Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>

ABSTRACT Ethanolamine (EA) is a valuable microbial carbon and nitrogen source derived from cell membranes. EA catabolism is suggested to occur in a cellular metabolic subsystem called a bacterial microcompartment (BMC), and the activation of EA utilization (eut) genes is linked to bacterial pathogen...

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Autores principales:	Zhe Zeng, Sjef Boeren, Varaang Bhandula, Samuel H. Light, Eddy J. Smid, Richard A. Notebaart, Tjakko Abee
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Listeria monocytogenes anaerobic catabolic pathways electron transport microcompartment Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/636051427c4c4d528bd90fc9e7874054
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spelling	oai:doaj.org-article:636051427c4c4d528bd90fc9e78740542021-12-02T19:22:27ZBacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>10.1128/mSystems.01349-202379-5077https://doaj.org/article/636051427c4c4d528bd90fc9e78740542021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01349-20https://doaj.org/toc/2379-5077ABSTRACT Ethanolamine (EA) is a valuable microbial carbon and nitrogen source derived from cell membranes. EA catabolism is suggested to occur in a cellular metabolic subsystem called a bacterial microcompartment (BMC), and the activation of EA utilization (eut) genes is linked to bacterial pathogenesis. Despite reports showing that the activation of eut is regulated by a vitamin B12-binding riboswitch and that upregulation of eut genes occurs in mice, it remains unknown whether EA catabolism is BMC dependent in Listeria monocytogenes. Here, we provide evidence for BMC-dependent anaerobic EA utilization via metabolic analysis, proteomics, and electron microscopy. First, we show vitamin B12-induced activation of the eut operon in L. monocytogenes coupled to the utilization of EA, thereby enabling growth. Next, we demonstrate BMC formation connected with EA catabolism with the production of acetate and ethanol in a molar ratio of 2:1. Flux via the ATP-generating acetate branch causes an apparent redox imbalance due to the reduced regeneration of NAD+ in the ethanol branch resulting in a surplus of NADH. We hypothesize that the redox imbalance is compensated by linking eut BMCs to anaerobic flavin-based extracellular electron transfer (EET). Using L. monocytogenes wild-type, BMC mutant, and EET mutant strains, we demonstrate an interaction between BMCs and EET and provide evidence for a role of Fe3+ as an electron acceptor. Taken together, our results suggest an important role of BMC-dependent EA catabolism in L. monocytogenes growth in anaerobic environments like the human gastrointestinal tract, with a crucial role for the flavin-based EET system in redox balancing. IMPORTANCE Listeria monocytogenes is a foodborne pathogen causing severe illness, and as such, it is crucial to understand the molecular mechanisms contributing to pathogenicity. One carbon source that allows L. monocytogenes to grow in humans is ethanolamine (EA), which is derived from phospholipids present in eukaryotic cell membranes. It is hypothesized that EA utilization occurs in bacterial microcompartments (BMCs), self-assembling subcellular proteinaceous structures and analogs of eukaryotic organelles. Here, we demonstrate that BMC-driven utilization of EA in L. monocytogenes results in increased energy production essential for anaerobic growth. However, exploiting BMCs and the encapsulated metabolic pathways also requires the balancing of oxidative and reductive pathways. We now provide evidence that L. monocytogenes copes with this by linking BMC activity to flavin-based extracellular electron transfer (EET) using iron as an electron acceptor. Our results shed new light on an important molecular mechanism that enables L. monocytogenes to grow using host-derived phospholipid degradation products.Zhe ZengSjef BoerenVaraang BhandulaSamuel H. LightEddy J. SmidRichard A. NotebaartTjakko AbeeAmerican Society for MicrobiologyarticleListeria monocytogenesanaerobic catabolic pathwayselectron transportmicrocompartmentMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Listeria monocytogenes anaerobic catabolic pathways electron transport microcompartment Microbiology QR1-502
spellingShingle	Listeria monocytogenes anaerobic catabolic pathways electron transport microcompartment Microbiology QR1-502 Zhe Zeng Sjef Boeren Varaang Bhandula Samuel H. Light Eddy J. Smid Richard A. Notebaart Tjakko Abee Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>
description	ABSTRACT Ethanolamine (EA) is a valuable microbial carbon and nitrogen source derived from cell membranes. EA catabolism is suggested to occur in a cellular metabolic subsystem called a bacterial microcompartment (BMC), and the activation of EA utilization (eut) genes is linked to bacterial pathogenesis. Despite reports showing that the activation of eut is regulated by a vitamin B12-binding riboswitch and that upregulation of eut genes occurs in mice, it remains unknown whether EA catabolism is BMC dependent in Listeria monocytogenes. Here, we provide evidence for BMC-dependent anaerobic EA utilization via metabolic analysis, proteomics, and electron microscopy. First, we show vitamin B12-induced activation of the eut operon in L. monocytogenes coupled to the utilization of EA, thereby enabling growth. Next, we demonstrate BMC formation connected with EA catabolism with the production of acetate and ethanol in a molar ratio of 2:1. Flux via the ATP-generating acetate branch causes an apparent redox imbalance due to the reduced regeneration of NAD+ in the ethanol branch resulting in a surplus of NADH. We hypothesize that the redox imbalance is compensated by linking eut BMCs to anaerobic flavin-based extracellular electron transfer (EET). Using L. monocytogenes wild-type, BMC mutant, and EET mutant strains, we demonstrate an interaction between BMCs and EET and provide evidence for a role of Fe3+ as an electron acceptor. Taken together, our results suggest an important role of BMC-dependent EA catabolism in L. monocytogenes growth in anaerobic environments like the human gastrointestinal tract, with a crucial role for the flavin-based EET system in redox balancing. IMPORTANCE Listeria monocytogenes is a foodborne pathogen causing severe illness, and as such, it is crucial to understand the molecular mechanisms contributing to pathogenicity. One carbon source that allows L. monocytogenes to grow in humans is ethanolamine (EA), which is derived from phospholipids present in eukaryotic cell membranes. It is hypothesized that EA utilization occurs in bacterial microcompartments (BMCs), self-assembling subcellular proteinaceous structures and analogs of eukaryotic organelles. Here, we demonstrate that BMC-driven utilization of EA in L. monocytogenes results in increased energy production essential for anaerobic growth. However, exploiting BMCs and the encapsulated metabolic pathways also requires the balancing of oxidative and reductive pathways. We now provide evidence that L. monocytogenes copes with this by linking BMC activity to flavin-based extracellular electron transfer (EET) using iron as an electron acceptor. Our results shed new light on an important molecular mechanism that enables L. monocytogenes to grow using host-derived phospholipid degradation products.
format	article
author	Zhe Zeng Sjef Boeren Varaang Bhandula Samuel H. Light Eddy J. Smid Richard A. Notebaart Tjakko Abee
author_facet	Zhe Zeng Sjef Boeren Varaang Bhandula Samuel H. Light Eddy J. Smid Richard A. Notebaart Tjakko Abee
author_sort	Zhe Zeng
title	Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>
title_short	Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>
title_full	Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>
title_fullStr	Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>
title_full_unstemmed	Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>
title_sort	bacterial microcompartments coupled with extracellular electron transfer drive the anaerobic utilization of ethanolamine in <named-content content-type="genus-species">listeria monocytogenes</named-content>
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/636051427c4c4d528bd90fc9e7874054
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Bacterial Microcompartments Coupled with Extracellular Electron Transfer Drive the Anaerobic Utilization of Ethanolamine in <named-content content-type="genus-species">Listeria monocytogenes</named-content>

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