Source: VANDERBILT UNIVERSITY, THE submitted to NRP
NANOSCALE INTERFACING OF PHOTOSYSTEM I PROTEINS FOR SOLAR CONVERSION
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
AFRI COMPETITIVE GRANT
Reporting Frequency
Annual
Accession No.
1018975
Grant No.
2019-67021-29857
Cumulative Award Amt.
$465,000.00
Proposal No.
2018-07415
Multistate No.
(N/A)
Project Start Date
Jun 15, 2019
Project End Date
Jun 14, 2023
Grant Year
2019
Program Code
[A1511]- Agriculture Systems and Technology: Nanotechnology for Agricultural and Food Systems
Recipient Organization
VANDERBILT UNIVERSITY, THE
110 21ST AVENUE S STE 937
NASHVILLE,TN 372032416
Performing Department
Chemical and Biomolecular Eng
Non Technical Summary
Solar energy has sufficient capacity to provide abundant clean energy to our planet and finally end our reliance on fossil fuels. However, the conversion of solar energy to usable electricity is currently more expensive than our widely utilized but environmentally polluting energy sources. This project will investigate the use of abundant and renewable natural proteins, extracted from green plants and agricultural crops, as nanoscale components that will be integrated with advanced materials to produce biohybrid solar cells. This research seeks to reduce the materials and processing costs of biohybrid solar cells while introducing new innovations to improve their overall efficiencies.Photosystem I (PSI) proteins efficiently convert the light they absorb into chemical energy to drive photosynthesis in green plants and achieve the highest reducing potentials in nature. Researchers from around the world have investigated the extraction of PSI proteins from green plants and cyanobacteria and the integration of the proteins with materials to prepare biohybrid films and devices. The efficiencies of such systems have been limited by the ability to rapidly transfer electrons into and out of the active sites of PSI. This project aims to take a major step toward commercially viable biohybrid solar cells by electrically wiring PSI proteins with carbon quantum dots and conducting polymers to provide a direct conduit for the more efficient transfer of electrons into and from the active sites of PSI while increasing the light absorbed by the protein. These new PSI-wired conjugates will be easier to interface with materials and surfaces to enable the preparation of new solid-state solar cells and natural dye-sensitized solar cells that are expected to greatly surpass the performance of today's biohybrid cells. Society will ultimately benefit from this work by having access to more affordable solar cells that are processed from vastly abundant, renewable, and truly green components.
Animal Health Component
10%
Research Effort Categories
Basic
80%
Applied
10%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
13314302020100%
Knowledge Area
133 - Pollution Prevention and Mitigation;

Subject Of Investigation
1430 - Greens and leafy vegetables;

Field Of Science
2020 - Engineering;
Goals / Objectives
Photosystem I (PSI) is a nanoscale protein complex in green plants and cyanobacteria that is nearly 100% efficient with the light it captures. This project will wire the active sites of PSI to equip it for biohybrid solar energy conversion. Carbon quantum dots (CQDs) with appropriate doping will be attached to PSI's stromal and lumenal sides to function as a reservoir for electrons and holes, respectively, to provide an on-demand feed of charge to PSI's electron transfer chain. These CQDs are known to fluoresce by downshifting UV light and upshifting IR light to the visible range to effectively expand the light that PSI can absorb. Conducting polymers will be grown from PSI's donor pocket to enable vastly improved interfacing to cathodes. The PSI-wired CQDs and conducting polymers will be used as chemical handles to selectively orient PSI at nanostructured electrode surfaces that provide high surface area to elevate photocurrents. These innovations at the nanoscale will be employed into new solid-state and dye-sensitized solar cells where direct electron transfer to and from PSI conjugates will lead to efficiency-to-cost ratios, electron turn-over rates, and biohybrid efficiencies that set the standard.Objectives1. Interface PSI proteins in a side-selective manner with nanoscale particles, including carbon quantum dots.2. Grow conducting polymers directly from the P700 active site to create PSI-conducting polymer conjugates.3. Orient PSI conjugates at nanostructured surfaces.4. Fabricate solar cells that exploit PSI nanoscale interfacing for solar conversion.
Project Methods
Efforts to expand knowledge include research papers and conference presentations to the technical field, graduate and undergraduate student research mentoring, development of new curriculum, classroom presentations, and classroom assignments for undergraduate and graduate students, and outreach to K-12 students.Evaluation of project success will be based on the successful... 1) preparation of new bionanomaterials and/or conjugates with unique properties, 2) fabrication of new biohybrid solar cell designs that outperform the current state-of-the-art biohybrid cells, 3) selective orientation of these new nanobiomaterials at electrode surfaces, 4) preparation of novel nanobiomaterial interfaces with increased rates of electron transfer.

Progress 06/15/19 to 06/13/23

Outputs
Target Audience: Scientists and engineers who research: biohybrid approaches, conducting polymers, solar energy conversion, applied photosynthesis, protein electrochemistry, electrode design, and food nanotechnology. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This project has supported the research of two Ph.D. students full time, plus another student whose salary has been supported by an NSF Graduate Fellowship. One of the Ph.D. students supported on this project won 1st Place in the ePoster competition in the fall of 2020 at the International Online Conference for Biohybrid Approaches to Solar Energy Conversion, which featured 60 researchers from across the world in leading biohybrid solar research groups. The Ph.D. students are learning to incorporate Photosystem I proteins with carbon dots, porous electrodes, conducting polymers (grown by the protein itself), and water-soluble conducting polymers in a layer-by-layer manner. The project has indirectly supported at least sixundergraduate students. The Ph.D. students trained the undergraduate students in these key areas. Of the undergraduate students who worked in the past year, one is an external underrepresented minority student who participated in our NSF REU program through the Vanderbilt Institute of Nanoscale Science and Engineering. One of the VU students did his honors research on this project and published a first-author manuscript. How have the results been disseminated to communities of interest?During the project lifetime, we have published nine peer-reviewed journal articles, and another is currently in submission. I expect at least two more manuscripts to be submitted based on the work performed under this grant. The students and professors have given many presentations of their work, including at international meetings. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Accomplishments Keyed to Each Grant Objective (above) 1. Carbon dots (CDs) enable tunable electronic properties based on synthesis, and thus, demonstrate an exciting system to interface with PSI proteins.In 2020, we published a manuscript on the electrochemical and electronic properties of CDs (Stachurski et al.,Nanoscale Advances, 2, 3375-3383, 2020).In that work, we reported a citrate buffer-facilitated synthesis of nitrogen-doped carbon dots (NCD) and explored the impact of urea concentration on observed electrochemical and optical properties. Optical absorbance and quantum yield of NCDs were found to increase with the dopant concentrations present in the hydrothermal reaction mixture. Electrochemical analysis demonstrates that increased nitrogen content results in the shifting of carbon dot oxidation potentials without the need of post-synthesis surface modifications. Over the range of molar ratios of dopant-to-citrate tested, the oxidation potentials of NCDs shifted up to 150 mV towards more negative potentials. This result is important as it suggests our ability to ultimately control the electronic interface between the NCDs and other particles. Based on preliminary results in 2021 regarding the interfacing of CDs with PSI proteins, we decided to focus on the remaining aims, in particular, Aims 2 and 3, which showed more promise as high-impact projects. 2. The P700reaction center of PSI has a sufficiently high potential to oxidize some monomers. In this grant, we have shown for the first time that the P700reaction center of PSI could be utilized to grow conducting polymers directly at this active donor site (Passantino, et al.ACS Appl. Polym. Mater. 4, 7852-7858,2022).Simply exposing a solution of PSI to pyrrole monomer and illuminating with solar simulated light produced a conductive and photoactive polypyrrole-PSI composite material.Successful polymerization of pyrrole from PSI was confirmed by the combination of infrared spectroscopy, UV-vis, thermogravimetric analysis, differential scanning calorimetry, and contact angle measurements. Impressively, the resulting conjugate powder can be pressed into a porous pellet that exhibits photo-induced enhancements in its conductivity. Such an accomplishment opens the door for new strategies for the direct wiring of PSI proteins to electrodes, semiconductors, and polymers to enable more efficient biohybrid solar electrodes and devices. 3. First, we successfully published the following manuscript (Wolfe et al., Langmuir, 2021, 37, 10481-10489).This work demonstrates the successful assembly of the water-soluble conducting polymer poly(3,4-ethylenedioxythiophene)-polystyrene sulfonate followed by PSI proteins as distinct layers for films up to 9 layer pairs and 70 nm in thickness, with highly reproducible layer thicknesses and distinct changes in surface chemistry.The photocurrent performance of the LBL films increased linearly up to 6-layer pairs. The turnover number (TN) of the PSI-PEDOT:PSS LBL assemblies greatly surpasses pure, drop-casted PSI multilayer films, highlighting that the rate of electron collection is improved through the systematic deposition of the protein complexes and conducting polymer.The capability to deposit high loadings of PSI between PEDOT:PSS layers, while retaining connection to the underlying electrode, shows the value in using LBL assembly to produce PSI and PEDOT:PSS bioelectrodes for photoelectrochemical energy harvesting applications. More recently, we have developed a strategy for successfully integrating PSI with PEDOT:PSS as a fast, 1-step route to much thicker films than can be achieved by the LBL assembly route above.In short, we have mixed PSI with PEDOT:PSS in aqueous solution and used spin coatingto achieve a uniform composite film that is photoactive and electroactive. The resulting films are much smoother than drop-casted films that we and others have predominately employed. The films are electrically conductive, even with the insulating protein. Combining PSI with PEDOT:PSS results in higher photocurrents as compared to films of the pure protein or pure polymer. We show that individual proteins are more efficent at low loadings when they are surrounded by the conducting polymer. These results were published in ACS Appl. Polym. Mater., 2023, 5, 3278-3288. We have just submitted a manuscript toNanoscale Advancesthat reports a novel way of combining proteins with conducting polymers.In this approach, we drop cast a film of PSI proteins and then electropolymerize pyrrole from the electrode surface through the voids in the protein film.The resulting film is photoactive and conductive, whereas pure polypyrrole is not photoactive. In contrast with the LBL and spin coating approaches above, this approach does not yield individual proteins wrapped in conducting polymer.Rather, the polymer interfaces with PSI clusters as it snakes through the voids in the film.We have observed that the synergistic photocurrent effects that we observed for the LBL and spin coating approaches--where a combination of PSI and polymer yields photocurrents well beyond that of the pure protein or pure polymer--does not occur for this system.Importantly, this absence of synergy informs that the interfacial contact between individual PSI proteins and the polymer is critical for enhancements in quantum efficiency. 4. We demonstrated a new solar cell fabrication procedure in 2020 that is much simpler and more reproducible than any biohybrid strategies published to date.The manuscript focused on a novel gel-based, natural dye sensitized solar cell (n-DSSC) in which a PSI protein film occupies a copper cathode while a blackberry anthocyanin dye is deposited within a mesoporous TiO2anode (Passantino, et al.,ACS Appl Bio Mater, 2020).The use of an agarose gel (from seaweed) for the electrolyte medium instead of solvent or water enables much simpler preparation of the cells and improved longevity of a sustainable solar cell. The presence of PSI in the device enables the cell to achieve a maximum power conversion efficiency of 0.30% (vs 0.18% without PSI). One of the main barriers to making viable Photosystem I-based biohybrid solar cells is the need for an electrochemical pathway to facilitate electron transfer between the P700reaction center of Photosystem I and an electrode. To this end, nature provides inspiration in the form of cytochrome c6, the natural electron donor to the P700site in certain photosynthetic species. Its natural ability to access the P700binding pocket and reduce the reaction center can be mimicked by employing cytochrome c, which has a similar protein structure and redox chemistry as cytochrome c6while also being compatible with a variety of electrode surfaces. The incorporation of cytochrome c has been previously demonstrated to improve the photocurrent generation of Photosystem I-based photoactive electrodes; however, due to the need for a high areal density of protein entrapment, the approaches used to construct the biohybrid electrode are often time consuming and/or require specialized electrode preparation. In our recently published work (Than et al.,Photosynthesis Research, 2023, 155, 299-308.), we use the quick and facile vacuum-assisted drop-casting technique to construct a Photosystem I/cytochrome c photoactive composite film with micron-scale thickness. We demonstrate that this simple fabrication technique can result in high cytochrome c loading and improvement in cathodic photocurrent over a drop-casted Photosystem I film without cytochrome c. In addition, we analyze the behavior of the cytochrome c/Photosystem I system at varying applied potentials to show that the improvement in performance can be attributed to enhancement of the electron transfer rate to P700sites and therefore the PSI turnover rate within the composite film.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kody D Wolfe, Dilek Dervishogullari, Joshua M Passantino, Christopher D Stachurski, G Kane Jennings, David E Cliffel, "Improving the stability of photosystem Ibased bioelectrodes for solar energy conversion," Current Opinion in Electrochemistry, 19, 27-34, 2020.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: oshua Passantino, Kody Wolfe, Keiann Simon, David Cliffel, and G. Kane Jennings, "Photosystem I Enhances the Efficiency of a Natural, Gel-Based Dye-Sensitized Solar Cell ACS Applied Bio Materials, 3 (7), 4465-4473, 2020.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: K. D. Wolfe, A. Gargye, F. Mwambutsa, L. Than, D. E. Cliffel, and G. K. Jennings, Layer-by-Layer Assembly of Photosystem I and PEDOT:PSS Biohybrid Films for Photocurrent Generation, Langmuir, 37, 10481-10489, 2021.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kody D Wolfe, Dilek Dervishogullari, Christopher D Stachurski, Joshua M Passantino, G Kane Jennings, David E Cliffel, "Photosystem I Multilayers within Porous Indium Tin Oxide Cathodes Enhance Mediated Electron Transfer," ChemElectroChem, 7, 595-603, 2020.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Chris Stachurski, G. Kane Jennings, David Cliffel, "Optical and Electrochemical Tuning of Hydrothermally Synthesized Nitrogen-Doped Carbon Dots" Nanoscale Advances, 2 (8), 3375-3383, 2020.
  • Type: Journal Articles Status: Published Year Published: 2022 Citation: J. M. Passantino, A. Williams, D. E. Cliffel, and G. K. Jennings, "Photooxidative Polymerization from Photosystem I Proteins," ACS Applied Polymer Materials 4 (10), 7852-7858, 2022.
  • Type: Journal Articles Status: Published Year Published: 2023 Citation: L. Than, K.D. Wolfe, D.E. Cliffel, and G. K. Jennings, "Drop-casted Photosystem I/cytochrome c multilayer films for biohybrid solar energy conversion," Photosynthesis Research 155 (3), 299-308, 2023.
  • Type: Journal Articles Status: Published Year Published: 2023 Citation: C. D. Stachurski, J. M. Williams, P. M. Tabaquin, E.D. Wood, N. Phambu, G. K. Jennings, and D. E. Cliffel, "Utilizing Toray Paper as a Metal?Free, High Surface Area Electrode for Photosystem IDriven Mediated Electron Transfer," Energy Technology 11 (4), 2201077, 2023.
  • Type: Journal Articles Status: Published Year Published: 2023 Citation: M. A Nabhan, C. A. Silvera Batista, D. E. Cliffel, and G. K. Jennings, "Spin Coating Photoactive Photosystem IPEDOT: PSS Composite Films," ACS Applied Polymer Materials 5 (5), 3278-3288, 2023.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Avi Gargye, Faustin Mwambutsa, and Kane Jennings, "Layer-By-Layer Films of Photosystem I and Conducting Polymers" Amer. Inst. of Chemical Engineers Annual Meeting, Undergraduate Poster Session, November, 2019
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Dilek Dervishogullari, Kody Wolfe, Christopher Stachurski, G Kane Jennings, David E Cliffel, "Multilayer Photosystem I Films within Porous Indium Tin Oxide Cathodes for Enhanced Photocurrent Generation," The Electrochemical Society Meeting, 2019.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Christopher Stachurski, Dilek Dervishogullari, Jade Stanley, Kody Wolfe, G Kane Jennings, David E Cliffel, "Photosystem I-Modified Multi-Walled Carbon Nanotube Anodes for Enhanced Solar Energy Conversion," The Electrochemical Society Meeting, 2019.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Christopher Stachurski, G Kane Jennings, David Cliffel, "Synthesis of nitrogen-doped carbon dots as charge transport materials for photosystem I-based biohybrid photovoltaics," Abstracts of the American Chemical Society Meeting, vol 258, August, 2019.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2020 Citation: Kody Wolfe, Dilek Dervishogullari, Christopher Stachurski, Joshua Passantino, G Kane Jennings, David E Cliffel, Electron Transfer at Photosystem I-Electrode Interfaces: Porous & Translucent Indium Tin Oxide Cathodes, Electrochemical Society Meeting, 2020.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2020 Citation: Joshua Passantino, Kody Wolfe, Keiann Simon, David E. Cliffel and G. Kane Jennings, "Photosystem I Integration in Natural, Two-Electrode, Gel-Based Dye-Sensitized Solar Cells," ePoster presentation, International Online Conference for Biohybrid Approaches to Solar Energy Conversion, 2020.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2020 Citation: Wolfe, K. D.; Gargye, A.; Than, L.; Cliffel, D. E.; Jennings, G. K. Electrostatic Interactions Between Photosystem I and PEDOT:PSS Enable Layer-by-Layer Assembly ePoster Presentation  International Online Conference on Bio-hybrid Approaches to Solar Energy Conversion, October 2020
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: G. K. Jennings, Biohybrid Solar Energy Conversion with Photosystem I Proteins, University of Oklahoma, Department of Chemical and Materials Engineering, October, 2021. (Seminar)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: J. Passantino, D. E. Cliffel, G. K. Jennings, Electropolymerization of Pyrrole by Photosystem I Proteins, AIChE Annual Meeting, Boston, November, 2021.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: L. Than, D. E. Cliffel, and G. K. Jennings, Mixed Photosystem I and Cytochrome C Films for Biohybrid Solar Energy Conversion, AIChE Annual Meeting, Boston, November, 2021.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: M. A. Nabhan, C. A. S. Batista, D. E. Cliffel, and G. K. Jennings. Spin Coating Photoactive Photosystem I-PEDOT:PSS Composite Films " 2022 Nanoscale Science and Engineering for Agriculture and Food Systems, Gordon Research Conference Jun-19-2022 - Jun-24-2022 Southern New Hampshire University in New Hampshire
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: J. M. Passantino, A. M. Williams, M. A. Nabhan, D. E. Cliffel, and G. K. Jennings. Photooxidative Polymerization of Pyrrole from Photosystem I Proteins, 2022 AIChE Annual Meeting in Phoenix, AZ November 14-17, 2022.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: M. A. Nabhan, C. A. S. Batista, D. E. Cliffel, and G. K. Jennings. Spin Coating Photoactive Photosystem I-PEDOT:PSS Composite Films 2022 AIChE Annual Meeting in Phoenix, AZ November 14-17, 2022.
  • Type: Theses/Dissertations Status: Published Year Published: 2021 Citation: K. D. Wolfe, "Electron Transfer at Biologically Modified Electrodes," Ph.D. Dissertation in Interdisiplinary Materials Science, Vanderbilt University, August, 2021.
  • Type: Theses/Dissertations Status: Published Year Published: 2021 Citation: C. D. Stachurski, "Development of Carbon Materials for Use in Photosystem I-Based Biohybrid Devices," Ph.D. Dissertation in Chemistry, Vanderbilt University, August, 2021.
  • Type: Theses/Dissertations Status: Published Year Published: 2022 Citation: L. V. Than, Mixed Photosystem I and Cytochrome C Films for Biohybrid Solar Energy Conversion, Bachelors Honors Thesis in Chemistry, Vanderbilt University, May, 2022.
  • Type: Theses/Dissertations Status: Published Year Published: 2022 Citation: John Williams, "Novel Biohybrid Photovoltaics for Expeditionary Energy," Ph.D. Dissertation in Interdisiplinary Materials Science, Vanderbilt University, May, 2022.
  • Type: Theses/Dissertations Status: Published Year Published: 2022 Citation: J. M. Passantino, "Targeted Electrochemical Reactions at the Active Sites of the Photosystem I Protein Complex," Ph.D. Dissertation in Chemical Engineering, Vanderbilt University, March, 2022.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2023 Citation: D.E. Cliffel, "Photosystem I Biohybrid Energy Conversion: Moving from Photoelectrochemistry to Solid-State Devices?" Biophotoelectrochemical Systems Workshop, Cambridge, UK, April, 2023.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: G. K. Jennings, "Integrating Plant Proteins with Polymers and Electrodes to Explore Biohybrid Solar Energy Conversion," Lehigh University, Department of Chemical Engineering, September, 2022. (seminar)
  • Type: Journal Articles Status: Submitted Year Published: 2023 Citation: J. M. Passantino, B. A. Christiansen, M. A. Nabhan, Z. J. Parkerson, T. D. Oddo, D. E. Cliffel, and G. K. Jennings, "Photoactive and Conductive Biohybrid Films by Polymerization of Pyrrole through Voids in Photosystem I Multilayer Films," Nanoscale Advances, submitted.


Progress 06/15/21 to 06/14/22

Outputs
Target Audience: Scientists and engineers who research: biohybrid approaches, conducting polymers, solar energy conversion, applied photosynthesis, protein electrochemistry, and electrode design Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?In the past year, four Ph.D. students involved in this project have successfully defended their theses (Chris Stachurski, Kody Wolfe, Josh Passantion, and John Williams). All were supported by the grant to an extent. Two were fully supported by this grant, one had salary and tuition support from an NSF graduate fellowship, and one had salary and tuition support from the US Army. Two are gainfully employed, one is transitioning to a job in the Army, and one is still in his job search. All these students learned to integrate Photosystem I proteins with other materials, including carbon dots and electrodes, carbon paper, conducting polymers, and gel-based photoelectrochemical cells. This past year, USDA funds helped support the entrepreneurship drive and passion for innovation of one of our graduate students, Marc Nabhan. Through a year long innovation realization class, Marc collaborated with JD and MBA students to explore avenues of commercializing Photosystem I-based technologies, an effort to translate his PhD thesis into a viable product tailored towards military applications. With the intention of being a liaison between science and the community, Marc drafted a proposal for the NSF Small Business Innovation Research (SBIR) program, improving his grant writing skills and teaching him the intricacies of funding applications. Marc also managed to receive a $2300 NSF microgrant that was awarded to him through Vanderbilt's center for innovation and design, the Wond'ry. With these funds, the student had a chance to participate in the Energy and Water Expo 2021, where he discussed his research and garnered valuable insights on the current state of energy innovation on a global scale, while networking with some of the industry leaders within his field of work. Five undergraduate students worked on this project in the past year alone. Three were Vanderbilt students and two were underrepresented minority students through the VINSE NSF REU program. One of the Vanderbilt students (Long Viet Than) successfully completed his dual degree in Chemical Engineering and Chemistry, with highest honors in Chemistry based on his Honors Dissertation on the electrode design with PSI and Cytochrome C proteins. He is first author on a manuscript to be submitted very soon. How have the results been disseminated to communities of interest? In the past year, we have published one manuscript on this project, with another that was submitted in early 2022 and is now in revision. For the entire project so far, we have published five manuscripts with one in revision, and at least four others to be submitted as we approach the NCE year. We or our students have also given at least three conference presentations in the past year. What do you plan to do during the next reporting period to accomplish the goals?1) Finish detailed SDS-PAGE characterization of PSI-polypyrrole conjugates and resubmit manuscript. 2) Examine PSI's ability to photopolymerize other monomers, continuing work with p-anisidine and o-anisidine. Perform detailed spectroscopic and SDS-PAGE characterization. 3) Complete detailed solution characterization of PSI-PEDOT:PSS interactions, including with analytical ultracentrifuge, and submit manuscript. 4) Investigate the use of PSI conjugates in a gel-based dye-sensitized solar cell. 5) Complete final stages of work on surface electropolymerization of pyrrole through the interstitial spaces of a PSI film to present a new method for composite, photoactive, conductive films.

Impacts
What was accomplished under these goals? Accomplishments Keyed to Each Grant Objective: 1. Interface Photosystem I (PSI) proteins in a side-selective manner with nanoscale particles, including carbon quantum dots. Carbon dots (CDs) enable tunable electronic properties based on synthesis, and thus, demonstrate an exciting system to interface with PSI proteins. In 2020, we published a manuscript on the electrochemical and electronic properties of CDs (Stachurski et al., Nanoscale Advances, 2, 3375-3383, 2020). Based on preliminary results in 2021 regarding the interfacing of CDs with PSI proteins, we have decided to focus on the remaining aims, in particular, Aim 2, which is showing more promise as a high-impact project. 2. Grow conducting polymers directly from the P700 active site to create PSI-conducting polymer conjugates. The P700 reaction center of PSI has the requisite formal potential to oxidize some monomers. Thus, we have proposed that the P700 reaction center of PSI could be utilized to grow conducting polymers directly at this active donor site. Such an accomplishment would enable new strategies for the direct wiring of oriented PSI proteins to electrodes, semiconductors, and polymers to enable more efficient biohybrid solar electrodes and devices. We have a manuscript in revision with the following key findings: The oxidative ability of the P700 reaction site of the protein is less studied than the reductive capabilities of the FB reaction site. We have shown that the oxidation potential of P700 is robust enough to initiate an oxidative polymerization of the redox monomer, pyrrole. This manuscript reports the first photoactive and conductive protein-polymer conjugate, which is accomplished by using extracted, unmodified PSI protein to perform the polymerization. The polymerization technique consists of adding monomer and a dopant to a solution of PSI and illuminating the sample with simulated sunlight. Successful polymerization of pyrrole from PSI is confirmed by the combination of infrared spectroscopy, UV-vis, thermogravimetric analysis, differential scanning calorimetry, and contact angle measurements. Conjugation between the protein and polymer is indicated by SDS-PAGE and is further supported by photoelectrochemical properties that differ from either PSI or polypyrrole alone. Impressively, the resulting conjugate powder can be pressed into a porous pellet that exhibits photo-induced enhancements in its conductivity. We are also investigating the PSI-induced photopolymerization of other monomers, including p- and o-anisidine. Each of these has low enough oxidation potentials to be polymerized by the P700 reaction center of PSI. Preliminary evidence shows infrared spectra and thermogravimetric curves that are consistent with the combination of PSI and conducting polymer. 3. Orient PSI conjugates at nanostructured surfaces. As we are still making and characterizing the conjugates, we have not yet explored their orientational attachment at different surfaces. Nonetheless, we have made major progress on two other projects that involve interfacing PSI directly with conducting polymers. First, we successfully published the following manuscript (Wolfe et al., "Layer-by-Layer Assembly of Photosystem I and PEDOT:PSS Biohybrid Films for Photocurrent Generation," Langmuir, 2021, 37, 10481-10489. This work demonstrates the successful assembly of the water-soluble conducting polymer poly(3,4-ethylenedioxythiophene)-polystyrene sulfonate followed by PSI proteins as distinct layers for films up to 9 layer pairs and 70 nm in thickness, with highly reproducible layer thicknesses and distinct changes in surface chemistry. The photocurrent performance of the LBL films increased linearly up to 6-layer pairs. The turnover number (TN) of the PSI-PEDOT:PSS LBL assemblies greatly surpasses pure, drop-casted PSI multilayer films, highlighting that the rate of electron collection is improved through the systematic deposition of the protein complexes and conducting polymer. The capability to deposit high loadings of PSI between PEDOT:PSS layers, while retaining connection to the underlying electrode, shows the value in using LBL assembly to produce PSI and PEDOT:PSS bioelectrodes for photoelectrochemical energy harvesting applications. In another strategy for successfully integrating PSI with PEDOT:PSS, we have developed a process to make well-mixed thin composite films via spin coating, which allows for uniform and rapid film formation where the composition and thickness of composite films can be readily tuned. We have assessed the composition, thickness, conductivity, scalability, and photoactivity of the resulting biohybrid PSI-polymer films. The combination of the protein and the polymer yields vastly increased photocurrents as compared to single-component films of the protein or polymer alone. This work is near submission, as of mid May, 2022. 4. Fabricate solar cells that exploit PSI nanoscale interfacing for solar conversion. We demonstrated a new solar cell fabrication procedure in 2020 that is much simpler and more reproducible than any biohybrid strategies published to date. The manuscript focused on a novel gel-based, natural dye sensitized solar cell (n-DSSC) in which a PSI protein film occupies a copper cathode while a blackberry anthocyanin dye is deposited within a mesoporous TiO2 anode (Passantino, et al., ACS Appl Bio Mater, 2020). The use of an agarose gel (from seaweed) for the electrolyte medium instead of solvent or water enables much simpler preparation of the cells and improved longevity of a sustainable solar cell. The presence of PSI in the device enables the cell to achieve a maximum power conversion efficiency of 0.30% (vs 0.18% without PSI). We plan to use this versatile gel-cell architecture, paired with unique electrodes and the conjugates described in Aim 2, to fabricate new biohybrid solar cells. The biomimetic electrode design described below is also a candidate for investigating in this cell architecture. One of the main barriers to making viable Photosystem I-based biohybrid solar cells is the need for an electrochemical pathway to facilitate electron transfer between the P700 reaction center of Photosystem I and an electrode. To this end, nature provides inspiration in the form of cytochrome c6, the natural electron donor to the P700 site in certain photosynthetic species. Its natural ability to access the P700 binding pocket and reduce the reaction center can be mimicked by employing cytochrome c, which has a similar protein structure and redox chemistry while also being compatible with a variety of electrode surfaces. The incorporation of cytochrome c has been previously demonstrated to improve the photocurrent generation of Photosystem I-based photoactive electrodes; however, due to the need for a high areal density of protein entrapment, the approaches used to construct the biohybrid electrode are often time consuming and/or require specialized electrode preparation. In our recent work, we use the quick and facile vacuum-assisted drop-casting technique to construct a Photosystem I/cytochrome c photoactive composite film with micron-scale thickness. We demonstrate that this simple fabrication technique can result in high cytochrome c loading and improvement in cathodic photocurrent over a drop-casted Photosystem I film without cytochrome c. In addition, we analyze the behavior of the cytochrome c/Photosystem I system at varying applied potentials to show that the improvement in performance can be attributed to enhancement of the electron transfer rate to P700 sites and therefore the PSI turnover rate within the composite film. This work is nearing submission.

Publications

  • Type: Journal Articles Status: Published Year Published: 2021 Citation: K. D. Wolfe, A. Gargye, F. Mwambutsa, L. Than, D. E. Cliffel, and G. K. Jennings, Layer-by-Layer Assembly of Photosystem I and PEDOT:PSS Biohybrid Films for Photocurrent Generation, Langmuir, 37, 10481-10489, 2021.
  • Type: Journal Articles Status: Under Review Year Published: 2022 Citation: J. M. Passantino, A. Williams, D. E. Cliffel, and G. K. Jennings, "Oxidative Polymerization from Photosystem I Proteins," Biomacromolecules, in revision, 2022.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: G. K. Jennings, Biohybrid Solar Energy Conversion with Photosystem I Proteins, University of Oklahoma, Department of Chemical and Materials Engineering, October, 2021. (Seminar)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: J. Passantino, D. E. Cliffel, G. K. Jennings, Electropolymerization of Pyrrole by Photosystem I Proteins, AIChE Annual Meeting, Boston, November, 2021.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: L. Than, D. E. Cliffel, and G. K. Jennings, Mixed Photosystem I and Cytochrome C Films for Biohybrid Solar Energy Conversion, AIChE Annual Meeting, Boston, November, 2021.
  • Type: Theses/Dissertations Status: Published Year Published: 2022 Citation: J. M. Passantino, "Targeted Electrochemical Reactions at the Active Sites of the Photosystem I Protein Complex," Ph.D. Dissertation in Chemical Engineering, Vanderbilt University, March, 2022.
  • Type: Theses/Dissertations Status: Published Year Published: 2021 Citation: K. D. Wolfe, "Electron Transfer at Biologically Modified Electrodes," Ph.D. Dissertation in Interdisiplinary Materials Science, Vanderbilt University, August, 2021.
  • Type: Theses/Dissertations Status: Published Year Published: 2021 Citation: C. D. Stachurski, "Development of Carbon Materials for Use in Photosystem I-Based Biohybrid Devices," Ph.D. Dissertation in Chemistry, Vanderbilt University, August, 2021.
  • Type: Theses/Dissertations Status: Published Year Published: 2022 Citation: L. V. Than, Mixed Photosystem I and Cytochrome C Films for Biohybrid Solar Energy Conversion, Bachelors Honors Thesis in Chemistry, Vanderbilt University, May, 2022.
  • Type: Theses/Dissertations Status: Published Year Published: 2022 Citation: John Williams, "Novel Biohybrid Photovoltaics for Expeditionary Energy," Ph.D. Dissertation in Interdisiplinary Materials Science, Vanderbilt University, May, 2022.


Progress 06/15/20 to 06/14/21

Outputs
Target Audience: (1) Scientists and engineers who research: biohybrid approaches, conducting polymers, solar energy conversion, applied photosynthesis, protein electrochemistry, and electrode design (2) 90 first-year engineering students at Vanderbilt University who learned to make a Photosystem I-driven dye sensitized solar cell and explain how it works. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has supported the research of two Ph.D. students full time for the past year, plus another student whose salary has been supported by an NSF Graduate Fellowship. One of the Ph.D. students supported on this project one 1st Place in the ePoster competition in the fall of 2020 at the International Online Conference for Biohybrid Approaches to Solar Energy Conversion, which featured 60 researchers from across the world in leading biohybrid solar research groups. The Ph.D. students are learning to incorporate Photosystem I proteins with carbon dots, porous electrodes, conducting polymers (grown by the protein itself), and water-soluble conducting polymers in a layer-by-layer manner. The project has indirectly supported four undergraduate students. The Ph.D. students are training the undergraduate students in these key areas. Of the undergraduate students who worked in the past year, three were Vanderbilt students and one is an external underrepresented minority student who participated in our NSF REU program through the Vanderbilt Institute of Nanoscale Science and Engineering. One of the VU students is doing his honors research on this project. How have the results been disseminated to communities of interest?In the past year, we have published two manuscripts on this project, with another that was submitted in May of 2021. For the entire project so far, we have published four manuscripts with one submitted. We or our students have also given seven conference presentations. What do you plan to do during the next reporting period to accomplish the goals?1. Exploit the PSI-photocatalyzed growth of polypyrrole conducting polymer in solution (see Accomplishments above) to create novel classes of biohybrid electrodes and protein-polymer conjugates. 2. Continue ongolng strategies for direct wiring to PSI active sites, including PSI-carbon dot, PSI-conducting polymer, and PSI-Cyt c conjugates on nanostructured electrodes, such as the macroporous ITO we have already developed and published on this project. 3. Develop more rapid processing to deposit composite PSI films that will be used to improve biohybrid solar cell performance. In the past year, we have impressive progress in spincoating uniform PSI-PEDOT/PSS composite films in which the ratio of PSI to conducting polymer and the film thickness is easily controlled. We envision that these unique hybrid films will be useful to fabricate solid-state solar cells in which the conducting polymer serves as a hole transport layer for PSI.

Impacts
What was accomplished under these goals? Accomplishments Keyed to Each Grant Objective: 1. Interface Photosystem I (PSI) proteins in a side-selective manner with nanoscale particles, including carbon quantum dots. Carbon dots (CDs) enable tunable electronic properties based on synthesis, and thus, demonstrate an exciting system to interface with PSI proteins. Before interfacing PSI proteins with CDs, we have sought to understand the electrochemical and electronic properties of the CDs, as summarized in our 2020 manuscript (Stachurski et al., Nanoscale Advances, 2, 3375-3383, 2020). In that work, we reported a citrate buffer-facilitated synthesis of nitrogen-doped carbon dots (NCD) and explored the impact of urea concentration on observed electrochemical and optical properties. Optical absorbance and quantum yield of NCDs were found to increase with the dopant concentrations present in the hydrothermal reaction mixture. Electrochemical analysis demonstrates that increased nitrogen content results in the shifting of carbon dot oxidation potentials without the need of post-synthesis surface modifications. Over the range of molar ratios of dopant-to-citrate tested, the oxidation potentials of NCDs shifted up to 150 mV towards more negative potentials. This result is important as it suggests our ability to ultimately control the electronic interface between the NCDs and our PSI proteins when we combine these exciting nanomaterials. Experiments are underway to attach the CDs to Photosystem I proteins using peptide chemistry. 2. Grow conducting polymers directly from the P700 active site to create PSI-conducting polymer conjugates. The P700 reaction center of PSI has the requisite formal potential to oxidize some monomers. Thus, we have proposed that the P700 reaction center of PSI could be utilized to grow conducting polymers directly at this active donor site. Such an accomplishment would enable new strategies for the direct wiring of oriented PSI proteins to electrodes, semiconductors, and polymers to enable more efficient biohybrid solar electrodes and devices. To date, we have shown that PSI proteins in the presence of pyrrole along with an oxidant and broad spectrum simulated sunlight, produce polypyrrole in significant quantities to greatly alter the visual properties of the solution. In the absence of PSI proteins, the conducting polymer is not formed. Evidence for the growth of the polymer include infrared spectra that show peaks corresponding to chemical bonds in both the protein and the polymer. The hybrid complexed material shows mild electrical conductivity. Dialysis of the solution removes unreacted pyrrole but not the conducting polymer. In fact, our attempts to separate the protein from the polymer so far have been unsuccessful, suggesting that the conducting polymer is covalently attached/connected to the protein, presumably near the P700 active site. A comprehensive suite of electrochemical measurements are underway to characterize the electronic interconnections between the protein and polymer and explore how these hybrid materials can be best applied in photoelectrochemical devices. As another strategy toward coupling PSI with conducting polymers, we are developing a novel route to deposit composite films of PSI and poly(3,4-ethylenedioxythiophene)-polystyrene sulfonate (PEDOT:PSS) by mixing the protein and water-soluble conducting polymer in solution prior to spin coating. The resulting films are uniform, and the thickness can be controlled by spin speed. This approach represents a major advance beyond drop casting, which typically yields films that are thicker at the edges than at the middle. The ratio of protein to conducting polymer in the film is easily adjusted by altering the ratio of the two components. In addition, the films can be cast within a minute, indicating compatibility of this method with advanced materials processing. 3. Orient PSI conjugates at nanostructured surfaces. While the orientation of PSI conjugates is on hold until we have developed the optimal strategies to produce the conjugates (see Objectives 1 and 2), we have developed two approaches during the course of the grant for (1) the incorporation of multilayered PSI films at nanostructured surfaces that I reported in last year's report (see Wolfe et al., ChemElectroChem, 7, 596-603, 2020) and in more recent news, (2) the assembly of Photosystem I and conducting polymer films in a layer-by-layer manner (Wolfe et al., Langmuir, submitted). For the layer-by-layer work, we have assembled the water-soluble conducting polymer PEDOT:PSS followed by PSI proteins as distinct layers for films up to 9 layer pairs and 70 nm in thickness, with highly reproducible layer thicknesses and distinct changes in surface chemistry. When tested in an electrochemical cell employing ubiquinone-0 as a mediator, the photocurrent performance of the LBL films increased linearly by 83 ± 6 nA/cm2 per layer up to 6-layer pairs. 6-layer pair samples yielded a photocurrent of 414 ± 13 nA/cm2, after which the achieved photocurrent diminished with additional layer pairs. The turnover number (TN) of the PSI-PEDOT:PSS LBL assemblies also greatly outperforms drop-casted PSI multilayer films, highlighting that the rate of electron collection is improved through the systematic deposition of the protein complexes and conducting polymer. The capability to deposit high loadings of PSI between PEDOT:PSS layers, while retaining connection to the underlying electrode, shows the value in using LBL assembly to produce PSI and PEDOT:PSS bioelectrodes for photoelectrochemical energy harvesting applications. As another approach to PSI orientation, we are investigating electron transfer to the protein Cytochrome c (Cyt c), which serves as the natural donor to Photosystem I in some organisms. Cyt c has a redox potential that is optimally positioned to donate electrons to the P700 reaction center of PSI. It is also much smaller than PSI, so it can fit within the lumenal pocket and it would have far greater coverage in terms of moles per area to receive electrons from the electrode. To date, we have shown that we can achieve reversible electron transfer to Cyt c monolayers on an electrode, but our longer-term goal is to use Cyt c as a protein wire into PSI proteins. 4. Fabricate solar cells that exploit PSI nanoscale interfacing for solar conversion. We took a step toward the objective in 2020 when we published work on a novel gel-based, natural dye sensitized solar cell (n-DSSC) in which a PSI protein film occupies a copper cathode while a blackberry anthocyanin dye is deposited within a mesoporous TiO2 anode (Passantino, et al., ACS Appl Bio Mater, 2020). This manuscript had not been published when I submitted the report last year. The use of an agarose gel (from seaweed) for the electrolyte medium instead of solvent or water enables much simpler preparation of the cells and improved longevity of a sustainable solar cell. The presence of PSI in the device enables the cell to achieve a maximum instantaneous power conversion efficiency of 0.30% (vs 0.18% without PSI) and a steady-state power conversion efficiency of 0.042% (vs 0.028% without PSI). In the current year, we are using this versatile gel-cell architecture, paired with unique electrodes, to fabricate new biohybrid solar cells. For example, using our polypyrrole-PSI hybrid complexes on an electrode surface within a gel cell would be a way to take advantage of the direct wiring of PSI complexes in an actual 2-electrode device. Also, using layer-by-layer films of PSI with PEDOT:PSS or PSI-Cyt c composite films would enable alternative cell designs.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kody D Wolfe, Dilek Dervishogullari, Christopher D Stachurski, Joshua M Passantino, G Kane Jennings, David E Cliffel, "Photosystem I Multilayers within Porous Indium Tin Oxide Cathodes Enhance Mediated Electron Transfer," ChemElectroChem, 7, 595-603, 2020.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kody D Wolfe, Dilek Dervishogullari, Joshua M Passantino, Christopher D Stachurski, G Kane Jennings, David E Cliffel, "Improving the stability of photosystem Ibased bioelectrodes for solar energy conversion," Current Opinion in Electrochemistry, 19, 27-34, 2020.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Joshua Passantino, Kody Wolfe, Keiann Simon, David Cliffel, and G. Kane Jennings, "Photosystem I Enhances the Efficiency of a Natural, Gel-Based Dye-Sensitized Solar Cell ACS Applied Bio Materials, 3, 4465-4473, 2020.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Chris Stachurski, G. Kane Jennings, David Cliffel, "Optical and Electrochemical Tuning of Hydrothermally Synthesized Nitrogen-Doped Carbon Dots" Nanoscale Advances,2, 3375-2283, 2020.
  • Type: Journal Articles Status: Submitted Year Published: 2021 Citation: Kody D. Wolfe, Avi Gargye, Faustin Mwambutsa, Long Than, David E. Cliffel, G. Kane Jennings, "Layer-by-Layer Assembly of Photosystem I and Poly(3,4-ethylenedioxythiophene)-Polystyrene Sulfonate (PEDOT:PSS) Biohybrid Films for Photocurrent Generation," Langmuir, submitted, 2021.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Avi Gargye, Faustin Mwambutsa, and Kane Jennings, "Layer-By-Layer Films of Photosystem I and Conducting Polymers" Amer. Inst. of Chemical Engineers Annual Meeting, Undergraduate Poster Session, November, 2019.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Dilek Dervishogullari, Kody Wolfe, Christopher Stachurski, G Kane Jennings, David E Cliffel, "Multilayer Photosystem I Films within Porous Indium Tin Oxide Cathodes for Enhanced Photocurrent Generation," The Electrochemical Society Meeting, 2019.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Christopher Stachurski, Dilek Dervishogullari, Jade Stanley, Kody Wolfe, G Kane Jennings, David E Cliffel, "Photosystem I-Modified Multi-Walled Carbon Nanotube Anodes for Enhanced Solar Energy Conversion," The Electrochemical Society Meeting, 2019.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Christopher Stachurski, G Kane Jennings, David Cliffel, "Synthesis of nitrogen-doped carbon dots as charge transport materials for photosystem I-based biohybrid photovoltaics," Abstracts of the American Chemical Society Meeting, vol 258, August, 2019.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2020 Citation: Kody Wolfe, Dilek Dervishogullari, Christopher Stachurski, Joshua Passantino, G Kane Jennings, David E Cliffel, Electron Transfer at Photosystem I-Electrode Interfaces: Porous & Translucent Indium Tin Oxide Cathodes, Electrochemical Society Meeting, 2020.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2020 Citation: Joshua Passantino, Kody Wolfe, Keiann Simon, David E. Cliffel and G. Kane Jennings, "Photosystem I Integration in Natural, Two-Electrode, Gel-Based Dye-Sensitized Solar Cells," ePoster presentation, International Online Conference for Biohybrid Approaches to Solar Energy Conversion, 2020.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2020 Citation: Wolfe, K. D.; Gargye, A.; Than, L.; Cliffel, D. E.; Jennings, G. K. Electrostatic Interactions Between Photosystem I and PEDOT:PSS Enable Layer-by-Layer Assembly ePoster Presentation  International Online Conference on Bio-hybrid Approaches to Solar Energy Conversion, October 2020


Progress 06/15/19 to 06/14/20

Outputs
Target Audience:(1) Scientists and engineers who research: biohybrid approaches, solar energy conversion, applied photosynthesis, protein electrochemistry, and electrode design (2) Over 90 first-year engineering students at Vanderbilt University who learned to assemble a Photosystem I-driven dye sensitized solar cell. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has supported the research of two Ph.D. students and three undergraduate students. The Ph.D. students are learning to incorporate Photosystem I proteins with carbon dots, porous electrodes, conducting polymers (grown by the protein itself), and gels. Also, the Ph.D. students are training the undergraduate students in these key areas. Of the undergraduate students, one was a Vanderbilt student and two were external underrepresented minority students who participated in our NSF REU program through the Vanderbilt Institute of Nanoscale Science and Engineering. How have the results been disseminated to communities of interest?We have published three papers related to this project in the past year, as detailed in the Products section. We have also given several conference presentations. What do you plan to do during the next reporting period to accomplish the goals?1. Begin to incorporate the carbon dots we have made, characterized, and published with PSI proteins through linking chemistry described in our proposal. 2. Use the PSI-photocatalyzed generation of conducting polymers in solution (see Accomplishments above) to make PSI-conducting polymer films and nanoscale conjugates. 3. Orient the PSI-carbon dot and PSI-conducting polymer conjugates on nanostructured electrodes, such as the macroporous ITO we have developed, as described in Accomplishments. 4. Continue to develop new ways to fabricate composite PSI films that will be used to improve biohybrid solar cell performance. For example, we have recently succeeded in spincoating a PSI-PEDOT/PSS composite film in which the ratio of PSI to polymer is easily controlled. We envision that these will be useful to fabricate solid-state solar cells in which the conducting polymer serves as a hole transport layer for PSI.

Impacts
What was accomplished under these goals? Accomplishments Keyed to Each Grant Objective: 1. Interface Photosystem I (PSI) proteins in a side-selective manner with nanoscale particles, including carbon quantum dots. Carbon dots (CDs) enable tunable electronic properties based on synthesis, and thus, demonstrate an exciting system to interface with PSI proteins. Before interfacing PSI proteins with CDs, we have sought to understand the electrochemical and electronic properties of the CDs, as summarized from a manuscript that is currently in revision (Stachurski et al., Nanoscale Advances, in revision). Here, we report a citrate buffer-facilitated synthesis of nitrogen-doped carbon dots (NCD) and explore the impact of urea concentration on observed electrochemical and optical properties. Optical absorbance and quantum yield of NCDs were found to increase with the dopant concentrations present in the hydrothermal reaction mixture. Electrochemical analysis demonstrates that increased nitrogen content results in the shifting of carbon dot oxidation potentials without the need of post-synthesis surface modifications. Over the range of molar ratios of dopant-to-citrate tested, the oxidation potentials of NCDs shifted up to 150 mV towards more negative potentials. This result is important as it suggests our ability to ultimately control the electronic interface between the NCDs and our PSI proteins when we combine these exciting nanomaterials. 2. Grow conducting polymers directly from the P700 active site to create PSI-conducting polymer conjugates. The P700 reaction center of PSI has the requisite formal potential to oxidize some monomers. Thus, we have proposed that the P700 reaction center of PSI could be utilized to grow conducting polymers directly at this active donor site. Such an accomplishment would enable new strategies for the direct wiring of oriented PSI proteins to electrodes, semiconductors, and polymers to enable more efficient biohybrid solar electrodes and devices. We have begun to explore the growth of polyaniline and polypyrrole from PSI proteins by exposure of the monomer and an oxidizing agent to the PSI proteins in solution. Key results obtained to date are as follows: (1) Both aniline and pyrrole are polymerized in bulk quantities from solution when exposed to Photosystem I proteins and an oxidant, whereas much lower amounts are polymerized when the monomer is exposed to oxidant without PSI. (2) In the case of polyaniline, a different form of the polymer is grown in light versus in dark. (3) A conductive pellet containing PSI and polypyrrole was obtained. In the coming year, we will seek to gain a greater control over this PSI-initiated polymerization reaction to produce nanoscale PSI-conducting polymer conjugates as well as ultrathin films with PSI entrapped by conducting polymer. 3. Orient PSI conjugates at nanostructured surfaces. While orientation of PSI conjugates must wait until we have developed the optimal strategies to produce the conjugates (see Objectives 1 and 2), we have made important advances in the incorporation of multilayered PSI films at nanostructured surfaces (see Wolfe et al., ChemElectroChem, 7, 596-603, 2020). Briefly, we have loaded indium tin oxide mesoporous and macroporous electrodes with PSI multilayers. Because ITO is ubiquitous in solar cells due to its transparent conductive abilities, we have focused on developing porous ITO electrodes for integration of PSI. For the macroporous electrode with regular 5 micron pores, PSI loads onto the electrode surface throughout the porosity and yields photocurrents that are three times greater than for those by PSI in mesoporous electrodes and 40x greater than those for PSI on a flat ITO electrode. The reason for this difference in performance is that PSI is too large to be incorporated throughout the mesoporous electrode, and thus, the surface area of the mesoporous electrode is not utilized as well as it is for the macroporous system. 4. Fabricate solar cells that exploit PSI nanoscale interfacing for solar conversion. As a step toward the objective, we have developed a new gel-based, natural dye sensitized solar cell (n-DSSC) in which a PSI protein film occupies a copper cathode while a blackberry anthocyanin dye is deposited within a mesoporous TiO2 anode (Passantino, et al., ACS Appl Bio Mater., in press). The use of an agarose gel (from seaweed) for the electrolyte medium instead of solvent or water enables much simpler preparation of the cells and improved longevity of a sustainable solar cell. The presence of PSI on the cathode causes a higher concentration of oxidized species to be present near the cathode and thereby ramps up the limiting current of the cell. This enhancement owes to PSI's light-driven asymmetric redox kinetics with the mediator (oxidation of the mediator by PSI is much faster than its reduction). The presence of PSI in the device enables the cell to achieve a maximum instantaneous power conversion efficiency of 0.30% (vs 0.18% without PSI) and a steady-state power conversion efficiency of 0.042% (vs 0.028% without PSI).

Publications

  • Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Dilek Dervishogullari, Kody Wolfe, Christopher Stachurski, G Kane Jennings, David E Cliffel, "Multilayer Photosystem I Films within Porous Indium Tin Oxide Cathodes for Enhanced Photocurrent Generation," The Electrochemical Society Meeting, 2019.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Christopher Stachurski, Dilek Dervishogullari, Jade Stanley, Kody Wolfe, G Kane Jennings, David E Cliffel, "Photosystem I-Modified Multi-Walled Carbon Nanotube Anodes for Enhanced Solar Energy Conversion," The Electrochemical Society Meeting, 2019.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kody D Wolfe, Dilek Dervishogullari, Joshua M Passantino, Christopher D Stachurski, G Kane Jennings, David E Cliffel, "Improving the stability of photosystem Ibased bioelectrodes for solar energy conversion," Current Opinion in Electrochemistry, 19, 27-34, 2020.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kody D Wolfe, Dilek Dervishogullari, Christopher D Stachurski, Joshua M Passantino, G Kane Jennings, David E Cliffel, "Photosystem I Multilayers within Porous Indium Tin Oxide Cathodes Enhance Mediated Electron Transfer," ChemElectroChem, 7, 595-603, 2020.
  • Type: Journal Articles Status: Under Review Year Published: 2020 Citation: Chris Stachurski, G. Kane Jennings, David Cliffel, "Optical and Electrochemical Tuning of Hydrothermally Synthesized Nitrogen-Doped Carbon Dots" Nanoscale Advances, in revision.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2020 Citation: Joshua Passantino, Kody Wolfe, Keiann Simon, David Cliffel, and G. Kane Jennings, "Photosystem I Enhances the Efficiency of a Natural, Gel-Based Dye-Sensitized Solar Cell ACS Applied Bio Materials, in press.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Avi Gargye, Faustin Mwambutsa, and Kane Jennings, "Layer-By-Layer Films of Photosystem I and Conducting Polymers" Amer. Inst. of Chemical Engineers Annual Meeting, Undergraduate Poster Session, November, 2019
  • Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Christopher Stachurski, G Kane Jennings, David Cliffel, "Synthesis of nitrogen-doped carbon dots as charge transport materials for photosystem I-based biohybrid photovoltaics," Abstracts of the American Chemical Society Meeting, vol 258, August, 2019.