Evolution of a new enzyme for carbon disulphide conversion by an acidothermophilic archaeon

摘要

Extremophilic organisms require specialized enzymes for their exotic metabolisms. Acid-loving thermophilic Archaea that live in the mudpots of volcanic solfataras obtain their energy from reduced sulphur compounds such as hydrogen sulphide (H_2S) and carbon disulphide (CS_2). The oxidation of these compounds into sulphuric acid creates the extremely acidic environment that characterizes solfataras. The hyperthermophilic Acidianus strain Al-3, which was isolated from the fumarolic, ancient sauna building at the Solfatara volcano (Naples, Italy), was shown to rapidly convert CS_2 into H_2S and carbon dioxide (CO_2), but nothing has been known about the modes of action and the evolution of the enzyme(s) involved. Here we describe the structure, the proposed mechanism and evolution of a CS_2 hydrolase from Acidianus Al-3. The enzyme monomer displays a typical P-carbonic anhydrase fold and active site, yet CO_2 is not one of its substrates. Owing to large carboxy- and amino-terminal arms, an unusual hexadecameric catenane oligomer has evolved. This structure results in the blocking of the entrance to the active site that is found in canonical P-carbonic anhydrases and the formation of a single 15-A-long, highly hydrophobic tunnel that functions as a specificity filter. The tunnel determines the enzyme's substrate specificity for CS_2, which is hydrophobic. The transposon sequences that surround the gene encoding this CS_2 hydrolase point to horizontal gene transfer as a mechanism for its acquisition during evolution. Our results show how the ancient P-carbonic anhydrase, which is central to global carbon metabolism, was transformed by divergent evolution into a crucial enzyme in CS_2 metabolism.