>
title_sort	staphylococcal protein a (<italic toggle="yes">spa</italic>) locus is a hot spot for recombination and horizontal gene transfer in <named-content content-type="genus-species">staphylococcus pseudintermedius</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/02b9388c932a43c191f7f5d13874d3b2
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Staphylococcal Protein A (<italic toggle="yes">spa</italic>) Locus Is a Hot Spot for Recombination and Horizontal Gene Transfer in <named-content content-type="genus-species">Staphylococcus pseudintermedius</named-content>

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