Extracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism

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...

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Autores principales: Damien Keogh, Ling Ning Lam, Lucinda E. Doyle, Artur Matysik, Shruti Pavagadhi, Shivshankar Umashankar, Pui Man Low, Jennifer L. Dale, Yiyang Song, Sean Pin Ng, Chris B. Boothroyd, Gary M. Dunny, Sanjay Swarup, Rohan B. H. Williams, Enrico Marsili, Kimberly A. Kline
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Publicado: American Society for Microbiology 2018
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Acceso en línea:https://doaj.org/article/99197a56cd094425a199d1639eb5b6d4
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spelling oai:doaj.org-article:99197a56cd094425a199d1639eb5b6d42021-11-15T15:53:27ZExtracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism10.1128/mBio.00626-172150-7511https://doaj.org/article/99197a56cd094425a199d1639eb5b6d42018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00626-17https://doaj.org/toc/2150-7511ABSTRACT 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.Damien KeoghLing Ning LamLucinda E. DoyleArtur MatysikShruti PavagadhiShivshankar UmashankarPui Man LowJennifer L. DaleYiyang SongSean Pin NgChris B. BoothroydGary M. DunnySanjay SwarupRohan B. H. WilliamsEnrico MarsiliKimberly A. KlineAmerican Society for MicrobiologyarticleEnterococcus faecalisbiofilmextracellular electron transferironmetabolismMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution DOAJ
collection DOAJ
language EN
topic Enterococcus faecalis
biofilm
extracellular electron transfer
iron
metabolism
Microbiology
QR1-502
spellingShingle Enterococcus faecalis
biofilm
extracellular electron transfer
iron
metabolism
Microbiology
QR1-502
Damien Keogh
Ling Ning Lam
Lucinda E. Doyle
Artur Matysik
Shruti Pavagadhi
Shivshankar Umashankar
Pui Man Low
Jennifer L. Dale
Yiyang Song
Sean Pin Ng
Chris B. Boothroyd
Gary M. Dunny
Sanjay Swarup
Rohan B. H. Williams
Enrico Marsili
Kimberly A. Kline
Extracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism
description 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.
format article
author Damien Keogh
Ling Ning Lam
Lucinda E. Doyle
Artur Matysik
Shruti Pavagadhi
Shivshankar Umashankar
Pui Man Low
Jennifer L. Dale
Yiyang Song
Sean Pin Ng
Chris B. Boothroyd
Gary M. Dunny
Sanjay Swarup
Rohan B. H. Williams
Enrico Marsili
Kimberly A. Kline
author_facet Damien Keogh
Ling Ning Lam
Lucinda E. Doyle
Artur Matysik
Shruti Pavagadhi
Shivshankar Umashankar
Pui Man Low
Jennifer L. Dale
Yiyang Song
Sean Pin Ng
Chris B. Boothroyd
Gary M. Dunny
Sanjay Swarup
Rohan B. H. Williams
Enrico Marsili
Kimberly A. Kline
author_sort Damien Keogh
title Extracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism
title_short Extracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism
title_full Extracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism
title_fullStr Extracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism
title_full_unstemmed Extracellular Electron Transfer Powers <named-content content-type="genus-species">Enterococcus faecalis</named-content> Biofilm Metabolism
title_sort extracellular electron transfer powers <named-content content-type="genus-species">enterococcus faecalis</named-content> biofilm metabolism
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/99197a56cd094425a199d1639eb5b6d4
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