Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)

IntroductionParacoccus yeei is the first species in the genus Paracoccus to be implicated in opportunistic infections in humans. As a result, P. yeei strains provide a valuable model for exploring how bacteria shift from a saprophytic to a pathogenic lifestyle, as well as for investigating the role...

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Main Authors: Magdalena Szuplewska, Dorota Sentkowska, Robert Lasek, Przemysław Decewicz, Mateusz Hałucha, Łukasz Funk, Cora Chmielowska, Dariusz Bartosik
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483110/full
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author Magdalena Szuplewska
Dorota Sentkowska
Robert Lasek
Przemysław Decewicz
Mateusz Hałucha
Łukasz Funk
Cora Chmielowska
Dariusz Bartosik
author_facet Magdalena Szuplewska
Dorota Sentkowska
Robert Lasek
Przemysław Decewicz
Mateusz Hałucha
Łukasz Funk
Cora Chmielowska
Dariusz Bartosik
author_sort Magdalena Szuplewska
collection DOAJ
description IntroductionParacoccus yeei is the first species in the genus Paracoccus to be implicated in opportunistic infections in humans. As a result, P. yeei strains provide a valuable model for exploring how bacteria shift from a saprophytic to a pathogenic lifestyle, as well as for investigating the role of horizontally transferred DNA in this transition. In order to gain deeper insights into the unique characteristics of this bacterium and the molecular mechanisms underlying its opportunistic behavior, a comparative physiological and genomic analysis of P. yeei strains was performed.ResultsComplete genomic sequences of 7 P. yeei isolates (both clinical and environmental) were obtained and analyzed. All genomes have a multipartite structure comprising numerous extrachromosomal replicons (59 different ECRs in total), including large chromids of the DnaA-like and RepB families. Within the mobile part of the P. yeei genomes (ECRs and transposable elements, TEs), a novel non-autonomous MITE-type element was identified. Detailed genus-wide comparative genomic analysis permitted the identification of P. yeei-specific genes, including several putative virulence determinants. One of these, the URE gene cluster, determines the ureolytic activity of P. yeei strains—a unique feature among Paracoccus spp. This activity is induced by the inclusion of urea in the growth medium and is dependent on the presence of an intact nikR regulatory gene, which presumably regulates expression of nickel (urease cofactor) transporter genes.DiscussionThis in-depth comparative analysis provides a detailed insight into the structure, composition and properties of P. yeei genomes. Several predicted virulence determinants (including URE gene clusters) were identified within ECRs, indicating an important role for the flexible genome in determining the opportunistic properties of this bacterium.
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spelling doaj-art-7cc959eaac184d8f8d4caac69885588d2025-08-20T02:49:48ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-11-011510.3389/fmicb.2024.14831101483110Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)Magdalena Szuplewska0Dorota Sentkowska1Robert Lasek2Przemysław Decewicz3Mateusz Hałucha4Łukasz Funk5Cora Chmielowska6Dariusz Bartosik7Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Environmental Microbiology and Biotechnology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandIntroductionParacoccus yeei is the first species in the genus Paracoccus to be implicated in opportunistic infections in humans. As a result, P. yeei strains provide a valuable model for exploring how bacteria shift from a saprophytic to a pathogenic lifestyle, as well as for investigating the role of horizontally transferred DNA in this transition. In order to gain deeper insights into the unique characteristics of this bacterium and the molecular mechanisms underlying its opportunistic behavior, a comparative physiological and genomic analysis of P. yeei strains was performed.ResultsComplete genomic sequences of 7 P. yeei isolates (both clinical and environmental) were obtained and analyzed. All genomes have a multipartite structure comprising numerous extrachromosomal replicons (59 different ECRs in total), including large chromids of the DnaA-like and RepB families. Within the mobile part of the P. yeei genomes (ECRs and transposable elements, TEs), a novel non-autonomous MITE-type element was identified. Detailed genus-wide comparative genomic analysis permitted the identification of P. yeei-specific genes, including several putative virulence determinants. One of these, the URE gene cluster, determines the ureolytic activity of P. yeei strains—a unique feature among Paracoccus spp. This activity is induced by the inclusion of urea in the growth medium and is dependent on the presence of an intact nikR regulatory gene, which presumably regulates expression of nickel (urease cofactor) transporter genes.DiscussionThis in-depth comparative analysis provides a detailed insight into the structure, composition and properties of P. yeei genomes. Several predicted virulence determinants (including URE gene clusters) were identified within ECRs, indicating an important role for the flexible genome in determining the opportunistic properties of this bacterium.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483110/fullParacoccus yeeiopportunistic pathogenmultipartite genomechromidevolution of pathogenic bacteriatransposable element
spellingShingle Magdalena Szuplewska
Dorota Sentkowska
Robert Lasek
Przemysław Decewicz
Mateusz Hałucha
Łukasz Funk
Cora Chmielowska
Dariusz Bartosik
Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)
Frontiers in Microbiology
Paracoccus yeei
opportunistic pathogen
multipartite genome
chromid
evolution of pathogenic bacteria
transposable element
title Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)
title_full Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)
title_fullStr Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)
title_full_unstemmed Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)
title_short Genome-wide comparative analysis of clinical and environmental strains of the opportunistic pathogen Paracoccus yeei (Alphaproteobacteria)
title_sort genome wide comparative analysis of clinical and environmental strains of the opportunistic pathogen paracoccus yeei alphaproteobacteria
topic Paracoccus yeei
opportunistic pathogen
multipartite genome
chromid
evolution of pathogenic bacteria
transposable element
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483110/full
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