Multi-heme Cytochrome-mediated Extracellular Electron Transfer by the Anaerobic Methanotroph 'Candidatus Methanoperedens Nitroreducens'

Overview

Journal Nat Commun

Specialty Biology

Date 2023 Sep 30

PMID 37777538

Authors

Xueqin Zhang

Georgina H Joyce

Andy O Leu

Jing Zhao

Hesamoddin Rabiee

Bernardino Virdis

Gene W Tyson

Zhiguo Yuan

Simon J McIlroy

Shihu Hu

Affiliations

Soon will be listed here.

Abstract

Anaerobic methanotrophic archaea (ANME) carry out anaerobic oxidation of methane, thus playing a crucial role in the methane cycle. Previous genomic evidence indicates that multi-heme c-type cytochromes (MHCs) may facilitate the extracellular electron transfer (EET) from ANME to different electron sinks. Here, we provide experimental evidence supporting cytochrome-mediated EET for the reduction of metals and electrodes by 'Candidatus Methanoperedens nitroreducens', an ANME acclimated to nitrate reduction. Ferrous iron-targeted fluorescent assays, metatranscriptomics, and single-cell imaging suggest that 'Ca. M. nitroreducens' uses surface-localized redox-active cytochromes for metal reduction. Electrochemical and Raman spectroscopic analyses also support the involvement of c-type cytochrome-mediated EET for electrode reduction. Furthermore, several genes encoding menaquinone cytochrome type-c oxidoreductases and extracellular MHCs are differentially expressed when different electron acceptors are used.

Citing Articles

Back flux during anaerobic oxidation of butane support archaea-mediated alkanogenesis.

Chen S, Chen S, Musat N, Kummel S, Ji J, Lund M Nat Commun. 2024; 15(1):9628.

PMID: 39511174 PMC: 11543930. DOI: 10.1038/s41467-024-53932-9.

Microbial magnetite oxidation via MtoAB porin-multiheme cytochrome complex in ES-1.

Keffer J, Zhou N, Rushworth D, Yu Y, Chan C bioRxiv. 2024; .

PMID: 39345469 PMC: 11429942. DOI: 10.1101/2024.09.20.614158.

Diversity, Methane Oxidation Activity, and Metabolic Potential of Microbial Communities in Terrestrial Mud Volcanos of the Taman Peninsula.

Slobodkin A, Rusanov I, Slobodkina G, Stroeva A, Chernyh N, Pimenov N Microorganisms. 2024; 12(7).

PMID: 39065117 PMC: 11279179. DOI: 10.3390/microorganisms12071349.

Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea.

Ouboter H, Mesman R, Sleutels T, Postma J, Wissink M, Jetten M Nat Commun. 2024; 15(1):1477.

PMID: 38368447 PMC: 10874420. DOI: 10.1038/s41467-024-45758-2.

References

Bjerg J, Boschker H, Larsen S, Berry D, Schmid M, Millo D . Long-distance electron transport in individual, living cable bacteria. Proc Natl Acad Sci U S A. 2018; 115(22):5786-5791. PMC: 5984516. DOI: 10.1073/pnas.1800367115. View

Nurk S, Meleshko D, Korobeynikov A, Pevzner P . metaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017; 27(5):824-834. PMC: 5411777. DOI: 10.1101/gr.213959.116. View

Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M, Goto S . KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics. 2019; 36(7):2251-2252. PMC: 7141845. DOI: 10.1093/bioinformatics/btz859. View

McAnulty M, Poosarla V, Kim K, Jasso-Chavez R, Logan B, Wood T . Electricity from methane by reversing methanogenesis. Nat Commun. 2017; 8:15419. PMC: 5442358. DOI: 10.1038/ncomms15419. View

Aklujkar M, Krushkal J, DiBartolo G, Lapidus A, Land M, Lovley D . The genome sequence of Geobacter metallireducens: features of metabolism, physiology and regulation common and dissimilar to Geobacter sulfurreducens. BMC Microbiol. 2009; 9:109. PMC: 2700814. DOI: 10.1186/1471-2180-9-109. View

Ouboter H, Berben T, Berger S, Jetten M, Sleutels T, Ter Heijne A . Methane-Dependent Extracellular Electron Transfer at the Bioanode by the Anaerobic Archaeal Methanotroph " Methanoperedens". Front Microbiol. 2022; 13:820989. PMC: 9039326. DOI: 10.3389/fmicb.2022.820989. View

Kang D, Li F, Kirton E, Thomas A, Egan R, An H . MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019; 7:e7359. PMC: 6662567. DOI: 10.7717/peerj.7359. View

Zhang X, Yuan Z, Hu S . Anaerobic oxidation of methane mediated by microbial extracellular respiration. Environ Microbiol Rep. 2021; 13(6):790-804. DOI: 10.1111/1758-2229.13008. View

Lovley D, Holmes D . Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms. Nat Rev Microbiol. 2021; 20(1):5-19. DOI: 10.1038/s41579-021-00597-6. View

10.

Berger S, Shaw D, Berben T, Ouboter H, In t Zandt M, Frank J . Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community. Biofilm. 2021; 3:100054. PMC: 8258643. DOI: 10.1016/j.bioflm.2021.100054. View

11.

Zhang X, McIlroy S, Vassilev I, Rabiee H, Plan M, Cai C . Polyhydroxyalkanoate-driven current generation via acetate by an anaerobic methanotrophic consortium. Water Res. 2022; 221:118743. DOI: 10.1016/j.watres.2022.118743. View

12.

Yu N, Wagner J, Laird M, Melli G, Rey S, Lo R . PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010; 26(13):1608-15. PMC: 2887053. DOI: 10.1093/bioinformatics/btq249. View

13.

Leu A, McIlroy S, Ye J, Parks D, Orphan V, Tyson G . Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family . mBio. 2020; 11(3). PMC: 7327174. DOI: 10.1128/mBio.01325-20. View

14.

Xiao Y, Zhang E, Zhang J, Dai Y, Yang Z, Christensen H . Extracellular polymeric substances are transient media for microbial extracellular electron transfer. Sci Adv. 2017; 3(7):e1700623. PMC: 5498105. DOI: 10.1126/sciadv.1700623. View

15.

Lu S, Wang J, Chitsaz F, Derbyshire M, Geer R, Gonzales N . CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res. 2019; 48(D1):D265-D268. PMC: 6943070. DOI: 10.1093/nar/gkz991. View

16.

Arshad A, Speth D, de Graaf R, Op den Camp H, Jetten M, Welte C . A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea. Front Microbiol. 2016; 6:1423. PMC: 4683180. DOI: 10.3389/fmicb.2015.01423. View

17.

Nauhaus K, Boetius A, Kruger M, Widdel F . In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol. 2002; 4(5):296-305. DOI: 10.1046/j.1462-2920.2002.00299.x. View

18.

Ye Y, Liu X, Nealson K, Rensing C, Qin S, Zhou S . Dissecting the Structural and Conductive Functions of Nanowires in Electroactive Biofilms. mBio. 2022; 13(1):e0382221. PMC: 8844916. DOI: 10.1128/mbio.03822-21. View

19.

Sieber C, Probst A, Sharrar A, Thomas B, Hess M, Tringe S . Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat Microbiol. 2018; 3(7):836-843. PMC: 6786971. DOI: 10.1038/s41564-018-0171-1. View

20.

Zhou Z, Tran P, Breister A, Liu Y, Kieft K, Cowley E . METABOLIC: high-throughput profiling of microbial genomes for functional traits, metabolism, biogeochemistry, and community-scale functional networks. Microbiome. 2022; 10(1):33. PMC: 8851854. DOI: 10.1186/s40168-021-01213-8. View