Bespoke Biomolecular Wires for Transmembrane Electron Transfer: Spontaneous Assembly of a Functionalized Multiheme Electron Conduit

Abstract

Shewanella oneidensis exchanges electrons between cellular metabolism and external redox partners in a process that attracts much attention for production of green electricity (microbial fuel cells) and chemicals (microbial electrosynthesis). A critical component of this pathway is the outer membrane spanning MTR complex, a biomolecular wire formed of the MtrA, MtrB, and MtrC proteins. MtrA and MtrC are decaheme cytochromes that form a chain of close-packed hemes to define an electron transfer pathway of 185 Å. MtrA is wrapped inside MtrB for solubility across the outer membrane lipid bilayer; MtrC sits outside the cell for electron exchange with external redox partners. Here, we demonstrate tight and spontaneous in vitro association of MtrAB with separately purified MtrC. The resulting complex is comparable with the MTR complex naturally assembled by Shewanella in terms of both its structure and rates of electron transfer across a lipid bilayer. Our findings reveal the potential for building bespoke electron conduits where MtrAB combines with chemically modified MtrC, in this case, labeled with a Ru-dye that enables light-triggered electron injection into the MtrC heme chain.

Photocatalytic Removal of the Greenhouse Gas Nitrous Oxide by Liposomal Microreactors

“…They readily photoreduce MV 2+ when irradiated with white light in the presence of EDTA (ethylenediaminetetraacetic acid) as sacrificial electron donor [20] . The nanoparticles also catalyze light‐driven transmembrane electron transfer through MtrCAB [15, 21] …”

“…[20] The nanoparticles also catalyze light-driven transmembrane electron transfer through MtrCAB. [15,21] Gas chromatography was used to assess photocatalytic removal of N 2 O by our liposome microreactors (Figure 5A). Headspace N 2 O concentration was sampled over 8 hr, with white-light irradiation in the first 4 hr, for suspensions of proteoliposomes containing MV, N 2 O, graphitic N-doped carbon dots and 25 mM EDTA.…”

Photocatalytic Removal of the Greenhouse Gas Nitrous Oxide by Liposomal Microreactors

“…From the rate of dithionite oxidation reported for the liposomes in this study, together with the spectroscopically defined MtrCAB concentration in the sample (see above), an electron flux of 28 s À 1 MtrCAB À 1 is estimated which is again [20] and of MtrCAB in lipid bilayers. [15,21]…”

“…In the oxidized state MtrCAB contains Fe III hemes that give a characteristic Soret band with maximum absorbance at 410 nm. [7b, 15] This feature was [15] for the MtrCAB complex from S. oneidensis based on the crystal structure [7c] of S. baltica MtrCAB. Hemes (orange) with iron (black) are shown as spheres within the MtrA and MtrC proteins (yellow).…”

Biodegradation of pollutants by exoelectrogenic bacteria is not always performed extracellularly

“…More recently, exoelectrogens, as well as non‐exoelectrogens, have been coupled to light‐harvesting nanomaterials, mainly CdS quantum dots, creating semi‐artificial photosynthetic biohybrids (Sakimoto et al ., 2016 ; Wang et al ., 2019 ; Martins et al ., 2021 ). Such biohybrids could in principle be engineered to use light energy to drive either outward and inward electron transfer (Piper et al ., 2021 ). So far, the focus has mainly been on photobioelectrosynthesis, where light‐driven electron transfer into microbes is utilized for the synthesis of organic materials, ammonia or hydrogen.…”