The Composition and Structure of Biofilms Developed by Propionibacterium acnes Isolated from Cardiac Pacemaker Devices

Okuda, Kenichi; Nagahori, Ryuichi; Yamada, Sakuo; Sugimoto, Shinya; Sato, Chikara; Sato, Mari; Iwase, Tomoyuki; Hara, Kazuhiro; Mizunoe, Yoshimitsu

doi:10.3389/fmicb.2018.00182

Cited by 53 publications

(42 citation statements)

References 62 publications

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“…Considering the diffusion barrier limit imposed by the EPS in the biofilms, the protection provided is intrinsincally linked to its biochemical composition as examplified by the interactions between gentamicin and alginate, the major component of mucoid P. aeruginosa biofilms [58]. Variations in the components ensuring the structural integrity of biofilms formed by different isolates of a bacterial strain such as S. aureus [47,59] or Propionibacterium acnes [60] were previously reported. Accordingly, the heterogeneous composition of biofilms formed by F. novicida or F. philomiragia observed here is not surprising.…”

Section: Discussionmentioning

confidence: 99%

Francisella novicida and F. philomiragia biofilm features conditionning fitness in spring water and in presence of antibiotics

et al. 2020

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Biofilms are currently considered as a predominant lifestyle of many bacteria in nature. While they promote survival of microbes, biofilms also potentially increase the threats to animal and public health in case of pathogenic species. They not only facilitate bacteria transmission and persistence, but also promote spreading of antibiotic resistance leading to chronic infections. In the case of Francisella tularensis, the causative agent of tularemia, biofilms have remained largely enigmatic. Here, applying live and static confocal microscopy, we report growth and ultrastructural organization of the biofilms formed in vitro by these microorganisms over the early transition from coccobacillary into coccoid shape during biofilm assembly. Using selective dispersing agents, we provided evidence for extracellular DNA (eDNA) being a major and conserved structural component of mature biofilms formed by both F. subsp. novicida and a human clinical isolate of F. philomiragia. We also observed a higher physical robustness of F. novicida biofilm as compared to F. philomiragia one, a feature likely promoted by specific polysaccharides. Further, F. novicida biofilms resisted significantly better to ciprofloxacin than their planktonic counterparts. Importantly, when grown in biofilms, both Francisella species survived longer in cold water as compared to free-living bacteria, a trait possibly associated with a gain in fitness in the natural aquatic environment. Overall, this study provides information on survival of Francisella when embedded with biofilms that should improve both the future management of biofilm-related infections and the design of effective strategies to tackle down the problematic issue of bacteria persistence in aquatic ecosystems.

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Section: Discussionmentioning

confidence: 99%

Francisella novicida and F. philomiragia biofilm features conditionning fitness in spring water and in presence of antibiotics

et al. 2020

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“…Immunostaining with α-dsDNA combined with CLSM also revealed the existence of long filaments of eDNA in biofilms formed either by Enterococcus faecalis (45) or Haemophilus influenzae ECM (46). Moreover, the presence of eDNA-containing fibrous structures in the ECM of Staphylococcus aureus and Propionibacterium acnes biofilms has also been reported using α-dsDNA and atmospheric scanning electron microscopy (47, 48). The use of different technical approaches reinforces the idea that the fibrous assemblies of eDNA observed in some bacterial biofilms actually exist and also offers a novel perspective of the ECM structure of pneumococcal biofilms.…”

Section: Discussionmentioning

confidence: 88%

Autolysin-Independent DNA Release inStreptococcus pneumoniae in vitroBiofilms

Domenech

Garcı́a

2018

Preprint

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Biofilms are defined as layers of cells of microorganisms 17 adhered to the surface of a substrate and embedded in an extracellular matrix 18 and provide an appropriate environment for increased genetic exchange. 19 Extracellular DNA (eDNA) is an essential component of the extracellular matrix 20 of microbial biofilms, but the pathway(s) responsible for DNA release are largely 21 unknown. Autolysis (either spontaneous or phage-induced) has been proposed 22 the major event leading to the appearance of eDNA. The 'suicidal tendency' of 23 Streptococcus pneumoniae is well-known, with lysis mainly caused by the 24 triggering of LytA, the major autolytic amidase. However, the LytC lysozyme 25 and CbpD (a possible murein hydrolase) have also been shown involved. The 26 present work examines the relationship between eDNA, autolysins, and the 27 formation and maintenance of in vitro pneumococcal biofilms, via fluorescent 28 labelling combined with confocal laser scanning microscopy, plus genetic 29 transformation experiments. Bacterial DNA release mechanisms other than 30 those entailing lytic enzymes were shown to be involved by demonstrating that 31 horizontal gene transfer in biofilms takes place even in the absence of 32 detectable autolytic activity. It had been previously suggested that the quorum 33 sensing systems ComABCDE and LuxS/AI-2 are involved in the production of 34 eDNA as a response to the accumulation of quorum sensing signals, although 35 our immunofluorescence results do not support this hypothesis. Evidence that 36 the release of DNA is somehow linked to the production of extracellular vesicles 37 by S. pneumoniae is provided. 38 IMPORTANCE Most human bacterial infections are caused by 39 microorganisms growing as biofilms. Bacteria in biofilms are less susceptible to 40 antimicrobials and to killing by the host immune system, are very difficult to 41 eliminate and cause recalcitrant and persistent diseases. Extracellular DNA is 42 one of the major components of the bacterial biofilm matrix. In the present 43 study, we provide direct evidence of the existence of biologically active 44 (transforming), extracellular DNA in Streptococcus pneumoniae biofilms. In 45 3previous studies, the involvement of three pneumococcal choline-binding 46 proteins with autolytic activity (LytA, LytC and CbpD) in DNA release had been 47 reported. In contrast, we demonstrate here that pneumococcal in vitro biofilms 48 do contain eDNA, even in the absence of these enzymes. Moreover, our results 49 suggest that DNA release in S. pneumoniae biofilms is connected with the 50 production of extracellular vesicles and that this DNA is associated to the outer 51 part of the vesicles. 52 53 4The human pathogen Streptococcus pneumoniae is a leading cause of 54 pneumonia, meningitis and bloodstream infections in the elderly, and one of the 55 main pathogens responsible for middle ear infections in children. It is carried 56 asymptomatically in the nasopharynx of many healthy adults, and in as many as 57 20-40% of healthy children ...

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“…It is most widely recognized as contributing to the pathogenesis of acne, while less appreciated in the pathogenesis of other conditions. The ability of C. acnes to form biofilms may be its most recognized virulence factor, as it can colonize artificial substrates [ 3 ]. It has been recently suggested that lysis of bacterial cells and release of cytoplasmic contents facilitate the formation of their biofilm [ 3 ].…”

Section: Discussionmentioning

confidence: 99%

“…The ability of C. acnes to form biofilms may be its most recognized virulence factor, as it can colonize artificial substrates [ 3 ]. It has been recently suggested that lysis of bacterial cells and release of cytoplasmic contents facilitate the formation of their biofilm [ 3 ]. Biofilm production may have been an important factor in the case presented, as the patient continued to have several positive blood cultures over the course of 4 years that were incompletely treated with antibiotics.…”

Section: Discussionmentioning

confidence: 99%

“…Shoulder prosthetic joint infections and cerebrovascular shunt infections are the most common, but infections of cardiovascular devices are also being identified now [2]. It is hypothesized that the ability of certain strains of C. acnes to produce biofilms can lead to colonization of cardiac pacemaker devices without overt signs of clinical infection [3].…”

Section: Introductionmentioning

confidence: 99%

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Persistent Cutibacterium (Formerly Propionibacterium) acnes Bacteremia and Refractory Endocarditis in a Patient with Retained Implantable Pacemaker Leads

Freedman

Aflatooni

Foster

et al. 2020

Case Reports in Infectious Diseases

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Cutibacterium (formerly Propionibacterium) acnes (C. acnes) is a commensal bacteria commonly found on the human skin and in the mouth. While the virulence of C. acnes is low in humans, it does produce a biofilm and has been identified as an etiologic agent in a growing number of implant-associated infections. C. acnes infections can prove diagnostically challenging as laboratory cultures can often take greater than 5 days to yield positive results, which are then often disregarded as contaminant. Patients with recurrent bacteremia in the setting of implantable devices warrant further studies to evaluate for an associated valvular or lead endocarditis. The patient in this report demonstrates how cardiac device-related endocarditis secondary to C. acnes can be overlooked due to the indolent nature of this pathogen. This patient presented with an implanted cardiac pacemaker device, as well as retained leads from a prior pacemaker. Transesophageal echocardiography was required to confirm the diagnosis in the setting of multiple positive blood cultures and negative transthoracic echocardiograms over a period of 4 years. The purpose of this report is to highlight the difficulties encountered in diagnosing C. acnes endocarditis in a patient with a cardiac implantable electronic device and persistently positive blood cultures.

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The Composition and Structure of Biofilms Developed by Propionibacterium acnes Isolated from Cardiac Pacemaker Devices

Cited by 53 publications

References 62 publications

Francisella novicida and F. philomiragia biofilm features conditionning fitness in spring water and in presence of antibiotics

Francisella novicida and F. philomiragia biofilm features conditionning fitness in spring water and in presence of antibiotics

Autolysin-Independent DNA Release inStreptococcus pneumoniae in vitroBiofilms

Persistent Cutibacterium (Formerly Propionibacterium) acnes Bacteremia and Refractory Endocarditis in a Patient with Retained Implantable Pacemaker Leads

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