Identifying the potential extracellular electron transfer pathways from a c-type cytochrome network

Abstract

Extracellular electron transfer (EET) is the key feature of some bacteria, such as Geobacter sulfurreducens and Shewanella oneidensis. Via EET processes, these bacteria can grow on electrode surfaces and make current output of microbial fuel cells. c-Type cytochromes can be used as carriers to transfer electrons, which play an important role in EET processes. Typically, from the inner (cytoplasmic) membrane through the periplasm to the outer membrane, they could form EET pathways. Recent studies suggest that a group of c-type cytochromes could form a network which extended the well-known EET pathways. We obtained the protein interaction information for all 41 c-type cytochromes in Shewanella oneidensis MR-1, constructed a large-scale protein interaction network, and studied its structural characteristics and functional significance. Centrality analysis has identified the top 10 key proteins of the network, and 7 of them are associated with electricity production in the bacteria, which suggests that the ability of Shewanella oneidensis MR-1 to produce electricity might be derived from the unique structure of the c-type cytochrome network. By modularity analysis, we obtained 5 modules from the network. The subcellular localization study has shown that the proteins in these modules all have diversiform cellular compartments, which reflects their potential to form EET pathways. In particular, combination of protein subcellular localization and operon analysis, the well-known and new candidate EET pathways are obtained from the Mtr-like module, indicating that potential EET pathways could be obtained from such a c-type cytochrome network.

Lack of Periplasmic Non-heme Protein SorA Increases Shewanella decolorationis Current Generation

“…The four proteins were predicted to be located in periplasmic space by using online software 2 , which is consistent with the SorAB location in several other bacteria such as Starkeya novella and Aeropyrum pernix (Meyer et al, 2004;Denger et al, 2008). SorA often coexists with SorB for sulfite respiration (Myers and Kelly, 2005) and is predicted to have electronic interactions with trimethylamine N-oxide reductase (TorA) and nitrate ammonification protein (NapA) in S. oneidensis MR-1 (Ding et al, 2014). Our previous results showed that deletion of gene SHD2782 in S. decolorationis S12 resulted in 30% decrease in current generation (Kong et al, 2017).…”

“…In S. decolorationis S12 periplasm, SorA co-exists with many other redox proteins, including those involved in EET. It is possible that SorA diverts electrons from the efficient EET pathways (e.g., cymA-MtrABC) to other electron pools (e.g., TorA and NapA) in the periplasm (Ding et al, 2014) and thus suppresses the current generation of strain S12.…”

Transcriptional regulatory module analysis reveals that bridge proteins reconcile multiple signals in extracellular electron transfer pathways

“…Shewanella oneidensis MR‐1 is one of the most well‐known electricigens and can respire anaerobically by utilizing a wide variety of extracellular electron acceptors (termed extracellular electron transfer, EET) . Currently, the following four EET pathways have been proposed to fulfill EET processes: (a) the MtrCAB pathway (CymA → MtrA → MtrB → MtrC/OmcA), (b) the MtrDEF pathway (CymA → MtrD → MtrE → MtrF), (c) the DMSO pathway (CymA → DmsE → DmsF → DmsA/DmsB), and (d) the SO_4360‐57 pathway (CymA → SO_4360 → SO_4359 → SO_4358/SO_4357) . Briefly, the inner membrane c ‐type cytochrome CymA can gather electrons generated in the cytoplasm; then, with the periplasmic c ‐type cytochromes MtrA/MtrD/DmsE/SO_4360 and outer membrane proteins MtrB/MtrE/DmsF/SO_4359, these electrons can be transferred from CymA to the extracellular components MtrC‐OmcA/MtrF/DmsAB/SO_4358‐57, respectively, which can further transfer the electrons to extracellular electron acceptors.…”

K-shell Analysis Reveals Distinct Functional Parts in an Electron Transfer Network and Its Implications for Extracellular Electron Transfer

“…The electron transfer network was then modeled as an undirected graph, in which nodes represent the proteins and the links represent protein interactions. It is clear that network structure strongly correlates with its function, for example, several classical EET pathways have been identified by modular analysis of a c -type cytochrome network ( Ding et al, 2014 ). As k-shell analysis has been widely used to explain both the formation and current structure of networks ( Kitsak et al, 2010 ; Pei et al, 2014 ), we thus engaged this method to study the formation and extension of Shewanella electron transfer network and its functional parts, as well as their potential implications for EET processes.…”

“…Previous studies have revealed the high efficiency of the prediction of biological pathways from biological networks ( Planas-Iglesias et al, 2012 ; Huang et al, 2013 ; Mukhopadhyay and Maulik, 2014 ). Following initial work on a small-scale c -type cytochrome network ( Zhang et al, 2008 ), a recent study constructed a network for all of 41 c -type cytochromes in S. oneidensis MR-1 and the classical EET pathways (e.g., MtrCAB, MtrDEF) can be identified from the c -type cytochrome network ( Ding et al, 2014 ). Furthermore, from the view of steric properties of individual proteins, Volkov and van Nuland (2012) performed extensive conformational sampling, mapped out functional epitopes in c -type cytochrome complexes (involving cytochrome c and other redox-active proteins such as peroxidase and cytochrome b 5 ) and then assessed the electron transfer properties of such interactions.…”