Distorted octahedral coordination of tungstate in a subfamily of specific binding proteins

Abstract

Bacteria and archaea import molybdenum and tungsten from the environment in the form of the oxyanions molybdate (MoO 4 2-) and tungstate (WO 4 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.

Anion Recognition in Water: Recent Advances from a Supramolecular and Macromolecular Perspective

“…The binding pocket is primarily hydrophobic, provides only four hydrogen bonds, and could also host iodide anions; unusually, the protein's biological function could also be activated in the presence of iodide 67. It was discovered in 2009 that bacterial uptake of molybdate and tungstate was enabled through modification of the anion itself: up to that time all known metalloprotein structures containing Mo or W displayed tetracoordinate metal centers, but octahedral coordination was encountered in transporter proteins, with two carboxylate groups providing extra coordination directly to the metal centers while hydrogen‐bond donors complemented the oxygen atoms 68. Such a finding could provide inspiration for new strategies to bind multiatomic anions.…”

Vanadium haloperoxidases: From the discovery 30 years ago to X-ray crystallographic and V K-edge absorption spectroscopic studies

“…small (comparable to the intensity for vanadate in that region) if it is taken over a relatively long data range ( Figure 5D). Alternative interpretations have been put forward for the remote haloperoxidase shells, such as a shell of protein heteroatoms that are H-bonded to the vanadate [135], and, by analogy to the archaeal tungstate binding proteins [136], throughabsorber multiple scattering involving the axial ligand donor atoms in the trigonal bipyramid, which would appear in the Fourier transform at the sum of the V-N(imidazole) and V-O(axial) distances [137].…”

Complexation and Toxicity of Copper in Higher Plants. II. Different Mechanisms for Copper versus Cadmium Detoxification in the Copper-Sensitive Cadmium/Zinc Hyperaccumulator Thlaspi caerulescens (Ganges Ecotype)

“…Their high intensity (in particular the 5-Å peak) suggests that it is a metalmetal interaction, because lighter elements cannot result in such a large peak at such an extreme distance from the central atom. Even multiple scattering within the first shell that recently has been identified in a very limited number of metalloproteins (Ha et al, 2007;Hollenstein et al, 2009) would occur at shorter distances and thus can be ruled out. The identity of the metal at 5 Å can be obtained from the EXAFS data only with an uncertainty of one or two atomic numbers, but due to the metal content in the plant samples it could only be a Cu-Cu interaction.…”