Jackson, R. B. et al. Human activities now fuel two-thirds of global methane emissions. Environ. Res. Lett. 19, 101002 (2024).
Ermler, U., Grabarse, W., Shima, S., Goubeaud, M. & Thauer, R. K. Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. Science 278, 1457–1462 (1997).
Grabarse, W. et al. On the mechanism of biological methane formation: structural evidence for conformational changes in methyl-coenzyme M reductase upon substrate binding. J. Mol. Biol. 309, 315–330 (2001).
Evans, P. N. et al. An evolving view of methane metabolism in the Archaea. Nat. Rev. Microbiol. 17, 219–232 (2019).
Scheller, S., Goenrich, M., Boecher, R., Thauer, R. K. & Jaun, B. The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 465, 606–608 (2010).
Hahn, C. J. et al. Crystal structure of a key enzyme for anaerobic ethane activation. Science 373, 118–121 (2021).
Rospert, S., Böcher, R., Albracht, S. P. J. & Thauer, R. K. Methyl-coenzyme M reductase preparations with high specific activity from H2-preincubated cells of Methanobacterium thermoautotrophicum. FEBS Lett. 291, 371–375 (1991).
Goubeaud, M., Schreiner, G. & Thauer, R. K. Purified methyl‐coenzyme‐M reductase is activated when the enzyme‐bound coenzyme F430 is reduced to the nickel (I) oxidation state by titanium (III) citrate. Eur. J. Biochem. 243, 110–114 (1997).
Becker, D. F. & Ragsdale, S. W. Activation of methyl-SCoM reductase to high specific activity after treatment of whole cells with sodium sulfide. Biochemistry 37, 2639–2647 (1998).
Zhou, Y., Dorchak, A. E. & Ragsdale, S. W. In vivo activation of methyl-coenzyme M reductase by carbon monoxide. Front. Microbiol. 4, 69 (2013).
Holliger, C., Pierik, A. J., Reijerse, E. J. & Hagen, W. R. A spectroelectrochemical study of factor F430 nickel (II/I) from methanogenic bacteria in aqueous solution. J. Am. Chem. Soc. 115, 5651–5656 (1993).
Chadwick, G. L., Joiner, A. M., Ramesh, S., Mitchell, D. A. & Nayak, D. D. McrD binds asymmetrically to methyl-coenzyme M reductase improving active-site accessibility during assembly. Proc. Natl Acad. Sci. USA 120, e2302815120 (2023).
Zheng, K., Ngo, P. D., Owens, V. L., Yang, X. P. & Mansoorabadi, S. O. The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea. Science 354, 339–342 (2016).
Prakash, D., Wu, Y., Suh, S. J. & Duin, E. C. Elucidating the process of activation of methyl-coenzyme M reductase. J. Bacteriol. 196, 2491–2498 (2014).
Rouvière, P. & Wolfe, R. Component A3 of the methylcoenzyme M methylreductase system of Methanobacterium thermoautotrophicum ΔH: resolution in two components. J. Bacteriol. 179, 4556–4562 (1989).
Kuhner, C. H., Lindenbach, B. D. & Wolfe, R. S. Component A2 of methylcoenzyme M reductase system from Methanobacterium thermoautotrophicum ΔH: nucleotide sequence and functional expression by Escherichia coli. J. Bacteriol. 175, 3195–3203 (1993).
Shao, N. et al. Expression of divergent methyl/alkyl coenzyme M reductases from uncultured archaea. Commun. Biol. 5, 1113 (2022).
Kaiser, J. T., Hu, Y., Wiig, J. A., Rees, D. C. & Ribbe, M. W. Structure of precursor-bound NifEN: a nitrogenase FeMo cofactor maturase/insertase. Science 331, 91–94 (2011).
Lancaster, K. M., Hu, Y., Bergmann, U., Ribbe, M. W. & DeBeer, S. X-ray spectroscopic observation of an interstitial carbide in NifEN-bound FeMoco precursor. J. Am. Chem. Soc. 135, 610–612 (2013).
Bao, J., de Dios Mateos, E. & Scheller, S. Efficient CRISPR/Cas12a-based genome-editing toolbox for metabolic engineering in Methanococcus maripaludis. ACS Synth. Biol. 11, 2496–2503 (2022).
Jarrett, J. T. in Encyclopedia of Biophysics (ed. Roberts, G. C. K.) 1153–1156 (Springer, 2013).
Duin, E. C., Prakash, D. & Brungess, C. in Methods in Enzymology, Vol. 494 (eds Rosenzweig, A. & Ragsdale, S. W.) 159–187 (Academic Press, 2011).
Rouvière, P. E., Bobik, T. A. & Wolfe, R. S. Reductive activation of the methyl coenzyme M methylreductase system of Methanobacterium thermoautotrophicum ΔH. J. Bacteriol. 170, 3946–3952 (1988).
Cedervall, P. E., Dey, M., Pearson, A. R., Ragsdale, S. W. & Wilmot, C. M. Structural insight into methyl-coenzyme M reductase chemistry using coenzyme B analogues. Biochemistry 49, 7683–7693 (2010).
Wongnate, T. et al. The radical mechanism of biological methane synthesis by methyl-coenzyme M reductase. Science 352, 953–958 (2016).
Hu, Y. & Ribbe, M. W. Biosynthesis of the metalloclusters of nitrogenases. Annu. Rev. Biochem. 85, 455–483 (2016).
Jasniewski, A. J., Lee, C. C., Ribbe, M. W. & Hu, Y. Reactivity, mechanism, and assembly of the alternative nitrogenases. Chem. Rev. 120, 5107–5157 (2020).
Tanifuji, K. et al. Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite. Nat. Chem. 13, 1228–1234 (2021).
Spatzal, T. et al. Evidence for interstitial carbon in nitrogenase FeMo cofactor. Science 334, 940 (2011).
Rutledge, H. L., Cook, B. D., Nguyen, H. P., Herzik, M. A. Jr & Tezcan, F. A. Structures of the nitrogenase complex prepared under catalytic turnover conditions. Science 377, 865–869 (2022).
Warmack, R. A. et al. Structural consequences of turnover-induced homocitrate loss in nitrogenase. Nat. Commun. 14, 1091 (2023).
Schmidt, F. V. et al. Structural insights into the iron nitrogenase complex. Nat. Struct. Mol. Biol. 31, 150–158 (2024).
Sippel, D. & Einsle, O. The structure of vanadium nitrogenase reveals an unusual bridging ligand. Nat. Chem. Biol. 13, 956–960 (2017).
Jenner, L. P., Cherrier, M. V., Amara, P., Rubio, L. M. & Nicolet, Y. An unexpected P-cluster like intermediate en route to the nitrogenase FeMo-co. Chem. Sci. 12, 5269–5274 (2021).
Stripp, S. T. et al. Second and outer coordination sphere effects in nitrogenase, hydrogenase, formate dehydrogenase, and CO dehydrogenase. Chem. Rev. 122, 11900–11973 (2022).
Page, C. C., Moser, C. C., Chen, X. & Dutton, P. L. Natural engineering principles of electron tunnelling in biological oxidation–reduction. Nature 402, 47–52 (1999).
Valer, L. et al. Histidine ligated iron‐sulfur peptides. ChemBioChem 23, e202200202 (2022).
Telser, J., Davydov, R., Horng, Y. C., Ragsdale, S. W. & Hoffman, B. M. Cryoreduction of methyl-coenzyme M reductase: EPR characterization of forms, MCRox1 and MCRred1. J. Am. Chem. Soc. 123, 5853–5860 (2001).
Mahlert, F., Bauer, C., Jaun, B., Thauer, R. K. & Duin, E. C. The nickel enzyme methyl-coenzyme M reductase from methanogenic archaea: in vitro induction of the nickel-based MCR-ox EPR signals from MCR-red2. J. Biol. Inorg. Chem. 7, 500–513 (2002).
Rettberg, L. A. et al. Probing the coordination and function of Fe4S4 modules in nitrogenase assembly protein NifB. Nat. Commun. 9, 2824 (2018).
Lago-Maciel, A. et al. Methylthio-alkane reductases use nitrogenase metalloclusters for carbon-sulfur bond cleavage. Preprint at bioRxiv https://doi.org/10.1101/2024.10.19.619033 (2024).
Hua, Z. S. et al. Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea. Nat. Commun. 10, 4574 (2019).
Mei, R., Kaneko, M., Imachi, H. & Nobu, M. K. The origin and evolution of methanogenesis and Archaea are intertwined. PNAS Nexus 2, pgad023 (2023).
Garcia, P. S., Gribaldo, S. & Borrel, G. Diversity and evolution of methane-related pathways in archaea. Annu. Rev. Microbiol. 76, 727–755 (2022).
Kang, W. et al. X‐Ray crystallographic analysis of NifB with a full complement of clusters: structural insights into the radical SAM‐dependent carbide insertion during nitrogenase cofactor assembly. Angew. Chem. Int. Ed. 60, 2364–2370 (2021).
Fay, A. W., Wiig, J. A., Lee, C. C. & Hu, Y. Identification and characterization of functional homologs of nitrogenase cofactor biosynthesis protein NifB from methanogens. Proc. Natl Acad. Sci. USA 112, 14829–14833 (2015).
Lie, T. J. et al. A genetic study of Nif-associated genes in a hyperthermophilic methanogen. Microbiol. Spectrum 10, e02093-21 (2022).
Saini, J., Dhamad, A., Muniyasamy, A., Alverson, A. J. & Lessner, D. J. The nitrogenase cofactor biogenesis enzyme NifB is essential for the viability of methanogens. Preprint at bioRxiv https://doi.org/10.1101/2023.10.20.563283 (2023).
Vazquez Ramos, J. et al. Characterization of the iron–sulfur clusters in the nitrogenase‐like reductase CfbC/D required for coenzyme F430 biosynthesis. FEBS J. 291, 3233–3248 (2024).
Zehnder, A. J. & Wuhrmann, K. Titanium (III) citrate as a nontoxic oxidation-reduction buffering system for the culture of obligate anaerobes. Science 194, 1165–1166 (1976).
Dürichen, H., Diekert, G. & Studenik, S. Redox potential changes during ATP‐dependent corrinoid reduction determined by redox titrations with europium (II)–DTPA. Protein Sci. 28, 1902–1908 (2019).
Buckel, W. & Thauer, R. K. Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochim. Biophys. Acta Bioenerg. 1827, 94–113 (2013).
Amstrup, S. K. et al. Structural remodelling of the carbon–phosphorus lyase machinery by a dual ABC ATPase. Nat. Commun. 14, 1001 (2023).
Jeoung, J. H., Martins, B. M. & Dobbek, H. Double‐cubane [8Fe9S] clusters: a novel nitrogenase‐related cofactor in biology. ChemBioChem 21, 1710–1716 (2020).
Goenrich, M., Duin, E. C., Mahlert, F. & Thauer, R. K. Temperature dependence of methyl-coenzyme M reductase activity and of the formation of the methyl-coenzyme M reductase red2 state induced by coenzyme B. J. Biol. Inorg. Chem. 10, 333–342 (2005).
Ebner, S., Jaun, B., Goenrich, M., Thauer, R. K. & Harmer, J. Binding of coenzyme B induces a major conformational change in the active site of methyl-coenzyme M reductase. J. Am. Chem. Soc. 132, 567–575 (2010).
Harmer, J. et al. Spin density and coenzyme M coordination geometry of the ox1 form of methyl-coenzyme M reductase: a pulse EPR study. J. Am. Chem. Soc. 127, 17744–17755 (2005).
Pérez-González, A. et al. Exploring the role of the central carbide of the nitrogenase active-site FeMo-cofactor through targeted 13 C labeling and ENDOR spectroscopy. J. Am. Chem. Soc. 143, 9183–9190 (2021).
Raymond, J., Siefert, J. L., Staples, C. R. & Blankenship, R. E. The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541–554 (2004).
Boyd, E. S. et al. A late methanogen origin for molybdenum‐dependent nitrogenase. Geobiology 9, 221–232 (2011).
Labun, K. et al. CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing. Nucleic Acids Res. 47, W171–W174 (2019).
Long, F., Wang, L., Lupa, B. & Whitman, W. B. A flexible system for cultivation of Methanococcus and other formate-utilizing methanogens. Archaea 2017, 7046026 (2017).
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
Bepler, T. et al. Positive-unlabeled convolutional neural networks for particle picking in cryo-electron micrographs. Nat. Methods 16, 1153–1160 (2019).
Jamali, K. et al. Automated model building and protein identification in cryo-EM maps. Nature 628, 450–457 (2024).
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
Moser, J. et al. Structure of ADP-aluminium fluoride-stabilized protochlorophyllide oxidoreductase complex. Proc. Natl Acad. Sci. USA 110, 2094–2098 (2013).
Garcia, A. K., McShea, H., Kolaczkowski, B. & Kaçar, B. Reconstructing the evolutionary history of nitrogenases: evidence for ancestral molybdenum‐cofactor utilization. Geobiology 18, 394–411 (2020).
Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
Nguyen, L. T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., Von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).
Valer, L. et al. Methods to identify and characterize iron–sulfur oligopeptides in water. Can. J. Chem. 100, 475–483 (2022).
Ragsdale, S. W., Raugei, S., Ginovska, B. & Wongnate, T. in The Biological Chemistry of Nickel (eds Zamble, D. et al.) 149–169 (Royal Society of Chemistry, 2017).
Portis, A. M. Electronic structure of F centers: saturation of the electron spin resonance. Phys. Rev. 91, 1071–1078 (1953).
Castner, T. G. Jr. Saturation of the paramagnetic resonance of a V center. Phys. Rev. 115, 1506–1515 (1959).
Hirsh, D. J. & Brudvig, G. W. Measuring distances in proteins by saturation-recovery EPR. Nat. Protoc. 2, 1770–1781 (2007).
Rupp, H., Rao, K. K., Hall, D. O. & Cammack, R. Electron spin relaxation of iron-sulphur proteins studied by microwave power saturation. Biochim. Biophys. Acta Protein Struct. 537, 255–269 (1978).
Adam, P. S., Kolyfetis, G. E., Bornemann, T. L., Vorgias, C. E. & Probst, A. J. Genomic remnants of ancestral methanogenesis and hydrogenotrophy in Archaea drive anaerobic carbon cycling. Sci. Adv. 8, eabm9651 (2022).