A synthetic biology approach to engineering living photovoltaics

Abstract

The ability to electronically interface living cells with electron accepting scaffolds is crucial for the development of next-generation biophotovoltaic technologies. Although recent studies have focused on engineering synthetic interfaces that can maximize electronic communication between the cell and scaffold, the efficiency of such devices is limited by the low conductivity of the cell membrane. This review provides a materials science perspective on applying a complementary, synthetic biology approach to engineering membrane-electrode interfaces. It focuses on the technical challenges behind the introduction of foreign extracellular electron transfer pathways in bacterial host cells and the past and future efforts to engineer photosynthetic organisms with artificial electron-export capabilities for biophotovoltaic applications. The article highlights advances in engineering protein-based, electron-exporting conduits in a model host organism, E. coli, before reviewing state-of-the-art biophotovoltaic technologies that use both unmodified and bioengineered photosynthetic bacteria with improved electron transport capabilities. A thermodynamic analysis is used to propose an energetically feasible pathway for extracellular electron transport in engineered cyanobacteria and identify metabolic bottlenecks amenable to protein engineering techniques. Based on this analysis, an engineered photosynthetic organism expressing a foreign, protein-based electron conduit yields a maximum theoretical solar conversion efficiency of 6–10% without accounting for additional bioengineering optimizations for light-harvesting.

Design of Optimized PEDOT‐Based Electrodes for Enhancing Performance of Living Photovoltaics Based on Phototropic Bacteria

“…For example, microbes can be bioengineered to produce their own mediators for improved indirect electron transfer [13] or to express electronic conduits for improved direct electron transfer in the absence of exogenous mediators. [14] The bioengineering of exoelectrogenic, photosynthetic cells has only recently emerged as a viable area of research [3][4][5][6][7][8][9][10][11][12][13][14][15] as studies continue to identify new naturally occurring exoelectrogenic microbes and to elucidate their electron transfer mechanisms. [16][17][18] However, even in absence of added mediators and bioengineering, bioelectricity generation from wildtype microbes can still be reasonably improved through appropriate electrode design.…”

“…Biophotovoltaics (BPVs) are electrochemical systems that can convert solar energy into electrical energy by exploiting the photosynthetic activity of autotrophs. Compared to BPV devices that rely on isolated photosynthetic proteins and cell fragments, BPVs based on living, whole‐cell microbes benefit from prolonged stability and diminished processing and maintenance costs 1–4. Whole‐cell BPVs, or living photovoltaics, operate similarly to conventional microbial fuel cells (MFCs),5 albeit using water as the fuel and light to enable its highly endothermic oxidation.…”

Purple Bacteria and 3D Redox Hydrogels for Bioinspired Photo‐bioelectrocatalysis

“…Isolated photosynthetic apparatus often allow an easier electron transfer process, as their active redox sites are easily accessible; however, maintaining their functionality after immobilization on the electrode surface is challenging . In contrast, intact bacterial cells have the advantage of being capable to self‐repair and reproduce . The major challenge for their application is the transfer of the photoexcited electrons to the electrode surface, which requires overcoming of the insulating layer constituted by the cellular membrane in a process defined as extracellular electron transfer (EET) .…”

“…[8] In contrast, intact bacterial cells have the advantage of being capable to self-repair and reproduce. [9] The major challenge for their application is the transfer of the photoexcited electrons to the electrode surface, [10] which requires overcoming of the insulating layer constituted by the cellular membrane in ap rocess defined as extracellular electron transfer (EET). [11] Exogenous soluble redox mediators are often utilized to accomplish EET,a s they can diffuse through the cellular membrane and shuttle the photoexcited electrons to the electrode surface.…”

Engineering bacteria for biogenic synthesis of chalcogenide nanomaterials

“…To create a synthetic microbial system capable of producing arsenic sulfide nanostructures, genes for arsenate and thiosulfate reduction were introduced via plasmids (Table 1) into a heterologous host, E. coli. Escherichia coli was chosen as the host organism because it is genetically well characterized with developed tools for synthetic biology applications and has successfully been used as a host strain for expression of Shewanella pathways (Malasarn et al, 2008;Ang et al, 2013;Jensen et al, 2016;Schuergers et al, 2017).…”