Genomic Plasticity Enables a Secondary Electron Transport Pathway in Shewanella oneidensis

Abstract

Microbial dissimilatory iron reduction is an important biogeochemical process. It is physiologically challenging because iron occurs in soils and sediments in the form of insoluble minerals such as hematite or ferrihydrite. Shewanella oneidensis MR-1 evolved an extended respiratory chain to the cell surface to reduce iron minerals. Interestingly, the organism evolved a similar strategy for reduction of dimethyl sulfoxide (DMSO), which is reduced at the cell surface as well. It has already been established that electron transfer through the outer membrane is accomplished via a complex in which ␤-barrel proteins enable interprotein electron transfer between periplasmic oxidoreductases and cell surface-localized terminal reductases. MtrB is the ␤-barrel protein that is necessary for dissimilatory iron reduction. It forms a complex together with the periplasmic decaheme c-type cytochrome MtrA and the outer membrane decaheme c-type cytochrome MtrC. Consequently, mtrB deletion mutants are unable to reduce ferric iron. The data presented here show that this inability can be overcome by a mobile genomic element with the ability to activate the expression of downstream genes and which is inserted within the SO4362 gene of the SO4362-to-SO4357 gene cluster. This cluster carries genes similar to mtrA and mtrB and encoding a putative cell surface DMSO reductase. Expression of SO4359 and SO4360 alone was sufficient to complement not only an mtrB mutant under ferric citrate-reducing conditions but also a mutant that furthermore lacks any outer membrane cytochromes. Hence, the putative complex formed by the SO4359 and SO4360 gene products is capable not only of membrane-spanning electron transfer but also of reducing extracellular electron acceptors.

Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1

“…There are now several examples of strains of Fe(III)-reducing microorganisms undergoing mutations to develop alternative strategies for extracellular electron transfer following gene deletions (65,66) or simply in response to strong selective pressure for rapid electron transfer (51). The ability of KN400 to adapt to the loss of pili demonstrates that caution may be warranted in extrapolating to natural environments the mechanisms for Fe(III) oxide reduction elucidated in studies with cultures maintained for long periods under laboratory conditions that do not mimic those found in soils and sediments.…”

Unbalanced fermentation of glycerol in Escherichia coli via heterologous production of an electron transport chain and electrode interaction in microbial electrochemical cells

“…Hence, cymA mutants are unable to use a multitude of anoxic electron acceptors, including ferric iron and anodes (Myers and Myers, 1997;Schwalb et al, 2003). Beyond CymA, MtrA is the only other periplasmic cytochrome that is required for iron and anode respiration (Bretschger et al, 2007;Schicklberger et al, 2013). Furthermore, among the array of expressed periplasmic c-type cytochromes, two proteins are produced in larger amounts (Fonseca et al, 2013).…”

Extracellular reduction of solid electron acceptors byShewanella oneidensis

“…In S. oneidensis the electron flux across the outer membrane can occur via one of four porin–cytochrome conduits; the MtrCAB complex, (Richardson et al, ) ; the MtrFED complex (McLean et al, ) the DmsEFA DMSO reductase system (Gralnick et al, ) and the SO_4359–SO_4360 system (Schicklberger et al, ). Of these the MtrCAB complex, which is constitutively expressed, is the best characterized and has a clear role in dissimilatory metal reduction.…”