Multi-heme cytochrome-mediated extracellular electron transfer by the anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’

Zhang, Xueqin; Joyce, Georgina H.; Leu, Andy O.; Zhao, Jing; Rabiee, Hesamoddin; Virdis, Bernardino; Tyson, Gene W.; Yuan, Zhiguo; McIlroy, Simon J.; Hu, Shihu

doi:10.1038/s41467-023-41847-w

Cited by 20 publications

(8 citation statements)

References 93 publications

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“…Surprisingly, varying the potential from 0 to 600 mV vs. SHE did not influence the EET mechanism of ‘ Ca . Methanoperedens’, in contrast to what was suggested by Zhang et al 38 . One reason for this could be the sub-optimal growth of ‘ Ca .…”

Section: Discussionmentioning

confidence: 71%

“…Although EET by ‘ Ca . Methanoperedens’ has been studied both in bioelectrochemical systems 36 , 38 , 42 – 45 and in relation to extracellular electron acceptors 17 , 23 , in most studies the EET mechanism has not further been unravelled. Three exceptions are studies focusing on the use of ferrihydrite 20 , birnessite 24 and a poised electrode at +400 mV by ‘ Ca .…”

Section: Discussionmentioning

confidence: 99%

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Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea

Ouboter,

Mesman,

Sleutels

et al. 2024

Nat Commun

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Anaerobic methanotrophic (ANME) archaea are environmentally important, uncultivated microorganisms that oxidize the potent greenhouse gas methane. During methane oxidation, ANME archaea engage in extracellular electron transfer (EET) with other microbes, metal oxides, and electrodes through unclear mechanisms. Here, we cultivate ANME-2d archaea (‘Ca. Methanoperedens’) in bioelectrochemical systems and observe strong methane-dependent current (91–93% of total current) associated with high enrichment of ‘Ca. Methanoperedens’ on the anode (up to 82% of the community), as determined by metagenomics and transmission electron microscopy. Electrochemical and metatranscriptomic analyses suggest that the EET mechanism is similar at various electrode potentials, with the possible involvement of an uncharacterized short-range electron transport protein complex and OmcZ nanowires.

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Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea

Ouboter,

Mesman,

Sleutels

et al. 2024

Nat Commun

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“…Importantly, the reduction of Fe(III) and IO 3 – by MR-1 WT and Δ mtrCAB significantly decreased in the presence of 2.5 mM Fe(III)-citrate, as compared to these cultures with a sole electron acceptor (Figure S2). This difference may result from the competition between MtrCAB or electron shunting for microbial IO 3 – and Fe(III) reduction or other unknown regulatory controls over IO 3 – and Fe(III) reduction in the presence of these two different electron acceptors . Transcriptomic analysis helps reveal the molecular mechanism underlying the differences observed in cultures with sole and dual electron acceptors.…”

Section: Resultsmentioning

confidence: 99%

“…− and Fe(III) reduction in the presence of these two different electron acceptors. 38 Transcriptomic analysis helps reveal the molecular mechanism underlying the differences observed in cultures with sole and dual electron acceptors − reduced by all of these strains were stoichiometrically balanced with the amount of I − generated at 19-day after reduction (Figure 3C).…”

Section: Bacterial Iomentioning

confidence: 99%

Abiotic and Biotic Reduction of Iodate Driven by Shewanella oneidensis MR-1

Jiang,

Cui,

Qian

et al. 2023

Environ. Sci. Technol.

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Iodate (IO3 –) can be abiotically reduced by Fe(II) or biotically reduced by the dissimilatory Fe(III)-reducing bacterium Shewanella oneidensis (MR-1) via its DmsEFAB and MtrCAB. However, the intermediates and stoichiometry between the Fe(II) and IO3 – reaction and the relative contribution of abiotic and biotic IO3 – reduction by biogenic Fe(II) and MR-1 in the presence of Fe(III) remain unclear. In this study, we found that abiotic reduction of IO3 – by Fe(II) produced intermediates HIO and I– at a ratio of 1:2, followed by HIO disproportionation to I– and IO3 –. Comparative analyses of IO3 – reduction by MR-1 wild type (WT), MR-1 mutants deficient in DmsEFAB or MtrCAB, and Shewanella sp. ANA-3 in the presence of Fe(III)-citrate, Fe(III) oxides, or clay minerals showed that abiotic IO3 – reduction by biogenic Fe(II) predominated under iron-rich conditions, while biotic IO3 – reduction by DmsEFAB played a more dominant role under iron-poor conditions. Compared to that in the presence of Fe(III)-citrate, MR-1 WT reduced more IO3 – in the presence of Fe(III) oxides and clay minerals. The observed abiotic and biotic IO3 – reduction by MR-1 under Fe-rich and Fe-limited conditions suggests that Fe(III)-reducing bacteria could contribute to the transformation of iodine species and I– enrichment in natural iodine-rich environments.

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“… , Shewanella features both the cytochrome-based and mediator (flavin)-based long-range extracellular electron transfer (EET) pathways . In contrast, the current understanding of the EET pathways of ANME Methanoperedenaceae is limited to the cytochrome-based mode . The potential EET discrepancy could lead to different catalytic mechanisms of PCs in facilitating iron oxide reduction by ANME Methanoperedenaceae in comparison to Shewanella , which warrants addressing.…”

Section: Introductionmentioning

confidence: 99%

Pyrogenic Carbon Promotes Anaerobic Oxidation of Methane Coupled with Iron Reduction via the Redox-Cycling Mechanism

Zhang,

Xie,

Cai

et al. 2023

Environ. Sci. Technol.

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Pyrogenic carbon (PC) can mediate electron transfer and thus catalyze biogeochemical processes to impact greenhouse gas (GHG) emissions. Here, we demonstrate that PC can contribute to mitigating GHG emissions by promoting the Fe(III)-dependent anaerobic oxidation of methane (AOM). It was found that the amendment PCs in microcosms dominated by Methanoperedenaceae performing Fe(III)-dependent AOM simultaneously promoted the rate of AOM and Fe(III) reduction with a consistent ratio close to the theoretical stoichiometry of 1:8. Further correlation analysis showed that the AOM rate was linearly correlated with the electron exchange capacity, but not the conductivity, of added PC materials, indicating the redox-cycling electron transfer mechanism to promote the Fe(III)-dependent AOM. The mass content of the C�O moiety from differentially treated PCs was well correlated with the AOM rate, suggesting that surface redox-active quinone groups on PCs contribute to facilitating Fe(III)dependent AOM. Further microbial analyses indicate that PC likely shuttles direct electron transfer from Methanoperedenaceae to Fe(III) reduction. This study provides new insight into the climate-cooling impact of PCs, and our evaluation indicates that the PC-facilitated Fe(III)-dependent AOM could have a significant contribution to suppressing methane emissions from the world's reservoirs.

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Multi-heme cytochrome-mediated extracellular electron transfer by the anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’

Cited by 20 publications

References 93 publications

Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea

Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea

Abiotic and Biotic Reduction of Iodate Driven by Shewanella oneidensis MR-1

Pyrogenic Carbon Promotes Anaerobic Oxidation of Methane Coupled with Iron Reduction via the Redox-Cycling Mechanism

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