Abstract
The present study aimed to understand the biofilm formation mechanism of Propionibacterium acnes by analyzing the components and structure of the biofilms. P. acnes strains were isolated from the surface of explanted cardiac pacemaker devices that exhibited no clinical signs of infection. Culture tests using a simple stamp culture method (pressing pacemakers against the surface of agar plates) revealed frequent P. acnes colonization on the surface of cardiac pacemaker devices. P. acnes was isolated from 7/31 devices, and the isolates were categorized by multilocus sequence typing into five different sequence types (STs): ST4 (JK18.2), ST53 (JK17.1), ST69 (JK12.2 and JK13.1), ST124 (JK5.3), ST125 (JK6.2), and unknown ST (JK19.3). An in vitro biofilm formation assay using microtiter plates demonstrated that 5/7 isolates formed biofilms. Inhibitory effects of DNase I and proteinase K on biofilm formation varied among isolates. In contrast, dispersin B showed no inhibitory activity against all isolates. Three-dimensional live/dead imaging of P. acnes biofilms with different biochemical properties using confocal laser microscopy demonstrated different distributions and proportions of living and dead cells. Additionally, it was suggested that extracellular DNA (eDNA) plays a role in the formation of biofilms containing living cells. Ultrastructural analysis of P. acnes biofilms using a transmission electron microscope and atmospheric scanning electron microscope revealed leakage of cytoplasmic components along with cell lysis and fibrous structures of eDNA connecting cells. In conclusion, the biochemical properties and structures of the biofilms differed among P. acnes isolates. These findings may provide clues for establishing countermeasures against biofilm-associated infection by P. acnes.
Highlights
Biofilms are clusters of microorganisms formed on biotic or abiotic surfaces (Hall-Stoodley et al, 2004)
Propionibacterium acnes has been reported to cause infections associated with implanted medical aids, such as cardiac devices (Chua et al, 1998; Zedtwitz-Liebenstein et al, 2003; Haidar et al, 2010), breast implants (Del Pozo et al, 2009; Rieger et al, 2009), and prosthetic joints (Piper et al, 2009)
Rohacek et al (2010) conducted culture tests of 115 asymptomatic pacemakers using sonication, which led to the isolation of mainly P. acnes and coagulase-negative staphylococcus (CNS)
Summary
Biofilms are clusters of microorganisms formed on biotic or abiotic surfaces (Hall-Stoodley et al, 2004). Bacterial cells in biofilms are embedded within a self-produced extracellular matrix (ECM) consisting of biomolecules such as nucleic acids, polysaccharides, and proteins (Flemming and Wingender, 2010). Pseudomonas aeruginosa produces at least three distinct alginate exopolysaccharides involving Pel and Psl that contribute to biofilm development and architecture (Ryder et al, 2007; Flemming and Wingender, 2010). In non-mucoid strains, which do not express alginate biosynthesis genes, Pel and Psl are involved in the establishment of biofilms (Flemming and Wingender, 2010). It has been shown that Haemophilus influenzae produces an ECM composed of proteins, nucleic acids, and a β-glucan during biofilm formation. EDNA appears to be an important component of ECM and essential in biofilm maintenance (Domenech et al, 2016)
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