Abstract
Bacteria and archaea import molybdenum and tungsten from the environment in the form of the oxyanions molybdate (MoO4 2−) and tungstate (WO4 2−). These substrates are captured by an external, high-affinity binding protein, and delivered to ATP binding cassette transporters, which move them across the cell membrane. We have recently reported a crystal structure of the molybdate/tungstate binding protein ModA/WtpA from Archaeoglobus fulgidus, which revealed an octahedrally coordinated central metal atom. By contrast, the previously determined structures of three bacterial homologs showed tetracoordinate molybdenum and tungsten atoms in their binding pockets. Until then, coordination numbers above four had only been found for molybdenum/tungsten in metalloenzymes where these metal atoms are part of the catalytic cofactors and coordinated by mostly non-oxygen ligands. We now report a high-resolution structure of A. fulgidus ModA/WtpA, as well as crystal structures of four additional homologs, all bound to tungstate. These crystal structures match X-ray absorption spectroscopy measurements from soluble, tungstate-bound protein, and reveal the details of the distorted octahedral coordination. Our results demonstrate that the distorted octahedral geometry is not an exclusive feature of the A. fulgidus protein, and suggest distinct binding modes of the binding proteins from archaea and bacteria.
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Abbreviations
- ABC:
-
ATP binding cassette
- AfModA:
-
Archaeoglobus fulgidus ModA/WtpA
- EXAFS:
-
Extended X-ray absorption fine structure
- MaModA:
-
Methanosarcina acetivorans ModA/WtpA
- MjModA:
-
Methanocaldococcus jannaschii ModA/WtpA
- PEG:
-
Poly(ethylene glycol)
- PfModA:
-
Pyrococcus furiosus ModA/WtpA
- PhModA:
-
Pyrococcus horikoshii ModA/WtpA
- Tris:
-
Tris(hydroxymethyl)aminomethane
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Acknowledgments
We thank the beamline staff at the Swiss Light Source for assistance with diffraction data collection, and D.C. Rees for discussions. This work was supported by the Roche Research Fund, the National Center for Competence in Research (NCCR) Structural Biology Zurich, the Swiss National Science Foundation, and the European Commission, Research Infrastructure Action under FP6 “Structuring the European Research Area Specific Programme,” contract no. RII3-CT-2004-506008 for supporting access to the EMBL. The coordinates and structure factors have been deposited in the Protein Data Bank under IDs 3CIJ (AfModA), 3CFX (MaModA), 3CG1 (PfModA), 3CFZ (MjModA), and 3CG3 (PhModA).
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K. Hollenstein and M. Comellas-Bigler contributed equally to this work.
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Hollenstein, K., Comellas-Bigler, M., Bevers, L.E. et al. Distorted octahedral coordination of tungstate in a subfamily of specific binding proteins. J Biol Inorg Chem 14, 663–672 (2009). https://doi.org/10.1007/s00775-009-0479-7
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DOI: https://doi.org/10.1007/s00775-009-0479-7