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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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 |
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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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