Marsili, E. | Search bioRxiv

bioRxiv2019

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

Enterococcus faecalis sortase-assembled endocarditis and biofilm-associated pili (Ebp) are a virulence factor implicated in enterococcal biofilm-associated infections and gastrointestinal colonization. We previously showed that E. faecalis biofilm metabolism is influenced by extracellular electron transfer (EET) under iron-rich conditions, raising the question of whether Ebp pili also play a role in EET. Here, we report a novel role of Ebp pili in E. faecalis adhesion to the iron oxides magnetite, goethite and hematite, where the EbpA tip adhesin contributes to this interaction. Adhesion by Ebp pili is conditionally important for EET to iron oxides, as pilus mutants are attenuated in EET under non-static growth conditions. In alignment with the established role of EET in redox homeostasis, we find that EET to ferricyanide supports E. faecalis anaerobic growth on glycerol. Further, in an antibiotic-treated mouse gastrointestinal colonization model, we show that E. faecalis mutants deficient in EET poorly colonize the intestinal niche. Taken together, our findings suggest that Ebp pili can influence E. faecalis metabolic fitness by promoting EET to iron oxides, raising new questions of how Ebp pili shape E. faecalis interactions with environmental ecosystems. Furthermore, the important role of EET in E. faecalis colonization of the dysbiotic gastrointestinal environment highlights the need for further inquiry into how EET contributes to E. faecalis microbial pathogenesis. ImportanceIn this study, we explored the interplay between extracellular electron transfer (EET) and an Enterococcus faecalis biofilm factor, the endocarditis and biofilm-associated pili (Ebp). We demonstrate that Ebp pili have a novel role in adhesion to iron oxides, which consequently promotes EET to iron oxides under non-static conditions. Along with our findings that E. faecalis EET can be coupled to anaerobic cell growth, our results point to a potential ecological role of Ebp pili in natural environments, outside of its established function in adhesion to host ligands. We provide the first evidence of the contribution of EET to E. faecalis colonization of the antibiotic-treated murine intestinal niche, which adds to the limited experimental evidence linking EET and microbial pathogenesis, as well as highlights the need for further studies of EET in bacterial pathogens.

microbiology↗

bioRxiv2017

Extracellular Electron Transfer Powers Enterococcus faecalis Biofilm Metabolism

Enterococci are important human commensals and significant opportunistic pathogens associated with endocarditis, urinary tract infections, wound and surgical site infections, and medical device associated infections. These infections often become chronic upon the formation of biofilm. The biofilm matrix establishes properties that distinguish this state from free-living bacterial cells and increase tolerance to antimicrobial interventions. The metabolic versatility of the Enterococci is reflected in the diversity and complexity of environments and communities in which they thrive. Understanding metabolic factors governing colonization and persistence in different host niches can reveal factors influencing the transition from commensal to opportunistic pathogen. Here, we report a new form of iron-dependent metabolism for Enterococcus faecalis where, in the absence of heme, respiration components can be utilised for extracellular electron transfer (EET). Iron augments E. faecalis biofilm growth and generates alterations in biofilm matrix, cell spatial distribution, and biofilm matrix properties. We identify the genes involved in iron-augmented biofilm growth and show that it occurs by promoting EET to iron within biofilm.\n\nSignificanceBacterial metabolic versatility is often key in dictating the outcome of host-pathogen interactions, yet determinants of metabolic shifts are difficult to resolve. The bacterial biofilm matrix provides the structural and functional support that distinguishes this state from free-living bacterial cells. Here, we show that the biofilm matrix provides access to resources necessary for metabolism and growth which are otherwise inaccessible in the planktonic state. Our data shows that in the absence of heme, components of Enterococcus faecalis respiration (l-lactate dehydrogenase and acetaldehyde dehydrogenase) may function as initiators of EET through the cytoplasmic membrane quinone pool and utilize matrix-associated iron to carry out EET. The presence of iron resources within the biofilm matrix leads to enhanced biofilm growth.

microbiology↗