Extracellular Fe(III) reductase structure reveals a modular organization enabling S-layer insertion and electron transfer to insoluble substrates

• Published in: Structure (London) 2023-02, Vol.31 (2), p.174-184.e3
• Main Authors: Tikhonova, Tamara V., Osipov, Evgenii M., Dergousova, Natalia I., Boyko, Konstantin M., Elizarov, Ivan M., Gavrilov, Sergey N., Khrenova, Maria G., Robb, Frank T., Solovieva, Anastasia Y., Bonch-Osmolovskaya, Elizaveta A., Popov, Vladimir O.
• Format: Article
• Language: English
• Subjects: Carboxydothermus ferrireducens; Cytochromes - metabolism; Electron Transport; Electrons; extracellular electron transfer; Ferric Compounds - metabolism; Gram-positive bacteria; multiheme cytochromes; Oxidation-Reduction; Oxidoreductases - genetics; Oxidoreductases - metabolism; S-layer attachment; terminal oxidoreductases; X-ray structure
• ISSN: 0969-2126; 1878-4186
• DOI: 10.1016/j.str.2022.12.010

The thermophilic anaerobic Gram-positive bacterium Carboxydothermus ferrireducens utilizes insoluble Fe(III) oxides as electron acceptors in respiratory processes using an extracellular 11-heme cytochrome c OmhA as a terminal reductase. OmhA is able to transfer electrons to soluble and insoluble Fe(III) compounds, substrates of multiheme oxidoreductases, and soluble electron shuttles. The crystal structure of OmhA at 2.5 Å resolution shows that it consists of two functionally distinct parts: the cytochrome с electron transfer and the S-layer binding domains. Nonaheme C-terminal subdomain of the cytochrome с domain is structurally similar to the extracellular multiheme cytochrome OcwA from the metal-reducing Gram-positive bacterium “Thermincola potens.” S-layer binding domain of OmhA is responsible for interaction with the S-layer that surrounds the Carboxydothermus ferrireducens cell envelope. The structural foundations enabling the embedding of extracellular multiheme cytochromes to the S-layer of a Gram-positive-type cell wall and putative electron transfer pathways to insoluble minerals are discussed. [Display omitted] •Extracellular cytochrome c OmhA transfers electrons to insoluble Fe(III) compounds•OmhA reveals modular organization and comprises two domains with distinct functions•SLP-like domain enables incorporation of OmhA into the S-layer of the microorganism•Cytochrome c domain provides electron transfer pathways to insoluble mineral acceptors Tikhonova et al. present the crystal structure of the 11-heme-containing cytochrome c OmhA, a key element of extracellular electron transfer of the Gram-positive bacterium Carboxydothermus ferrireducens. The structural foundations of OmhA binding to the S-layer of the microorganism and putative electron transfer pathways to mineral acceptors are discussed.