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A conspicuous nickel protein in microbial mats that oxidize methane anaerobically

Abstract

Anaerobic oxidation of methane (AOM) in marine sediments is an important microbial process in the global carbon cycle and in control of greenhouse gas emission. The responsible organisms supposedly reverse the reactions of methanogenesis1,2,3,4,5,6,7,8, but cultures providing biochemical proof of this have not been isolated. Here we searched for AOM-associated cell components in microbial mats from anoxic methane seeps in the Black Sea9,10,11. These mats catalyse AOM rather than carry out methanogenesis. We extracted a prominent nickel compound displaying the same absorption spectrum as the nickel cofactor F430 of methyl-coenzyme M reductase, the terminal enzyme of methanogenesis12; however, the nickel compound exhibited a higher molecular mass than F430. The apparent variant of F430 was part of an abundant protein that was purified from the mat and that consists of three different subunits. Determined amino-terminal amino acid sequences matched a gene locus cloned from the mat. Sequence analyses revealed similarities to methyl-coenzyme M reductase from methanogenic archaea. The abundance of the nickel protein (7% of extracted proteins) in the mat suggests an important role in AOM.

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Figure 1: Biochemical analysis of a microbial mat that oxidizes methane anaerobically.
Figure 2: Identification of the genes encoding the dominant protein, Ni-protein I, in the mat with the capacity for anaerobic oxidation of methane.
Figure 3: Phylogenetic relationships between Ni-protein I and MCR, and between the ANME-1 cluster and methanogenic archaea.

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Acknowledgements

We are particularly grateful to W. Michaelis, K. Nauhaus, R. Seifert and the Professor Logachev shipboard party for providing microbial mat samples, and to A. Boetius for coordination work and advice. We thank J. Moll, R. Appel and M. Sordel-Klippert for technical assistance; J. Knecht for the chemical analyses; D. Linder for N-terminal sequencing; and H. Teeling and T. Lombardot for help with bioinformatics. This work is part of the projects MUMM, GHOSTDABS and the GenoMic network Göttingen, supported by the Federal Ministry of Education and Research (Germany). Further support came from the Max Planck Society. This is a publication of GHOSTDABS and of the programme GEOTECHNOLOGIEN of the Federal Ministry of Education and Research and the Deutsche Forschungsgemeinschaft.

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Correspondence to Friedrich Widdel or Rudolf K. Thauer.

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Krüger, M., Meyerdierks, A., Glöckner, F. et al. A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426, 878–881 (2003). https://doi.org/10.1038/nature02207

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