Dataset Information

Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria.

ABSTRACT: Mineral-respiring bacteria use a process called extracellular electron transfer to route their respiratory electron transport chain to insoluble electron acceptors on the exterior of the cell. We recently characterized a flavin-based extracellular electron transfer system that is present in the foodborne pathogen Listeria monocytogenes, as well as many other Gram-positive bacteria, and which highlights a more generalized role for extracellular electron transfer in microbial metabolism. Here we identify a family of putative extracellular reductases that possess a conserved posttranslational flavinylation modification. Phylogenetic analyses suggest that divergent flavinylated extracellular reductase subfamilies possess distinct and often unidentified substrate specificities. We show that flavinylation of a member of the fumarate reductase subfamily allows this enzyme to receive electrons from the extracellular electron transfer system and support L. monocytogenes growth. We demonstrate that this represents a generalizable mechanism by finding that a L. monocytogenes strain engineered to express a flavinylated extracellular urocanate reductase uses urocanate by a related mechanism and to a similar effect. These studies thus identify an enzyme family that exploits a modular flavin-based electron transfer strategy to reduce distinct extracellular substrates and support a multifunctional view of the role of extracellular electron transfer activities in microbial physiology.

SUBMITTER: Light SH

PROVIDER: S-EPMC6936397 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria.

Light Samuel H SH Méheust Raphaël R Ferrell Jessica L JL Cho Jooyoung J Deng David D Agostoni Marco M Iavarone Anthony T AT Banfield Jillian F JF D'Orazio Sarah E F SEF Portnoy Daniel A DA

Proceedings of the National Academy of Sciences of the United States of America 20191209 52

Mineral-respiring bacteria use a process called extracellular electron transfer to route their respiratory electron transport chain to insoluble electron acceptors on the exterior of the cell. We recently characterized a flavin-based extracellular electron transfer system that is present in the foodborne pathogen <i>Listeria monocytogenes</i>, as well as many other Gram-positive bacteria, and which highlights a more generalized role for extracellular electron transfer in microbial metabolism. He ...[more]

PMID: 31818955

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Project description:Extracellular electron transfer is the key process underpinning the development of bioelectrochemical systems for the production of energy or added-value compounds. Thermincola potens JR is a promising Gram-positive bacterium to be used in these systems because it is thermophilic. In this paper, we describe the structural and functional properties of the nonaheme cytochrome OcwA, which is the terminal reductase of this organism. The structure of OcwA, determined at 2.2-Å resolution, shows that the overall fold and organization of the hemes are not related to other metal reductases and instead are similar to those of multiheme cytochromes involved in the biogeochemical cycles of nitrogen and sulfur. We show that, in addition to solid electron acceptors, OcwA can also reduce soluble electron shuttles and oxyanions. These data reveal that OcwA can work as a multipurpose respiratory enzyme allowing this organism to grow in environments with rapidly changing availability of terminal electron acceptors without the need for transcriptional regulation and protein synthesis.IMPORTANCE Thermophilic Gram-positive organisms were recently shown to be a promising class of organisms to be used in bioelectrochemical systems for the production of electrical energy. These organisms present a thick peptidoglycan layer that was thought to preclude them to perform extracellular electron transfer (i.e., exchange catabolic electrons with solid electron acceptors outside the cell). In this paper, we describe the structure and functional mechanisms of the multiheme cytochrome OcwA, the terminal reductase of the Gram-positive bacterium Thermincola potens JR found at the cell surface of this organism. The results presented here show that this protein can take the role of a respiratory "Swiss Army knife," allowing this organism to grow in environments with soluble and insoluble substrates. Moreover, it is shown that it is unrelated to terminal reductases found at the cell surface of other electroactive organisms. Instead, OcwA is similar to terminal reductases of soluble electron acceptors. Our data reveal that terminal oxidoreductases of soluble and insoluble substrates are evolutionarily related, providing novel insights into the evolutionary pathway of multiheme cytochromes.

Project description:To exchange electrons with extracellular substrates, some microorganisms employ extracellular electron transfer (EET) pathways that physically connect extracellular redox reactions to intracellular metabolic activity. These pathways are made of redox and structural proteins that work cooperatively to transfer electrons between extracellular substrates and the cytoplasmic membrane. Crucial to the bacterial and archaeal EET pathways are the quinol oxidases and/or quinone reductases in the cytoplasmic membrane where they recycle the quinone/quinol pool in the cytoplasmic membrane during EET reaction. Up to date, three different families of quinol oxidases and/or quinone reductases involved in bacterial EET have been discovered. They are the CymA, CbcL/MtrH/MtoC, and ImcH families of quinol oxidases and/or quinone reductases that are all multiheme c-type cytochromes (c-Cyts). To investigate to what extent they are distributed among microorganisms, we search the bacterial as well as archaeal genomes for the homologs of these c-Cyts. Search results reveal that the homologs of these c-Cyts are only found in the Domain Bacteria. Moreover, the CymA homologs are only found in the phylum of Proteobacteria and most of them are in the Shewanella genus. In addition to Shewanella sp., CymA homologs are also found in other Fe(III)-reducing bacteria, such as of Vibrio parahaemolyticus. In contrast to CymA, CbcL/MtrH/MtoC, and ImcH homologs are much more widespread. CbcL/MtrH/MtoC homologs are found in 15 phyla, while ImcH homologs are found in 12 phyla. Furthermore, the heme-binding motifs of CbcL/MtrH/MtoC and ImcH homologs vary greatly, ranging from 3 to 23 and 6 to 10 heme-binding motifs for CbcL/MtrH/MtoC and ImcH homologs, respectively. Moreover, CymA and CbcL/MtrH/MtoC homologs are found in both Fe(III)-reducing and Fe(II)-oxidizing bacteria, suggesting that these families of c-Cyts catalyze both quinol-oxidizing and quinone-reducing reactions. ImcH homologs are only found in the Fe(III)-reducing bacteria, implying that they are only the quinol oxidases. Finally, some bacteria have the homologs of two different families of c-Cyts, which may improve the bacterial capability to exchange electrons with extracellular substrates.

Dataset Information

Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria.

Publications

Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria.

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