Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus Strains

Staphylococcus aureus is an opportunistic pathogen of humans and warm-blooded animals and presents a growing threat in terms of multi-drug resistance. Despite numerous studies, the basis of staphylococcal virulence and switching between commensal and pathogenic phenotypes is not fully understood. Us...

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Main Authors: Emilia A. Bonar, Michal Bukowski, Marcin Hydzik, Urszula Jankowska, Sylwia Kedracka-Krok, Magdalena Groborz, Grzegorz Dubin, Viktoria Akkerboom, Jacek Miedzobrodzki, Artur J. Sabat, Alexander W. Friedrich, Benedykt Wladyka
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-09-01
Series:Frontiers in Cellular and Infection Microbiology
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Online Access:https://www.frontiersin.org/article/10.3389/fcimb.2018.00313/full
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author Emilia A. Bonar
Michal Bukowski
Marcin Hydzik
Urszula Jankowska
Sylwia Kedracka-Krok
Magdalena Groborz
Grzegorz Dubin
Grzegorz Dubin
Viktoria Akkerboom
Jacek Miedzobrodzki
Artur J. Sabat
Alexander W. Friedrich
Benedykt Wladyka
author_facet Emilia A. Bonar
Michal Bukowski
Marcin Hydzik
Urszula Jankowska
Sylwia Kedracka-Krok
Magdalena Groborz
Grzegorz Dubin
Grzegorz Dubin
Viktoria Akkerboom
Jacek Miedzobrodzki
Artur J. Sabat
Alexander W. Friedrich
Benedykt Wladyka
author_sort Emilia A. Bonar
collection DOAJ
description Staphylococcus aureus is an opportunistic pathogen of humans and warm-blooded animals and presents a growing threat in terms of multi-drug resistance. Despite numerous studies, the basis of staphylococcal virulence and switching between commensal and pathogenic phenotypes is not fully understood. Using genomics, we show here that S. aureus strains exhibiting virulent (VIR) and non-virulent (NVIR) phenotypes in a chicken embryo infection model genetically fall into two separate groups, with the VIR group being much more cohesive than the NVIR group. Significantly, the genes encoding known staphylococcal virulence factors, such as clumping factors, are either found in different allelic variants in the genomes of NVIR strains (compared to VIR strains) or are inactive pseudogenes. Moreover, the pyruvate carboxylase and gamma-aminobutyrate permease genes, which were previously linked with virulence, are pseudogenized in NVIR strain ch22. Further, we use comprehensive proteomics tools to characterize strains that show opposing phenotypes in a chicken embryo virulence model. VIR strain CH21 had an elevated level of diapolycopene oxygenase involved in staphyloxanthin production (protection against free radicals) and expressed a higher level of immunoglobulin-binding protein Sbi on its surface compared to NVIR strain ch22. Furthermore, joint genomic and proteomic approaches linked the elevated production of superoxide dismutase and DNA-binding protein by NVIR strain ch22 with gene duplications.
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spelling doaj.art-fc441c71aed14b348367dc832abb52402022-12-22T00:25:51ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882018-09-01810.3389/fcimb.2018.00313395188Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus StrainsEmilia A. Bonar0Michal Bukowski1Marcin Hydzik2Urszula Jankowska3Sylwia Kedracka-Krok4Magdalena Groborz5Grzegorz Dubin6Grzegorz Dubin7Viktoria Akkerboom8Jacek Miedzobrodzki9Artur J. Sabat10Alexander W. Friedrich11Benedykt Wladyka12Department of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandDepartment of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandDepartment of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandMalopolska Centre of Biotechnology, Jagiellonian University, Krakow, PolandDepartment of Physical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandDepartment of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandMalopolska Centre of Biotechnology, Jagiellonian University, Krakow, PolandDepartment of Microbiology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandDepartment of Medical Microbiology, University Medical Center Groningen, University of Groningen, Groningen, NetherlandsDepartment of Microbiology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandDepartment of Medical Microbiology, University Medical Center Groningen, University of Groningen, Groningen, NetherlandsDepartment of Medical Microbiology, University Medical Center Groningen, University of Groningen, Groningen, NetherlandsDepartment of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, PolandStaphylococcus aureus is an opportunistic pathogen of humans and warm-blooded animals and presents a growing threat in terms of multi-drug resistance. Despite numerous studies, the basis of staphylococcal virulence and switching between commensal and pathogenic phenotypes is not fully understood. Using genomics, we show here that S. aureus strains exhibiting virulent (VIR) and non-virulent (NVIR) phenotypes in a chicken embryo infection model genetically fall into two separate groups, with the VIR group being much more cohesive than the NVIR group. Significantly, the genes encoding known staphylococcal virulence factors, such as clumping factors, are either found in different allelic variants in the genomes of NVIR strains (compared to VIR strains) or are inactive pseudogenes. Moreover, the pyruvate carboxylase and gamma-aminobutyrate permease genes, which were previously linked with virulence, are pseudogenized in NVIR strain ch22. Further, we use comprehensive proteomics tools to characterize strains that show opposing phenotypes in a chicken embryo virulence model. VIR strain CH21 had an elevated level of diapolycopene oxygenase involved in staphyloxanthin production (protection against free radicals) and expressed a higher level of immunoglobulin-binding protein Sbi on its surface compared to NVIR strain ch22. Furthermore, joint genomic and proteomic approaches linked the elevated production of superoxide dismutase and DNA-binding protein by NVIR strain ch22 with gene duplications.https://www.frontiersin.org/article/10.3389/fcimb.2018.00313/fullgenomegenomicspathogenproteomeproteomicsStaphylococcus aureus
spellingShingle Emilia A. Bonar
Michal Bukowski
Marcin Hydzik
Urszula Jankowska
Sylwia Kedracka-Krok
Magdalena Groborz
Grzegorz Dubin
Grzegorz Dubin
Viktoria Akkerboom
Jacek Miedzobrodzki
Artur J. Sabat
Alexander W. Friedrich
Benedykt Wladyka
Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus Strains
Frontiers in Cellular and Infection Microbiology
genome
genomics
pathogen
proteome
proteomics
Staphylococcus aureus
title Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus Strains
title_full Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus Strains
title_fullStr Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus Strains
title_full_unstemmed Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus Strains
title_short Joint Genomic and Proteomic Analysis Identifies Meta-Trait Characteristics of Virulent and Non-virulent Staphylococcus aureus Strains
title_sort joint genomic and proteomic analysis identifies meta trait characteristics of virulent and non virulent staphylococcus aureus strains
topic genome
genomics
pathogen
proteome
proteomics
Staphylococcus aureus
url https://www.frontiersin.org/article/10.3389/fcimb.2018.00313/full
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