Extracellular electron transfer features of Gram-positive bacteria

ABSTRACT Exoelectrogens are able to transfer electrons extracellularly, enabling them to respire on insoluble terminal electron acceptors. Extensively studied exoelectrogens, such as Geobacter sulfurreducens and Shewanella oneidensis, are Gram negative. More recently, it has been reported that Gram-positive bacteria, such as Listeria monocytogenes and Enterococcus faecalis, also exhibit the ability to transfer electrons extracellularly, although it is still unclear whether this has a function in respiration or in redox control of the environment, for instance, by reducing ferric iron for iron uptake. In this issue of Journal of Bacteriology, Hederstedt and colleagues report on experiments that directly compare extracellular electron transfer (EET) pathways for ferric iron reduction and respiration and find a clear difference (L. Hederstedt, L. Gorton, and G. Pankratova, J Bacteriol 202:e00725-19, 2020, https://doi.org/10.1128/JB.00725-19), providing further insights and new questions into the function and metabolic pathways of EET in Gram-positive bacteria.

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Faculty Opinions recommendation of A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.734001876.793550856 ◽

2018 ◽

Author(s):

Angelika Gründling

Keyword(s):

Electron Transfer ◽

Transfer Mechanism ◽

Extracellular Electron Transfer ◽

Gram Positive ◽

Electron Transfer Mechanism ◽

Gram Positive Bacteria

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1915678116 ◽

2019 ◽

Vol 116 (52) ◽

pp. 26892-26899 ◽

Cited By ~ 10

Author(s):

Samuel H. Light ◽

Raphaël Méheust ◽

Jessica L. Ferrell ◽

Jooyoung Cho ◽

David Deng ◽

...

Keyword(s):

Electron Transfer ◽

Phylogenetic Analyses ◽

Foodborne Pathogen ◽

Extracellular Electron Transfer ◽

Transfer System ◽

Gram Positive ◽

Gram Positive Bacteria ◽

Electron Transfer System ◽

Transport Chain ◽

Insoluble Electron Acceptors

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 pathogenListeria 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 supportL. monocytogenesgrowth. We demonstrate that this represents a generalizable mechanism by finding that aL. monocytogenesstrain 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.

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Novel Extracellular Electron Transfer Channels in a Gram-Positive Thermophilic Bacterium

Frontiers in Microbiology ◽

10.3389/fmicb.2020.597818 ◽

2021 ◽

Vol 11 ◽

Author(s):

Sergey N. Gavrilov ◽

Daria G. Zavarzina ◽

Ivan M. Elizarov ◽

Tamara V. Tikhonova ◽

Natalia I. Dergousova ◽

...

Keyword(s):

Electron Transfer ◽

Thermophilic Bacterium ◽

Hyperthermophilic Archaea ◽

Extracellular Electron Transfer ◽

Gram Positive ◽

Thermal Environments ◽

Gram Positive Bacteria ◽

Microscopic Studies ◽

First Time ◽

Transfer Channels

Biogenic transformation of Fe minerals, associated with extracellular electron transfer (EET), allows microorganisms to exploit high-potential refractory electron acceptors for energy generation. EET-capable thermophiles are dominated by hyperthermophilic archaea and Gram-positive bacteria. Information on their EET pathways is sparse. Here, we describe EET channels in the thermophilic Gram-positive bacterium Carboxydothermus ferrireducens that drive exoelectrogenesis and rapid conversion of amorphous mineral ferrihydrite to large magnetite crystals. Microscopic studies indicated biocontrolled formation of unusual formicary-like ultrastructure of the magnetite crystals and revealed active colonization of anodes in bioelectrochemical systems (BESs) by C. ferrireducens. The internal structure of micron-scale biogenic magnetite crystals is reported for the first time. Genome analysis and expression profiling revealed three constitutive c-type multiheme cytochromes involved in electron exchange with ferrihydrite or an anode, sharing insignificant homology with previously described EET-related cytochromes thus representing novel determinants of EET. Our studies identify these cytochromes as extracellular and reveal potentially novel mechanisms of cell-to-mineral interactions in thermal environments.

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Long-distance electron transfer in a filamentous Gram-positive bacterium

Nature Communications ◽

10.1038/s41467-021-21709-z ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Yonggang Yang ◽

Zegao Wang ◽

Cuifen Gan ◽

Lasse Hyldgaard Klausen ◽

Robin Bonné ◽

...

Keyword(s):

Electron Transfer ◽

Microbial Fuel Cells ◽

Extracellular Electron Transfer ◽

Gram Negative Bacteria ◽

Positive Bacterium ◽

Long Distance ◽

Gram Positive ◽

Gram Negative ◽

Force Microscopy ◽

Cell Envelopes

AbstractLong-distance extracellular electron transfer has been observed in Gram-negative bacteria and plays roles in both natural and engineering processes. The electron transfer can be mediated by conductive protein appendages (in short unicellular bacteria such as Geobacter species) or by conductive cell envelopes (in filamentous multicellular cable bacteria). Here we show that Lysinibacillus varians GY32, a filamentous unicellular Gram-positive bacterium, is capable of bidirectional extracellular electron transfer. In microbial fuel cells, L. varians can form centimetre-range conductive cellular networks and, when grown on graphite electrodes, the cells can reach a remarkable length of 1.08 mm. Atomic force microscopy and microelectrode analyses suggest that the conductivity is linked to pili-like protein appendages. Our results show that long-distance electron transfer is not limited to Gram-negative bacteria.

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Extracellular Electron Transfer Mediated by Flavins in Gram-positive Bacillus sp. WS-XY1 and Yeast Pichia stipitis

Electrochimica Acta ◽

10.1016/j.electacta.2014.09.096 ◽

2014 ◽

Vol 146 ◽

pp. 564-567 ◽

Cited By ~ 47

Author(s):

Song Wu ◽

Yong Xiao ◽

Lu Wang ◽

Yue Zheng ◽

Kenlin Chang ◽

...

Keyword(s):

Electron Transfer ◽

Pichia Stipitis ◽

Extracellular Electron Transfer ◽

Bacillus Sp ◽

Gram Positive

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How thermophilic Gram-positive organisms perform extracellular electron transfer: characterization of the cell surface terminal reductase OcwA

10.1101/641308 ◽

2019 ◽

Author(s):

N.L. Costa ◽

B. Hermann ◽

V. Fourmond ◽

M. Faustino ◽

M. Teixeira ◽

...

Keyword(s):

Electron Transfer ◽

Cell Surface ◽

Electron Acceptors ◽

Added Value ◽

Extracellular Electron Transfer ◽

Bioelectrochemical Systems ◽

Positive Bacterium ◽

Gram Positive ◽

Evolutionary Pathway ◽

Structural And Functional Properties

AbstractExtracellular 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 2.2Å resolution shows that the overall-fold and organization of the hemes are not related to other metal reductases and instead are similar to that 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 take the role of a respiratory ‘swiss-army knife’ allowing this organism to grow in environments with rapidly changing availability of terminal electron acceptors without the need for transcriptional regulation and protein synthesis.ImportanceThermophilic 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 of the cell). In this manuscript 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 is unrelated with terminal reductases found at the cell surface of other electroactive organisms. Instead, OcwA is similar to terminal reductases of soluble electron acceptors. Our data reveals that terminal oxidoreductases of soluble and insoluble substrates are evolutionarily related, providing novel insights into the evolutionary pathway of multiheme cytochromes.

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