Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes

Abstract

Dissimilatory reduction of metal (e.g. Fe, Mn) (hydr)oxides represents a challenge for microorganisms, as their cell envelopes are impermeable to metal (hydr)oxides that are poorly soluble in water. To overcome this physical barrier, the Gram-negative bacteria Shewanella oneidensis MR-1 and Geobacter sulfurreducens have developed electron transfer (ET) strategies that require multihaem c-type cytochromes (c-Cyts). In S. oneidensis MR-1, multihaem c-Cyts CymA and MtrA are believed to transfer electrons from the inner membrane quinone/quinol pool through the periplasm to the outer membrane. The type II secretion system of S. oneidensis MR-1 has been implicated in the reduction of metal (hydr)oxides, most likely by translocating decahaem c-Cyts MtrC and OmcA across outer membrane to the surface of bacterial cells where they form a protein complex. The extracellular MtrC and OmcA can directly reduce solid metal (hydr)oxides. Likewise, outer membrane multihaem c-Cyts OmcE and OmcS of G. sulfurreducens are suggested to transfer electrons from outer membrane to type IV pili that are hypothesized to relay the electrons to solid metal (hydr)oxides. Thus, multihaem c-Cyts play critical roles in S. oneidensis MR-1- and G. sulfurreducens-mediated dissimilatory reduction of solid metal (hydr)oxides by facilitating ET across the bacterial cell envelope.

Fig. 1

Proposed models depicting electron transfer pathways for S. oneidensis MR-1 (A) and G. sulfurreducens (B) during dissimilatory reduction of solid metal (hydr)oxides. For simplicity, the quinone-reducing portion of respiratory chain, the peptidoglycan layer and the individual components of the type II secretion system (T2S) and type IV pilus (T4P) biogenesis machine (other than GspD/PilQ, GspF/PilC and pseudopilus/pilus apparatus) are omitted from these models. Identified multihaem c-type cytochromes (c-Cyts) are in red. Yellow arrows indicate the proposed electron transfer (ET) path. A. As a member of NapC/NirT family of quinol dehydrogenases, inner membrane (IM) c-Cyt CymA of S. oneidensis MR-1 is capable of oxidizing quinol at IM and reducing the redox proteins, such as c-Cyt MtrA, at periplasm (PS). MtrA might also interact with the outer membrane (OM) protein MtrB. Although it is not a c-Cyt, MtrB is speculated to facilitate ET across OM to MtrC, an OM c-Cyt. Pseudopilus apparatus of T2S, whose formation is regulated by a protein complex in the IM, where only GspF is shown, pushes MtrC and OmcA (another OM c-Cyt) from PS through GspD to the surface of bacterial cells where MtrC and OmcA form a functional complex. The cell surface MtrC and OmcA are capable of directly reducing solid Fe(III)/Mn(III, IV) (hydr)oxides. B. In G. sulfurreducens, OM c-Cyts OmcE and OmcS are suggested to transfer electrons to the T4P apparatus, which then transfers electrons directly to solid Fe(III)/Mn(III, IV) (hydr)oxides. The structural components that mediate ET from the IM to OmcE/OmcS in the OM during reduction of solid metal (hydr)oxides have yet to be identified experimentally.