scholarly journals Extracellular Electron Transfer Powers Enterococcus faecalis Biofilm Metabolism

2017 ◽  
Author(s):  
Damien Keogh ◽  
Ling Ning Lam ◽  
Lucinda E. Doyle ◽  
Artur Matysik ◽  
Shruti Pavagadhi ◽  
...  

AbstractEnterococci 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.SignificanceBacterial 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.

mBio ◽  
2018 ◽  
Vol 9 (2) ◽  
Author(s):  
Damien Keogh ◽  
Ling Ning Lam ◽  
Lucinda E. Doyle ◽  
Artur Matysik ◽  
Shruti Pavagadhi ◽  
...  

ABSTRACT Enterococci are important human commensals and significant opportunistic pathogens. Biofilm-related enterococcal infections, such as endocarditis, urinary tract infections, wound and surgical site infections, and medical device-associated 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 to biofilm pathogenicity. Here, we report a form of iron-dependent metabolism for Enterococcus faecalis where, in the absence of heme, extracellular electron transfer (EET) and increased ATP production augment biofilm growth. We observe alterations in biofilm matrix depth and composition during iron-augmented biofilm growth. We show that the ldh gene encoding l -lactate dehydrogenase is required for iron-augmented energy production and biofilm formation and promotes EET. IMPORTANCE Bacterial metabolic versatility can often influence the outcome of host-pathogen interactions, yet causes 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 can immobilize iron, providing access to this growth-promoting resource which is otherwise inaccessible in the planktonic state. Our data show that in the absence of heme, Enterococcus faecalis l -lactate dehydrogenase promotes EET and uses matrix-associated iron to carry out EET. Therefore, the presence of iron within the biofilm matrix leads to enhanced biofilm growth.


mBio ◽  
2019 ◽  
Vol 10 (3) ◽  
Author(s):  
Damien Keogh ◽  
Ling Ning Lam ◽  
Lucinda E. Doyle ◽  
Artur Matysik ◽  
Shruti Pavagadhi ◽  
...  

2019 ◽  
Vol 9 (16) ◽  
pp. 1970055 ◽  
Author(s):  
Galina Pankratova ◽  
Dmitry Pankratov ◽  
Ross D. Milton ◽  
Shelley D. Minteer ◽  
Lo Gorton

2017 ◽  
Vol 2017 ◽  
pp. 1-10 ◽  
Author(s):  
Olga Mitrofanova ◽  
Ayslu Mardanova ◽  
Vladimir Evtugyn ◽  
Lydia Bogomolnaya ◽  
Margarita Sharipova

Serratia marcescensis an emerging opportunistic pathogen responsible for many hospital-acquired infections including catheter-associated bacteremia and urinary tract and respiratory tract infections. Biofilm formation is one of the mechanisms employed byS. marcescensto increase its virulence and pathogenicity. Here, we have investigated the main steps of the biofilm formation byS. marcescensSR 41-8000. It was found that the biofilm growth is stimulated by the nutrient-rich environment. The time-course experiments showed thatS. marcescenscells adhere to the surface of the catheter and start to produce extracellular polymeric substances (EPS) within the first 2 days of growth. After 7 days,S. marcescensbiofilms maturate and consist of bacterial cells embedded in a self-produced matrix of hydrated EPS. In this study, the effect ofBacillus pumilus3-19 proteolytic enzymes on the structure of 7-day-oldS. marcescensbiofilms was examined. Using quantitative methods and scanning electron microscopy for the detection of biofilm, we demonstrated a high efficacy of subtilisin-like protease and glutamyl endopeptidase in biofilm removal. Enzymatic treatment resulted in the degradation of the EPS components and significant eradication of the biofilms.


2020 ◽  
Vol 202 (7) ◽  
Author(s):  
Lars Hederstedt ◽  
Lo Gorton ◽  
Galina Pankratova

ABSTRACT Enterococcus faecalis cells are known to have ferric reductase activity and the ability to transfer electrons generated in metabolism to the external environment. We have isolated mutants defective in ferric reductase activity and studied their electron transfer properties to electrodes mediated by ferric ions and an osmium complex-modified redox polymer (OsRP). Electron transfer mediated with ferric ions and ferric reductase activity were both found to be dependent on the membrane-associated Ndh3 and EetA proteins, consistent with findings in Listeria monocytogenes. In contrast, electron transfer mediated with OsRP was independent of these two proteins. Quinone in the cell membrane was required for the electron transfer with both mediators. The combined results demonstrate that extracellular electron transfer from reduced quinone to ferric ions and to OsRP occurs via different routes in the cell envelope of E. faecalis. IMPORTANCE The transfer of reducing power in the form of electrons, generated in the catabolism of nutrients, from a bacterium to an extracellular acceptor appears to be common in nature. The electron acceptor can be another cell or abiotic material. Such extracellular electron transfer contributes to syntrophic metabolism and is of wide environmental, industrial, and medical importance. Electron transfer between microorganisms and electrodes is fundamental in microbial fuel cells for energy production and for electricity-driven synthesis of chemical compounds in cells. In contrast to the much-studied extracellular electron transfer mediated by cell surface exposed cytochromes, little is known about components and mechanisms for such electron transfer in organisms without these cytochromes and in Gram-positive bacteria such as E. faecalis, which is a commensal gut lactic acid bacterium and opportunistic pathogen.


2012 ◽  
Vol 40 (6) ◽  
pp. 1261-1267 ◽  
Author(s):  
Liang Shi ◽  
Kevin M. Rosso ◽  
John M. Zachara ◽  
James K. Fredrickson

Originally discovered in the dissimilatory metal-reducing bacterium Shewanella oneidensis MR-1 (MR-1), key components of the Mtr (i.e. metal-reducing) pathway exist in all strains of metal-reducing Shewanella characterized. The protein components identified to date for the Mtr pathway of MR-1 include four multihaem c-Cyts (c-type cytochromes), CymA, MtrA, MtrC and OmcA, and a porin-like outer membrane protein MtrB. They are strategically positioned along the width of the MR-1 cell envelope to mediate electron transfer from the quinone/quinol pool in the inner membrane to Fe(III)-containing minerals external to the bacterial cells. A survey of microbial genomes has identified homologues of the Mtr pathway in other dissimilatory Fe(III)-reducing bacteria, including Aeromonas hydrophila, Ferrimonas balearica and Rhodoferax ferrireducens, and in the Fe(II)-oxidizing bacteria Dechloromonas aromatica RCB, Gallionella capsiferriformans ES-2 and Sideroxydans lithotrophicus ES-1. The apparent widespread distribution of Mtr pathways in both Fe(III)-reducing and Fe(II)-oxidizing bacteria suggests a bidirectional electron transfer role, and emphasizes the importance of this type of extracellular electron-transfer pathway in microbial redox transformation of iron. The organizational and electron-transfer characteristics of the Mtr pathways may be shared by other pathways used by micro-organisms for exchanging electrons with their extracellular environments.


2019 ◽  
Author(s):  
Ling Ning Lam ◽  
Jun Jie Wong ◽  
Artur Matysik ◽  
Jason J. Paxman ◽  
Kelvin Kian Long Chong ◽  
...  

AbstractEnterococcus faecalisis 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. TheE. faecalissortase-assembled endocarditis and biofilm associated pilus (Ebp) is involved in adhesion and biofilm formationin vitroandin vivo. Extracellular electron transfer (EET) also promotesE. faecalisbiofilm 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 augmentedE. faecalisGI 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 inE. faecalis, and that these processes plays an important role inE. faecalisexpansion in the GI tract.SignificanceUnderstanding 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 forEnterococcus faecalisendocarditis 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 theE. faecalisbiofilm. Our findings support a model in whichE. faecalisuse EET to drive the reduction of pilus-associated ferric iron, leading to iron acquisition inE. faecalisbiofilm, and contributing to enterococcal virulence in the GI tract.


2021 ◽  
Vol 2 (1) ◽  
Author(s):  
Ziyu Li ◽  
Weiwei Chang ◽  
Tianyu Cui ◽  
Dake Xu ◽  
Dawei Zhang ◽  
...  

AbstractMicrobiologically influenced corrosion of metals is prevalent in both natural and industrial environments, causing enormous structural damage and economic loss. Exactly how microbes influence corrosion remains controversial. Here, we show that the pitting corrosion of stainless steel is accelerated in the presence of Shewanella oneidensis MR-1 biofilm by extracellular electron transfer between the bacterial cells and the steel electrode, mediated by a riboflavin electron shuttle. From pitting measurements, X-ray photoelectron spectroscopy and Mott-Schottky analyses, the addition of an increased amount of riboflavin is found to induce a more defective passive film on the stainless steel. Electrochemical impedance spectroscopy reveals that enhanced bioanodic and biocathodic process can both promote the corrosion of the stainless steel. Using in situ scanning electrochemical microscopy, we observe that extracellular electron transfer between the bacterium and the stainless steel is bidirectional in nature and switchable depending on the passive or active state of the steel surface.


2014 ◽  
Vol 60 (11) ◽  
pp. 753-759 ◽  
Author(s):  
Enren Zhang ◽  
Yamin Cai ◽  
Yue Luo ◽  
Zhe Piao

Great attention has been focused on Gram-negative bacteria in the application of microbial fuel cells. In this study, the Gram-positive bacterium Enterococcus faecalis was employed in microbial fuel cells. Bacterial biofilms formed by E. faecalis ZER6 were investigated with respect to electricity production through the riboflavin-shuttled extracellular electron transfer. Trace riboflavin was shown to be essential for transferring electrons derived from the oxidation of glucose outside the peptidoglycan layer in the cell wall of E. faecalis biofilms formed on the surface of electrodes, in the absence of other potential electron mediators (e.g., yeast extract).


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