Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms

Carbonic anhydrase, a zinc enzyme found in organisms from all kingdoms, catalyses the reversible hydration of carbon dioxide and is used for inorganic carbon acquisition by phytoplankton. In the oceans, where zinc is nearly depleted, diatoms use cadmium as a catalytic metal atom in cadmium carbonic anhydrase (CDCA). Here we report the crystal structures of CDCA in four distinct forms: cadmium-bound, zinc-bound, metal-free and acetate-bound. Despite lack of sequence homology, CDCA is a structural mimic of a functional β-carbonic anhydrase dimer, with striking similarity in the spatial organization of the active site residues. CDCA readily exchanges cadmium and zinc at its active site—an apparently unique adaptation to oceanic life that is explained by a stable opening of the metal coordinating site in the absence of metal. Given the central role of diatoms in exporting carbon to the deep sea, their use of cadmium in an enzyme critical for carbon acquisition establishes a remarkable link between the global cycles of cadmium and carbon. Cadmium fills a niche A major part of the carbon export from the atmosphere to the deep ocean is carried out by marine phytoplankton, using carbonic anhydrase to catalyse the reversible hydration of carbon dioxide. The active site of this enzyme usually contains zinc, but some diatoms substitute cadmium — usually regarded as a toxic element — as the catalytic metal atom. The X-ray crystal structures of four forms of this enzyme from the diatom Thalassiosira weissflogii — cadmium-bound, zinc-bound, metal-free and acetate-bound — have now been determined. The enzyme can easily exchange metals at its catalytic centre, suggesting that marine diatoms use of cadmium when zinc is rare, a considerable competitive advantage in the metal-poor environment of the oceans. The X-ray crystal structures of the cadmium-bound, zinc-bound, metal-free and acetate-bound forms of cadmium carbonic anhydrase are solved; the enzyme can incorporate either zinc or cadmium as its metal centre and can easily exchange one metal for the other.