TiO2: A Critical Interfacial Material for Incorporating Photosynthetic Protein Complexes and Plasmonic Nanoparticles into Biophotovoltaics

TiO2, a photosensitive semiconducting material, has been widely reported as a good photoanode material in dye-sensitized solar cells and new emerging perovskite cells. Its proper electronic band structure, surface chemistry and hydrophilic nature provide a reactive surface for interfacing with different organic and inorganic photon capturing materials in photovoltaics. Here, we review its enabling role in incorporating two special materials toward biophotovoltaics, including photosynthetic protein complexes extracted from plants and plasmonic nanoparticles (e.g., gold or silver nanoparticles), which interplay to enhance the absorption and utilization of sun light. We will first give a brief introduction to the TiO2 photoanode, including preparation, optical and electrochemical properties, and then summarize our recent research and other related literature on incorporating photosynthetic light harvest complexes and plasmonic nanoparticles onto anatase TiO2 photoanodes as a means to tap into the charge separation, electron and energy transfer, and photovoltaic enhancements in the bio-photovoltaics

The Development of Biophotovoltaic Systems for Power Generation and Biological Analysis.

Biophotovoltaic systems (BPVs) resemble microbial fuel cells, but utilise oxygenic photosynthetic microorganisms associated with an anode to generate an extracellular electrical current, which is stimulated by illumination. Study and exploitation of BPVs have come a long way over the last few decades, having benefited from several generations of electrode development and improvements in wiring schemes. Power densities of up to 0.5 W m-2 and the powering of small electrical devices such as a digital clock have been reported. Improvements in standardisation have meant that this biophotoelectrochemical phenomenon can be further exploited to address biological questions relating to the organisms. Here, we aim to provide both biologists and electrochemists with a review of the progress of BPV development with a focus on biological materials, electrode design and interfacial wiring considerations, and propose steps for driving the field forward

Rational design of artificial redox-mediating systems toward upgrading photobioelectrocatalysis

Photobioelectrocatalysis has recently attracted particular research interest owing to the possibility to achieve sunlight-driven biosynthesis, biosensing, power generation, and other niche applications. However, physiological incompatibilities between biohybrid components lead to poor electrical contact at the biotic-biotic and biotic-abiotic interfaces. Establishing an electrochemical communication between these different interfaces, particularly the biocatalyst-electrode interface, is critical for the performance of the photobioelectrocatalytic system. While different artificial redox mediating approaches spanning across interdisciplinary research fields have been developed in order to electrically wire biohybrid components during bioelectrocatalysis, a systematic understanding on physicochemical modulation of artificial redox mediators is further required. Herein, we review and discuss the use of diffusible redox mediators and redox polymer-based approaches in artificial redox-mediating systems, with a focus on photobioelectrocatalysis. The future possibilities of artificial redox mediator system designs are also discussed within the purview of present needs and existing research breadth

Fullerenes Enhance Self-Assembly and Electron Injection of Photosystem i in Biophotovoltaic Devices

This paper describes the fabrication of microfluidic devices with a focus on controlling the orientation of photosystem I (PSI) complexes, which directly affects the performance of biophotovoltaic devices by maximizing the efficiency of the extraction of electron/hole pairs from the complexes. The surface chemistry of the electrode on which the complexes assemble plays a critical role in their orientation. We compared the degree of orientation on self-assembled monolayers of phenyl-C61-butyric acid and a custom peptide on nanostructured gold electrodes. Biophotovoltaic devices fabricated with the C61 fulleroid exhibit significantly improved performance and reproducibility compared to those utilizing the peptide, yielding a 1.6-fold increase in efficiency. In addition, the C61-based devices were more stable under continuous illumination. Our findings show that fulleroids, which are well-known acceptor materials in organic photovoltaic devices, facilitate the extraction of electrons from PSI complexes without sacrificing control over the orientation of the complexes, highlighting this combination of traditional organic semiconductors with biomolecules as a viable approach to coopting natural photosynthetic systems for use in solar cells

Self-assembled photosystem-I biophotovoltaics on nanostructured TiO2 and ZnO

The abundant pigment-protein membrane complex photosystem-I (PS-I) is at the heart of the Earth’s energy cycle. It is the central molecule in the “Z-scheme” of photosynthesis, converting sunlight into the chemical energy of life. Commandeering this intricately organized photosynthetic nanocircuitry and re-wiring it to produce electricity carries the promise of inexpensive and environmentally friendly solar power. We here report that dry PS-I stabilized by surfactant peptides functioned as both the light-harvester and charge separator in solar cells self-assembled on nanostructured semiconductors. Contrary to previous attempts at biophotovoltaics requiring elaborate surface chemistries, thin film deposition, and illumination concentrated into narrow wavelength ranges the devices described here are straightforward and inexpensive to fabricate and perform well under standard sunlight yielding open circuit photovoltage of 0.5 V, fill factor of 71%, electrical power density of 81 µW/cm2 and photocurrent density of 362 µA/cm2, over four orders of magnitude higher than any photosystem-based biophotovoltaic to date

A High Power-Density, Mediator-Free, Microfluidic Biophotovoltaic Device for Cyanobacterial Cells.

Biophotovoltaics has emerged as a promising technology for generating renewable energy because it relies on living organisms as inexpensive, self-repairing, and readily available catalysts to produce electricity from an abundant resource: sunlight. The efficiency of biophotovoltaic cells, however, has remained significantly lower than that achievable through synthetic materials. Here, a platform is devised to harness the large power densities afforded by miniaturized geometries. To this effect, a soft-lithography approach is developed for the fabrication of microfluidic biophotovoltaic devices that do not require membranes or mediators. Synechocystis sp. PCC 6803 cells are injected and allowed to settle on the anode, permitting the physical proximity between cells and electrode required for mediator-free operation. Power densities of above 100 mW m-2 are demonstrated for a chlorophyll concentration of 100 μM under white light, which is a high value for biophotovoltaic devices without extrinsic supply of additional energy.RCUK, OtherThis is the final version of the article. It first appeared from Wiley via http://dx.doi.org/10.1002/aenm.20140129

Optymalizacja procesów transferu energii i transferu elektronowego w biofotowoltaicznych nanourządzeniach zawierających fotosystem I oraz cytochrom c553 z ekstremofilnego krasnorostu Cyanidioschyzon merolae

One of the biggest challenges of modern-day solar technologies is to develop carbon-neutral, efficient and sustainable systems for solar energy conversion into electricity and fuel. Over the last two decades there has been a growing impact of ‘green’ solar conversion technologies based on the natural solar energy converters, such as the robust extremophilic photosystem I (PSI) and its associated protein cofactors. The main bottleneck of the currently available biophotovoltaic and solar-to-fuel technologies is the low power conversion efficiency of the available devices due to wasteful charge recombination reactions at the interfaces between the working modules, as well as instability of the organic and inorganic components. This thesis describes the development of three novel approaches to improve energy and electron transfer in PSI-based biophotoelectrodes and plasmonic nanostructures: (1) construction of all-solid-state mediatorless biophotovoltaic devices incorporating p-doped silicon substrate, extremophilic robust PSI complex and its associated light harvesting antenna (PSI-LHCI) in conjunction with its natural electron donor cytochrome c553 (cyt c553) from a red microalga Cyanidioschyzon merolae and (2), biofunctionalization of the silver nanowires (AgNWs) with a highly organised architecture of the cyt c553/PSI-LHCI assembly for the significant improvement of absorption cross-section of the C. merolae PSI-LHCI complex due to plasmonic interactions between the distinct subpool of chlorophylls (Chls) and AgNWs nanoconstructs. The third (3) approach was based on development of the photo-driven in vitro hydrogen production system following hybridisation of the robust extremophilic PSI-LHCI complex with the novel and established proton reducing catalysts (PRC). The last approach has led to generation of molecular hydrogen with TOF of 521 mol H2 (mol PSI)-1 min-1 and 729 mol H2 (mol PSI)-1 min-1 for the hybrid systems of PSI-LHCI with cobaloxime and the DuBois-type mononuclear nickel proton reduction catalysts, respectively. The TOF values for biophotocatalytic H2 production obtained in this study were 3-fold and 16.6-fold higher than those published for cyanobacterial PSI/PRC hybrid systems employing cobaloxime and a similar Ni mononuclear PRC, respectively. Construction of all-solid-state mediatorless PSI-based nanodevices was facilitated by biopassivation of the p-doped Si substrate with His6-tagged cyt c553, as evidenced by significant lowering of the inherent dark saturation current (J0), a well-known semiconductor surface recombination parameter. Five distinct variants of cyt c553 were obtained by genetically engineering the specific linker peptides of 0-19 amino acids in length between the cyt c553 holoprotein and a C-terminal His6-tag, the latter being the affinity ‘anchor’ used for specific immobilisation of this protein on the semiconductor surface. The calculated 2D Gibbs free energy maps for all the five cyt c553 variants and the protein lacking any peptide linker showed a much higher number of thermodynamically feasible conformations for the cyt c variants containing longer linker peptides upon their specific immobilisation on the Si surface. The bioinformatic calculations were verified by constructing the respective cyt c553/Si bioelectrodes and measuring their dark current-voltage (J-V) characteristics to determine the degree of p-doped Si surface passivation, measured by minimisation of the J0 recombination parameter. The combined bioinformatic and J-V analyses indicated that the cyt c553 variants with longer linker peptides, up to 19AA in length, allowed for more structural flexibility of immobilised cyt c553 in terms of both, orientation and distance of the haem group with respect to the Si surface, resulting in efficient biopassivation of this semiconductor substrate. This molecular approach has allowed for the developing of an alternative, cheap and facile route for significant reduction of the inherent minority charge recombination at the p-doped Si surface. To improve direct electron transfer within all-solid state PSI-based nanodevices, the specific His6-tagged cyt c553 variants, generated in this study, were attached to the Ni-NTA-functionalised p-doped Si surface prior to incorporation of the PSI-LHCI photoactive layer. Such nanoarchitecture resulted in an open-circuit potential increment of 333 μV for the specific PSI-LHCI/cyt c553/Si nanodevice compared to the control device devoid of cyt c553. Moreover, the all-solid state mediatorless PSI-LHCI-based devices produced photocurrents in the range of 104-234 μA/cm2 when a bias of -0.25 V was applied, demonstrating one of the highest photocurrents for this type of solid-state devices reported to date. The power conversion efficiency of the PSI-LHCI/p-doped Si devices was 20-fold higher when 19AA variant of cyt c553 was incorporated as the biological conductive interface between the PSI-LHCI photoactive module and the substrate, demonstrating the significant role of this cyt variant for improving direct electron transfer within the PSI-based all-solid-state mediatorless biophotovoltaic device. In a complementary line of research, it was demonstrated that the highly controlled assembly of C. merolae PSI-LHCI complex on plasmon-generating AgNWs substantially improved the optical functionality of such a novel biohybrid nanostructure. By comparing fluorescence intensities measured for PSI-LHCI complex randomly oriented on AgNWs and the results obtained for the PSI-LHCI/cyt c553 bioconjugate with AgNWs it was concluded that the specific binding of PSI-LHCI complex with the defined uniform orientation yields selective excitation of a pool of Chls that are otherwise almost non-absorbing. This is remarkable, as this work shows for the first time that plasmonic excitations in metallic nanostructures not only can be used to enhance native absorption of photosynthetic pigments, but also, by employing cyt c553 as the conjugation cofactor, to activate the specific Chl pools as the absorbing sites, only when the uniform and well-defined orientation of PSI-LHCI complex with respect to plasmonic nanostructures is achieved. This innovative approach paves the way for the next generation solar energy-converting technologies to outperform the reported-to-date biohybrid devices with respect to power conversion efficiency.Jednym z głównych wyzwań technologicznych jest opracowanie wydajnych i odnawialnych systemów konwersji energii słonecznej w elektryczność i paliwo, stosując zerowy bilans emisji związków węgla. W ciągu ostatnich dwóch dekad nastąpił znaczący postęp w zastosowaniu “zielonych” technologii biofotowoltaicznych, opartych na naturalnych białkach absorbujących energię słoneczną, takich jak fotosystem I (PSI) wraz ze związanymi z nim kompleksami antenowymi i kofaktorami transportu elektronowego. Głównym ograniczeniem obecnych urządzeń fotowoltaicznych jest ich niska wydajność kwantowa, związana z procesami rekombinacji ładunku w interfejsach pomiędzy modułami tych urządzeń, jak również ograniczona stabilność zastosowanych jak dotąd biologicznych i syntetycznych komponentów. W ramach niniejszej rozprawy doktorskiej opracowano nowatorską technologię, polegającą na zastosowaniu wysokostabilnego PSI oraz naturalnego donora elektronów dla tego kompleksu, cytochromu c553 (cyt c553), wyizolowanych z ekstremofilnego krasnorostu Cyanidioschyzon merolae, do konstrukcji trzech typów nanourządzeń biofotowoltaicznych: (1), biofotoogniw w stałej konfiguracji (ang., all-solid-state), zawierających domieszkowany pozytywnie półprzewodnikowy substrat krzemowy (ang., p-doped Si, p-Si) wraz z warstwami fotoaktywnego kompleksu PSI i cyt c553; (2), plazmonowych srebrnych bionanodrutów (AgNWs), funkcjonalizowanych wysokouporządkowaną nanoarchitekturą monowarstw PSI i cyt c553, oraz (3), systemu fotokatalitycznej produkcji wodoru cząsteczkowego in vitro z zastosowaniem kompleksów hybrydowych PSI wraz z syntetycznymi katalizatorami redukcji protonów (ang., proton reducing catalysts, PRC). W przypadku ostatniego z powyższych systemów, optymalizacja biofotokatalitycznej produkcji wodoru cząsteczkowego z zastosowaniem systemów hybrydowych z PSI i PRC, opartych na kobaloksymie i niklowym katalizatorze mononuklearnym typu DuBois, precypitowanych na powierzchni PSI w roztworze wodnym, pozwoliła na osiągnięcie aktywności wydzielania wodoru odpowiednio, 521 moli H2 (mol PSI)-1 min-1 oraz 729 moli H2 (mol PSI)-1 min-1, przewyższając tym samym 3-17-krotnie aktywność wydzielania wodoru w podobnych systemach biohybrydowych i warunkach pomiarowych. Poraz pierwszy zastosowano cyt c553 z C-terminalną metką His6 do biopasywacji półprzewodnikowego substratu p-Si, mierzonej minimalizacją parametru rekombinacji powierzchniowej J0. Poprzez inżynierię genetyczną sklonowano i wyrażono w E. coli 5 różnych wariantów cyt c553, z których 4 zawierały w swej strukturze sekwencje peptydowe o długości 5-19 aminokwasów (AA), aby zbadać ich wpływ na procesy rekombinacji ładunku w obrębie elektrody krzemowej. Peptydy te zostały wstawione pomiędzy holobiałkiem a metką His6, którą zastosowano do unieruchomienia każdego z wariantów cyt c553 na powierzchni elektrody. Obliczenie energii swobodnej Gibbsa pozwoliło na utworzenie konformacyjnych map 2D dla każdego z wariantów, w których pokazano, iż warianty z semi-helikalnym peptydem 19AA przyjmują znacząco większą liczbę termodynamicznie możliwych konformacji na powierzchni elektrody pod względem odległości i kąta nachylenia grupy hemowej w stosunku do powierzchni elektrody. Bioinformatyczna analiza została potwierdzona poprzez ciemniową charakterystykę prądowo-napięciową (J-V) utworzonych odpowiednio bioelektrod krzemowo-cytochromowych. Stwierdzono, że warianty cyt c553 z dłuższymi peptydami pomiędzy metką His6 a holobiałkiem efektywnie minimalizują prądy ciemniowe krzemowego substratu, najprawdopodobniej dzięki istnieniu większej ilości termodynamicznie zoptymalizowanych konformacji cytochromu, pozwalających na minimalizację rekombinacji ładunku powierzchniowego substratu. Funkcjonalizacja elektrody p-Si wariantem cyt c553, charakteryzującym się największym stopniem swobody orientacji grupy hemowej w stosunku powierzchni elektrody krzemowej, pozwoliła na efektywną biopasywację tego półprzewodnikowego substratu poprzez minimalizację parametru J0, co z kolei pozwoliło na zwiększenie parametru Voc o 333 μV w biofotoogniwach typu PSI/cyt c553/p-Si, w porównaniu do kontroli zawierającej jedynie PSI/p-Si. Uzyskano fotoprądy w stałych biofotoogniwach PSI/p-Si w zakresie 104-234 μA cm-2 (przy nadpotencjale -0.25 V), co należy do jednych z najwyższych wartości fotoprądów wygenerowanych przez stałe biofotoogniwa z PSI, w podobnych warunkach pomiarowych. Jednocześnie wydajność konwersji energii słonecznej w fotoogniwach typu PSI-LHCI/cyt c553/p-Si była 20-krotnie wyższa, w obecności wariantu cyt c553 19AA, zastosowanego w tych urządzeniech jako biologiczna warstwa biopasywacji substratu krzemowego oraz warstwa kondukcyjna pomiędzy substratem a PSI. Tym samym wykazano, że ów wariant może być zastosowany w urządzeniach biofotowoltaicznych do zwiększenia transferu elektronowego pomiędzy substratem a PSI. W równoległym i komplementarnym kierunku badań, zastosowanie równomiernej i specyficznie ukierunkowanej nanoarchitektury fotoaktywnej warstwy PSI na plazmonowych nanostrukturach metalicznych AgNWs, sfunkcjonalizowanych uprzednio cyt c553, pozwoliło na znaczące zwiększenie efektywnej absorpcji PSI, w zakresie spektralnym, w którym PSI jest nieaktywny in vivo, poprzez aktywację specyficznej puli tzw. czerwonych cząsteczek chlorofilu w obrębie fluoroforów PSI. Tym samym pokazano, że oddziaływania plazmonowe mogą być efektywnie zastosowane nie tylko do zwiększenia całkowitej absorpcji fotoaktywnych kompleksów białkowych, ale również do aktywacji spektralnej specyficznych pigmentów, wyłącznie w obrębie wysokouporządkowanej i zorientowanej nanoarchitektury tych fotokompleksów na nanokonstruktach plazmonowych. Powyższe nowatorskie podejście badawcze może być w przyszłości zastosowane do konstrukcji nowej generacji urządzeń biofotowoltaicznych o zwiększonej wydajności konwersji energii słonecznej

Enhancement of Power Output by using Alginate Immobilized Algae in Biophotovoltaic Devices.

We report for the first time a photosynthetically active algae immobilized in alginate gel within a fuel cell design for generation of bioelectricity. The algal-alginate biofilm was utilized within a biophotovoltaics (BPV) device developed for direct bioelectricity generation from photosynthesis. A peak power output of 0.289 mWm-2 with an increase of 18% in power output compared to conventional suspension culture BPV device was observed. The increase in maximum power density was correlated to the maximum relative electron transport rate (rETRm). The semi-dry type of photosynthetically active biofilm proposed in this work may offer significantly improved performances in terms of fuel cell design, bioelectricity generation, oxygen production and CO2 reduction

Graphene oxide decorated with gold enables efficient biophotovolatic cells incorporating photosystem I

This paper describes the use of reduced graphene oxide decorated with gold nanoparticles as an efficient electron transfer layer for solid-state biophotovoltic cells containing photosystem I as the sole photo-active component. Together with polytyrosine–polyaniline as a hole transfer layer, this device architecture results in an open-circuit voltage of 0.3 V, a fill factor of 38% and a short-circuit current density of 5.6 mA cm(−2) demonstrating good coupling between photosystem I and the electrodes. The best-performing device reached an external power conversion efficiency of 0.64%, the highest for any solid-state photosystem I-based photovoltaic device that has been reported to date. Our results demonstrate that the functionality of photosystem I in the non-natural environment of solid-state biophotovoltaic cells can be improved through the modification of electrodes with efficient charge-transfer layers. The combination of reduced graphene oxide with gold nanoparticles caused tailoring of the electronic structure and alignment of the energy levels while also increasing electrical conductivity. The decoration of graphene electrodes with gold nanoparticles is a generalizable approach for enhancing charge-transfer across interfaces, particularly when adjusting the levels of the active layer is not feasible, as is the case for photosystem I and other biological molecules