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      Sortase-assembled pili promote extracellular electron transfer and iron acquisition in Enterococcus faecalis biofilm

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          Abstract

          Enterococcus faecalis is an opportunistic human pathogen and the cause of biofilm-associated infections of the heart, catheterized urinary tract, wounds, and the dysbiotic gut where it can expand to high numbers upon microbiome perturbations. The E. faecalis sortase-assembled endocarditis and biofilm associated pilus (Ebp) is involved in adhesion and biofilm formation in vitro and in vivo. Extracellular electron transfer (EET) also promotes E. faecalis biofilm formation in iron-rich environments, however neither the mechanism underlying EET nor its role in virulence was previously known. Here we show that iron associated with Ebp serve as a terminal electron acceptor for EET, leading to extracellular iron reduction and intracellular iron accumulation. We found that a MIDAS motif within the EbpA tip adhesin is required for interaction with iron, EET, and FeoB-mediated iron uptake. We demonstrate that MenB and Ndh3, essential components of the aerobic respiratory chain and a specialized flavin-mediated electron transport chain, respectively, are required for iron-mediated EET. In addition, using a mouse gastrointestinal (GI) colonization model, we show that EET is essential for colonization of the GI tract, and Ebp is essential for augmented E. faecalis GI colonization when dietary iron is in excess. Taken together, our findings show that pilus mediated capture of iron within biofilms enables EET-mediated iron acquisition in E. faecalis, and that these processes plays an important role in E. faecalis expansion in the GI tract.

          Significance

          Understanding enterococcal biofilm development is the first step towards improved therapeutics for the often antimicrobial resistant infections caused by these bacteria. Here we report a role for Enterococcus faecalis endocarditis and biofilm associated pili (Ebp) in mediating iron-dependent biofilm growth and contributing to extracellular electron transfer (EET) which in turn promotes iron acquisition. Furthermore, we characterize the mechanisms underlying electron transfer in the E. faecalis biofilm. Our findings support a model in which E. faecalis use EET to drive the reduction of pilus-associated ferric iron, leading to iron acquisition in E. faecalis biofilm, and contributing to enterococcal virulence in the GI tract.

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          Author and article information

          Journal
          bioRxiv
          April 07 2019
          10.1101/601666
          © 2019
          Product

          Microbiology & Virology

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