Volume 16, Issue 1 p. 255-264
Research article

Rare earth metals are essential for methanotrophic life in volcanic mudpots

Arjan Pol

Arjan Pol

Department of Microbiology, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands

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Thomas R. M. Barends

Thomas R. M. Barends

Department of Biomolecular Mechanisms, Max-Planck Institute for Medical Research, Jahnstrasse 29, D-69120 Heidelberg, Germany

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Andreas Dietl

Andreas Dietl

Department of Biomolecular Mechanisms, Max-Planck Institute for Medical Research, Jahnstrasse 29, D-69120 Heidelberg, Germany

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Ahmad F. Khadem

Ahmad F. Khadem

Department of Microbiology, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands

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Jelle Eygensteyn

Jelle Eygensteyn

Department of General Instruments, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands

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Mike S. M. Jetten

Corresponding Author

Mike S. M. Jetten

Department of Microbiology, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands

For correspondence. E-mail [email protected]; Tel. (+31) (0) 24 365 2940; Fax (+31) (0) 24 365 2830.Search for more papers by this author
Huub J. M. Op den Camp

Huub J. M. Op den Camp

Department of Microbiology, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands

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First published: 18 August 2013
Citations: 368

Summary

Growth of Methylacidiphilum fumariolicum SolV, an extremely acidophilic methanotrophic microbe isolated from an Italian volcanic mudpot, is shown to be strictly dependent on the presence of lanthanides, a group of rare earth elements (REEs) such as lanthanum (Ln), cerium (Ce), praseodymium (Pr) and neodymium (Nd). After fractionation of the bacterial cells and crystallization of the methanol dehydrogenase (MDH), it was shown that lanthanides were essential as cofactor in a homodimeric MDH comparable with one of the MDHs of Methylobacterium extorquens AM1. We hypothesize that the lanthanides provide superior catalytic properties to pyrroloquinoline quinone (PQQ)-dependent MDH, which is a key enzyme for both methanotrophs and methylotrophs. Thus far, all isolated MxaF-type MDHs contain calcium as a catalytic cofactor. The gene encoding the MDH of strain SolV was identified to be a xoxF-ortholog, phylogenetically closely related to mxaF. Analysis of the protein structure and alignment of amino acids showed potential REE-binding motifs in XoxF enzymes of many methylotrophs, suggesting that these may also be lanthanide-dependent MDHs. Our findings will have major environmental implications as metagenome studies showed (lanthanide-containing) XoxF-type MDH is much more prominent in nature than MxaF-type enzymes.