Photoreduction of Shewanella oneidensis Extracellular Cytochromes by Organic Chromophores and Dye‐Sensitized TiO₂

Abstract

The transfer of photoenergized electrons from extracellular photosensitizers across a bacterial cell envelope to drive intracellular chemical transformations represents an attractive way to harness nature's catalytic machinery for solar‐assisted chemical synthesis. In Shewanella oneidensis MR‐1 (MR‐1), trans‐outer‐membrane electron transfer is performed by the extracellular cytochromes MtrC and OmcA acting together with the outer‐membrane‐spanning porin⋅cytochrome complex (MtrAB). Here we demonstrate photoreduction of solutions of MtrC, OmcA, and the MtrCAB complex by soluble photosensitizers: namely, eosin Y, fluorescein, proflavine, flavin, and adenine dinucleotide, as well as by riboflavin and flavin mononucleotide, two compounds secreted by MR‐1. We show photoreduction of MtrC and OmcA adsorbed on RuII‐dye‐sensitized TiO2 nanoparticles and that these protein‐coated particles perform photocatalytic reduction of solutions of MtrC, OmcA, and MtrCAB. These findings provide a framework for informed development of strategies for using the outer‐membrane‐associated cytochromes of MR‐1 for solar‐driven microbial synthesis in natural and engineered bacteria.

Engineered Nanoenzymes with Multifunctional Properties for Next‐Generation Biological and Environmental Applications

“…[ 88 ] Ainsworth and colleagues coated Ru II ‐dye‐sensitized TiO 2 nanoparticles with surface exposed MtrC and OmcA from S. oneidensis MR‐1 eliciting photocatalytic reduction of these proteins. [ 89 ] The inclusion of these cytochromes into abiotic Ru‐sensitized TiO 2 nanoparticles improved the ability of these nanoparticles to reduce protein complexes paving the way for the development of strategies that use surface‐exposed proteins for solar microbial synthesis.…”

Membrane Protein Modified Electrodes in Bioelectrocatalysis

“…The transmembrane cytochrome MtrCAB, helped by OmcA located on the outside of the membrane, are known to transfer electrons between the interior of the cell and extracellular materials ( Figure 6) [231,232]. In the presence of a sacrificial electron donor, MtrC and OmcA can be photoreduced by water-soluble photosensitisers including eosin Y, fluorescein, proflavine, flavin, and adenine dinucleotide, riboflavin and flavin mononucleotide [233]. In an in vitro approach, it was showed that dye-sensitised TiO 2 nanoparticles can photoreduce MtrC or OmcA, either in solution or one an electrode surface [233][234][235] and it might be possible to extend this process to reductive photosynthesis in S. oneidensis [236].…”

“…In the presence of a sacrificial electron donor, MtrC and OmcA can be photoreduced by water-soluble photosensitisers including eosin Y, fluorescein, proflavine, flavin, and adenine dinucleotide, riboflavin and flavin mononucleotide [233]. In an in vitro approach, it was showed that dye-sensitised TiO 2 nanoparticles can photoreduce MtrC or OmcA, either in solution or one an electrode surface [233][234][235] and it might be possible to extend this process to reductive photosynthesis in S. oneidensis [236]. To provide a proof-of-concept, we recently reconstituted MtrCAB into proteoliposomes encapsulating a redox dye, Reactive Red 120 (RR120), which can be reductively bleached.…”

The Molecular Basis for Binding of an Electron Transfer Protein to a Metal Oxide Surface

“…Electron transfer between a protein and inorganic material forms the foundation for a wide range of enzyme-and microbebased bioelectronic, 1 bioelectrocatalytic 2 and optobioelectronic 3 applications, including bioelectronic sensing, 1,4 solar production of fuels, 5 bioremediation, 6 biomining, 7 water purification, 8 and microbial 9 and enzymatic 10 fuel cells. The major scientific challenge in these fields is achieving electron transfer that is energetically efficient at a rate that is commensurate with enzyme turnover.…”

“…Electron transfer between a protein and inorganic material forms the foundation for a wide range of enzyme- and microbe-based bioelectronic, bioelectrocatalytic and optobioelectronic applications, including bioelectronic sensing, , solar production of fuels, bioremediation, biomining, water purification, and microbial and enzymatic fuel cells. The major scientific challenge in these fields is achieving electron transfer that is energetically efficient at a rate that is commensurate with enzyme turnover. ,, The coupling distance for direct electron transfer, which requires proper positioning of the redox site of the protein relative to the electrode material, varies between 10 and 30 Å. , To address this challenge, researchers have sought to orient enzymes on the electrode surface by displaying molecules on the electrode that mimic substrates of the enzyme, − by attaching molecules that penetrate the enzyme close to an electron relay center on the electrode, , and electrostatically directed covalent bonding of the protein to the electrode .…”