Zeta-carbonic anhydrases show CS2 hydrolase activity: A new metabolic carbon acquisition pathway in diatoms?

CDCA1 is a very peculiar member of the Carbonic Anhydrase (CA) family. It has been the first enzyme to show an efficient utilization of Cd(II) ions in Nature and a unique adaptation capability to live on the surface ocean. Indeed, in this environment, which is extremely depleted in essential metal ions, CDCA1 can utilize Zn(II) or Cd(II) as catalytic metal to support the metabolic needs of fast growing diatoms. In this paper we demonstrate a further catalytic versatility of this enzyme by using a combination of X-ray crystallography, molecular dynamics simulations and enzymatic experiments. First we identified the CO2 binding site and the way in which this substrate travels from the environment to the enzyme active site. Then, starting from the observation of a structural similarity with the substrate entry route of CS2 hydrolase from Acidanius A1-3, we hypothesized and demonstrated that also CS2 is a substrate for CDCA1. This finding is new and unexpected since until now only few CS2 hydrolases have been characterized, and none of them is reported to have any CO2 hydratase action. The physiological implications of this supplementary catalytic activity still remain to be unveiled. We suggest here that it could represent another ability of diatoms expressing CDCA1 to adapt to the external environment. Indeed, the ability of this enzyme to convert CS2 could represent an alternative source of carbon acquisition for diatoms, in addition to CO2. (C) 2021 The Authors. Published by Elsevier B.V. on behalf of Research Network of Computational and Structural Biotechnology.

Automated summary

CDCA1 is a unique enzyme within the Carbonic Anhydrase family, capable of utilizing Cd(II) ions and adapting to surface ocean environments. It has been shown to catalyze both CO2 and CS2, potentially providing diatoms with an alternative carbon source for growth and adaptation to their surroundings.