New insights in uranium bioremediation by cytochromes of the bacterium Geotalea uraniireducens

Abstract

The bacterium Geotalea uraniireducens, commonly found in uranium-contaminated environments, plays a key role in bioremediation strategies by converting the soluble hexavalent form of uranium (U(VI)) into less soluble forms ( e.g., U(IV)). While most of the reduction and concomitant precipitation of uranium occur outside the cells, there have been reports of important reduction processes taking place in the periplasm. In any case, the triheme periplasmic cytochromes are key players, either by ensuring an effective interface between the cell’s interior and exterior or by directly participating in the reduction of the metal. Therefore, understanding the functional mechanism of the highly abundant triheme cytochromes in G. uraniireducens’ is crucial for elucidating the respiratory pathways in this bacterium. In this work, a detailed functional characterization of the triheme cytochromes PpcA and PpcB from G. uraniireducens was conducted using NMR and visible spectroscopy techniques. Despite sharing high amino acid sequence identity and structural homology with their counterparts from Geobacter sulfurreducens, the results showed that the heme reduction potential values are less negative, the order of oxidation of the hemes is distinct, and the redox and redox-Bohr network of interactions revealed unprecedented functional mechanisms in the cytochromes of G. uraniireducens. In these cytochromes, the reduction potential values of the three heme groups are much more similar, resulting in a narrower range of values, that facilitates directional electron flow from the inner membrane, thereby optimizing the uranium reduction.