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

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 A resolution shows that it consists of two functionally distinct parts: the cytochrome s electron transfer and the S-layer binding domains. Nonaheme C-terminal subdomain of the cytochrome s domain is structurally similar to the extracellular multiheme cytochrome OcwA from the metal-reducing Gram-posi-tive 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.

Automated summary

The paper investigates Carboxydothermus ferrireducens, a thermophilic anaerobic Gram-positive bacterium that utilizes insoluble Fe(III) oxides as electron acceptors with the help of extracellular 11-heme cytochrome c OmhA as a terminal reductase. OmhA can transfer electrons to both soluble and insoluble Fe(III) compounds, as well as substrates of multiheme oxidoreductases and soluble electron shuttles. The crystal structure of OmhA reveals two distinct parts: the cytochrome's electron transfer domain and the S-layer binding domain. The article discusses the embedding of extracellular multiheme cytochromes to the S-layer of a Gram-positive-type cell wall and the potential electron transfer pathways to insoluble minerals.