Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR‐1

Abstract

SummaryFour distinct pathways predicted to facilitate electron flow for respiration of externally located substrates are encoded in the genome of Shewanella oneidensis strain MR-1. Although the pathways share a suite of similar proteins, the activity of only two of these pathways has been described. Respiration of extracellular substrates requires a mechanism to facilitate electron transfer from the quinone pool in the cytoplasmic membrane to terminal reductase enzymes located on the outer leaflet of the outer membrane. The four pathways share MtrA paralogues, a periplasmic electron carrier cytochrome, and terminal reductases similar to MtrC for reduction of metals, flavins and electrodes or to DmsAB for reduction of dimethyl sulphoxide (DMSO). The promiscuity of respiratory electron transfer reactions catalysed by these pathways has made studying strains lacking single proteins difficult. Here, we present a comprehensive analysis of MtrA and MtrC paralogues in S. oneidensis to define the roles of these proteins in respiration of insoluble iron oxide, soluble iron citrate, flavins and DMSO. We present evidence that some periplasmic electron carrier components and terminal reductases in these pathways can provide partial compensation in the absence of the primary component, a phenomenon described as modularity, and discuss biochemical and evolutionary implications.

Microbial community structure and function of Nitrobenzene reduction biocathode in response to carbon source switchover

“…In this study, the detected outer membrane cytochrome c genes included decaheme OmcA/MtrC (Richter et al, 2012a), MtrF (a homologue of OmcA/MtrC) (Coursolle and Gralnick, 2010), and OmpA. Periplasmic multi-heme cytochrome c including one decaheme MtrA, 11 decaheme DmsE (a homologue of MtrA) (Coursolle and Gralnick, 2010), 3 inner membrane anchored (periplasm side) tetraheme NapC/NirT (a homologue of quinol dehydrogenase CymA) (McMillan et al, 2012) and 2 transmembrane high-molecular-weight cytochrome electron-transferring complexes were detected (Fig. 7).…”

Structure of a bacterial cell surface decaheme electron conduit

“…To exploit these abundant electron sinks, specific respiratory electron transfer mechanisms must overcome the physical limitations associated with electron transfer across the outer membrane (OM) to solid extracellular terminal electron acceptors. In Shewanella oneidensis this involves proteins coded by the mtrDEF-omcA-mtrCAB gene cluster (1,2). MtrA and MtrB form a trans-OM electron transport complex that comprises a β-barrel porin (MtrB) in which a decaheme cytochrome (MtrA) is embedded (3,4).…”

Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials

“…This possibility is heavily used by dissimilatory metal reducing bacteria (DMRB), which are capable of using extracellular solid metal oxides as terminal respiratory electron sinks, a process that has been suggested to proceed via direct cell-mineral contact (1), extracellular redox shuttles (2), and/or pilus-like appendages (3,4). Although essential to the survival of the bacterium, extracellular ET also plays an important role in the biogeochemical cycling of transition metals (5)(6)(7).…”