Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue

Inflammation is one of the hallmarks of prostate cancer. The origin of inflammation is unknown, but microbial infections are suspected to play a role. In previous studies, the Gram-positive, low virulent bacterium Cutibacterium (formerly Propionibacterium) acnes was frequently isolated from prostati...

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Main Authors: Sabina Davidsson, Jessica Carlsson, Paula Mölling, Natyra Gashi, Ove Andrén, Swen-Olof Andersson, Elzbieta Brzuszkiewicz, Anja Poehlein, Munir A. Al-Zeer, Volker Brinkmann, Carsten Scavenius, Seven Nazipi, Bo Söderquist, Holger Brüggemann
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-11-01
Series:Frontiers in Microbiology
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Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.02241/full
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spelling doaj-cf826655653942d9b925157efec7160f2020-11-24T21:13:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-11-01810.3389/fmicb.2017.02241301550Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic TissueSabina Davidsson0Jessica Carlsson1Paula Mölling2Natyra Gashi3Ove Andrén4Swen-Olof Andersson5Elzbieta Brzuszkiewicz6Anja Poehlein7Munir A. Al-Zeer8Volker Brinkmann9Carsten Scavenius10Seven Nazipi11Bo Söderquist12Holger Brüggemann13Department of Urology, Faculty of Medicine and Health, Örebro University, Örebro, SwedenDepartment of Urology, Faculty of Medicine and Health, Örebro University, Örebro, SwedenDepartment of Laboratory Medicine, Clinical Microbiology, Faculty of Medicine and Health, Örebro University, Örebro, SwedenDepartment of Urology, Faculty of Medicine and Health, Örebro University, Örebro, SwedenDepartment of Urology, Faculty of Medicine and Health, Örebro University, Örebro, SwedenDepartment of Urology, Faculty of Medicine and Health, Örebro University, Örebro, SwedenDepartment of Genomic and Applied Microbiology, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, GermanyDepartment of Genomic and Applied Microbiology, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, GermanyDepartment of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, GermanyMicroscopy Core Facility, Max Planck Institute for Infection Biology, Berlin, GermanyDepartment of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkDepartment of Biomedicine, Aarhus University, Aarhus, DenmarkDepartment of Laboratory Medicine, Clinical Microbiology, Faculty of Medicine and Health, Örebro University, Örebro, SwedenDepartment of Biomedicine, Aarhus University, Aarhus, DenmarkInflammation is one of the hallmarks of prostate cancer. The origin of inflammation is unknown, but microbial infections are suspected to play a role. In previous studies, the Gram-positive, low virulent bacterium Cutibacterium (formerly Propionibacterium) acnes was frequently isolated from prostatic tissue. It is unclear if the presence of the bacterium represents a true infection or a contamination. Here we investigated Cutibacterium acnes type II, also called subspecies defendens, which is the most prevalent type among prostatic C. acnes isolates. Genome sequencing of type II isolates identified large plasmids in several genomes. The plasmids are highly similar to previously identified linear plasmids of type I C. acnes strains associated with acne vulgaris. A PCR-based analysis revealed that 28.4% (21 out of 74) of all type II strains isolated from cancerous prostates carry a plasmid. The plasmid shows signatures for conjugative transfer. In addition, it contains a gene locus for tight adherence (tad) that is predicted to encode adhesive Flp (fimbrial low-molecular weight protein) pili. In subsequent experiments a tad locus-encoded putative pilin subunit was identified in the surface-exposed protein fraction of plasmid-positive C. acnes type II strains by mass spectrometry, indicating that the tad locus is functional. Additional plasmid-encoded proteins were detected in the secreted protein fraction, including two signal peptide-harboring proteins; the corresponding genes are specific for type II C. acnes, thus lacking from plasmid-positive type I C. acnes strains. Further support for the presence of Flp pili in C. acnes type II was provided by electron microscopy, revealing cell appendages in tad locus-positive strains. Our study provides new insight in the most prevalent prostatic subspecies of C. acnes, subsp. defendens, and indicates the existence of Flp pili in plasmid-positive strains. Such pili may support colonization and persistent infection of human prostates by C. acnes.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02241/fullCutibacterium acnesPropionibacterium acnesplasmidfimbrial low-molecular weight proteinpilitight adherence
collection DOAJ
language English
format Article
sources DOAJ
author Sabina Davidsson
Jessica Carlsson
Paula Mölling
Natyra Gashi
Ove Andrén
Swen-Olof Andersson
Elzbieta Brzuszkiewicz
Anja Poehlein
Munir A. Al-Zeer
Volker Brinkmann
Carsten Scavenius
Seven Nazipi
Bo Söderquist
Holger Brüggemann
spellingShingle Sabina Davidsson
Jessica Carlsson
Paula Mölling
Natyra Gashi
Ove Andrén
Swen-Olof Andersson
Elzbieta Brzuszkiewicz
Anja Poehlein
Munir A. Al-Zeer
Volker Brinkmann
Carsten Scavenius
Seven Nazipi
Bo Söderquist
Holger Brüggemann
Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue
Frontiers in Microbiology
Cutibacterium acnes
Propionibacterium acnes
plasmid
fimbrial low-molecular weight protein
pili
tight adherence
author_facet Sabina Davidsson
Jessica Carlsson
Paula Mölling
Natyra Gashi
Ove Andrén
Swen-Olof Andersson
Elzbieta Brzuszkiewicz
Anja Poehlein
Munir A. Al-Zeer
Volker Brinkmann
Carsten Scavenius
Seven Nazipi
Bo Söderquist
Holger Brüggemann
author_sort Sabina Davidsson
title Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue
title_short Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue
title_full Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue
title_fullStr Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue
title_full_unstemmed Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue
title_sort prevalence of flp pili-encoding plasmids in cutibacterium acnes isolates obtained from prostatic tissue
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-11-01
description Inflammation is one of the hallmarks of prostate cancer. The origin of inflammation is unknown, but microbial infections are suspected to play a role. In previous studies, the Gram-positive, low virulent bacterium Cutibacterium (formerly Propionibacterium) acnes was frequently isolated from prostatic tissue. It is unclear if the presence of the bacterium represents a true infection or a contamination. Here we investigated Cutibacterium acnes type II, also called subspecies defendens, which is the most prevalent type among prostatic C. acnes isolates. Genome sequencing of type II isolates identified large plasmids in several genomes. The plasmids are highly similar to previously identified linear plasmids of type I C. acnes strains associated with acne vulgaris. A PCR-based analysis revealed that 28.4% (21 out of 74) of all type II strains isolated from cancerous prostates carry a plasmid. The plasmid shows signatures for conjugative transfer. In addition, it contains a gene locus for tight adherence (tad) that is predicted to encode adhesive Flp (fimbrial low-molecular weight protein) pili. In subsequent experiments a tad locus-encoded putative pilin subunit was identified in the surface-exposed protein fraction of plasmid-positive C. acnes type II strains by mass spectrometry, indicating that the tad locus is functional. Additional plasmid-encoded proteins were detected in the secreted protein fraction, including two signal peptide-harboring proteins; the corresponding genes are specific for type II C. acnes, thus lacking from plasmid-positive type I C. acnes strains. Further support for the presence of Flp pili in C. acnes type II was provided by electron microscopy, revealing cell appendages in tad locus-positive strains. Our study provides new insight in the most prevalent prostatic subspecies of C. acnes, subsp. defendens, and indicates the existence of Flp pili in plasmid-positive strains. Such pili may support colonization and persistent infection of human prostates by C. acnes.
topic Cutibacterium acnes
Propionibacterium acnes
plasmid
fimbrial low-molecular weight protein
pili
tight adherence
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.02241/full
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