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Coupling biology to synthetic nanomaterials for semi-artificial photosynthesis

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Abstract

Biohybrid artificial photosynthesis aims to combine the advantages of biological specificity with a range of synthetic nanomaterials to create innovative semi-synthetic systems for solar-to-chemical conversion. Biological systems utilize highly efficient molecular catalysts for reduction–oxidation reactions. They can operate with minimal overpotentials while selectively channeling reductant energy into specific transformation chemistries and product forming pathways. Nanomaterials can be synthesized to have efficient light-absorption capacity and tuneability of charge separation by manipulation of surface chemistries and bulk compositions. These complementary aspects have been combined in a variety of ways, for example, where biological light-harvesting complexes function as antenna for nanoparticle catalysts or where nanoparticles function as light capture, charge separation components for coupling to chemical conversion by redox enzymes and whole cells. The synthetic diversity that is possible with biohybrids is still being explored. The progress arising from creative approaches is generating new model systems to inspire scale-up technologies and generate understanding of the fundamental mechanisms that control energy conversion at the molecular scale. These efforts are leading to discoveries of essential design principles that can enable the development of scalable artificial photosynthesis systems.

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References

  • Ai X, Xu Q, Jones M, Song Q, Ding S-Y, Ellingson RJ, Himmel M, Rumbles G (2007) Photophysics of (CdSe) ZnS colloidal quantum dots in an aqueous environment stabilized with amino acids and genetically-modified proteins. Photochem Photobiol Sci 6(9):1027–1033

    Article  CAS  PubMed  Google Scholar 

  • Amelia M, Impellizzeri S, Monaco S, Yildiz I, Silvi S, Raymo FM, Credi A (2011) Structural and size effects on the spectroscopic and redox properties of CdSe nanocrystals in solution: the role of defect states. ChemPhysChem 12(12):2280–2288

    Article  CAS  PubMed  Google Scholar 

  • Bang JH, Kamat PV (2011) CdSe quantum dot-fullerene hybrid nanocomposite for solar energy conversion: electron transfer and photoelectrochemistry. ACS Nano 5(12):9421–9427

    Article  CAS  PubMed  Google Scholar 

  • Bansal P, Duhan JS, Gahlawat SK (2014) Biogenesis of nanoparticles: a review. Afr J Biotechnol 13(28):2778–2785

    Article  CAS  Google Scholar 

  • Barber J (2009) Photosynthetic energy conversion: natural and artificial. Chem Soc Rev 38(1):185–196

    Article  CAS  PubMed  Google Scholar 

  • Bera D, Qian L, Tseng T-K, Holloway PH (2010) Quantum dots and their multimodal applications: a review. Materials 3(4):2260–2345

    Article  CAS  PubMed Central  Google Scholar 

  • Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, Ghirardi M, Gunner M, Junge W, Kramer DM, Melis A (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332(6031):805–809

    Article  CAS  PubMed  Google Scholar 

  • Brown KA, Dayal S, Ai X, Rumbles G, King PW (2010) Controlled assembly of hydrogenase-CdTe nanocrystal hybrids for solar hydrogen production. J Am Chem Soc 132(28):9672–9680

    Article  CAS  PubMed  Google Scholar 

  • Brown KA, Wilker MB, Boehm M, Dukovic G, King PW (2012) Characterization of photochemical processes for H2 production by CdS nanorod–[FeFe] hydrogenase complexes. J Am Chem Soc 134(12):5627–5636

    Article  CAS  PubMed  Google Scholar 

  • Brown KA, Song Q, Mulder DW, King PW (2014) Diameter dependent electron transfer kinetics in semiconductor-enzyme complexes. ACS Nano 8(10):10790–10798

    Article  CAS  PubMed  Google Scholar 

  • Brown KA, Wilker MB, Boehm M, Hamby H, Dukovic G, King PW (2016a) Photocatalytic regeneration of nicotinamide cofactors by quantum dot-enzyme biohybrid complexes. ACS Catal 6(4):2201–2204

    Article  CAS  Google Scholar 

  • Brown KA, Harris DF, Wilker MB, Rasmussen A, Khadka N, Hamby H, Keable S, Dukovic G, Peters JW, Seefeldt LC, King PW (2016b) Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid. Science 352(6284):448–450

    Article  CAS  PubMed  Google Scholar 

  • Caputo CA, Wang L, Beranek R, Reisner E (2015) Carbon nitride–TiO2 hybrid modified with hydrogenase for visible light driven hydrogen production. Chem Sci 6(10):5690–5694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in photosystem II: a comparative and evolutionary overview. Biochim Biophys Acta (BBA) 1817(1):26–43

    Article  CAS  Google Scholar 

  • Chen S, Wang L-W (2012) Thermodynamic oxidation and reduction potentials of photocatalytic semiconductors in aqueous solution. Chem Mater 24(18):3659–3666

    Article  CAS  Google Scholar 

  • Chica B, Wu C-H, Liu Y, Adams MW, Lian T, Dyer RB (2017) Balancing electron transfer rate and driving force for efficient photocatalytic hydrogen production in CdSe/CdS nanorod–[NiFe] hydrogenase assemblies. Energy Environ Sci 10(10):2245–2255

    Article  CAS  Google Scholar 

  • Cui S-C, Tachikawa T, Fujitsuka M, Majima T (2011) Photoinduced electron transfer in a quantum dot-cucurbituril supramolecular complex. J Phys Chem C 115(5):1824–1830

    Article  CAS  Google Scholar 

  • Ding Y, Bertram JR, Eckert C, Bommareddy RR, Patel R, Conradie A, Bryan S, Nagpal P (2019) Nanorg microbial factories: light-driven renewable biochemical synthesis using quantum dot-bacteria nano-biohybrids. J Am Chem Soc 141(26):10272–10282

    Article  CAS  PubMed  Google Scholar 

  • Fang X, Sokol K, Heidary N, Kandiel TA, Zhang JZ, Reisner E (2019) Structure-activity relationships of hierarchical three-dimensional electrodes with photosystem II for semi-artificial photosynthesis. Nano Lett 19(3):1844–1850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleming GR, Schlau-Cohen GS, Amarnath K, Zaks J (2012) Design principles of photosynthetic light-harvesting. Faraday Discuss 155:27–41

    Article  CAS  PubMed  Google Scholar 

  • Galanie S, Thodey K, Trenchard IJ, Interrante MF, Smolke CD (2015) Complete biosynthesis of opioids in yeast. Science 349(6252):1095–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorka M, Schartner J, van der Est A, Rögner M, Golbeck JH (2014) Light-mediated hydrogen generation in photosystem I: attachment of a naphthoquinone-molecular wire–Pt nanoparticle to the A1A and A1B sites. Biochemistry 53(14):2295–2306

    Article  CAS  PubMed  Google Scholar 

  • Greenbaum E (1985) Platinized chloroplasts: a novel photocatalytic material. Science 230(4732):1373–1375

    Article  CAS  PubMed  Google Scholar 

  • Greene BL, Joseph CA, Maroney MJ, Dyer RB (2012) Direct evidence of active-site reduction and photodriven catalysis in sensitized hydrogenase assemblies. J Am Chem Soc 134(27):11108–11111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimme RA, Lubner CE, Bryant DA, Golbeck JH (2008) Photosystem I/molecular wire/metal nanoparticle bioconjugates for the photocatalytic production of H2. J Am Chem Soc 130(20):6308–6309

    Article  CAS  PubMed  Google Scholar 

  • Grimme RA, Lubner CE, Golbeck JH (2009) Maximizing H2 production in photosystem I/dithiol molecular wire/platinum nanoparticle bioconjugates. Dalton Trans 45:10106–10113

    Article  CAS  Google Scholar 

  • Guo J, Suástegui M, Sakimoto KK, Moody VM, Xiao G, Nocera DG, Joshi NS (2018) Light-driven fine chemical production in yeast biohybrids. Science 362(6416):813–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamon C, Ciaccafava A, Infossi P, Puppo R, Even-Hernandez P, Lojou E, Marchi V (2014) Synthesis and enzymatic photo-activity of an O 2 tolerant hydrogenase–CdSe@ CdS quantum rod bioconjugate. Chem Commun 50(39):4989–4992

    Article  CAS  Google Scholar 

  • Heathcote P, Jones MR, Fyfe PK (2003) Type I photosynthetic reaction centres: structure and function. Philos Trans R Soc Lond Ser B 358(1429):231–243

    Article  CAS  Google Scholar 

  • Hutton GAM, Reuillard B, Martindale BCM, Caputo CA, Lockwood CWJ, Butt JN, Reisner E (2016) Carbon dots as versatile photosensitizers for solar-driven catalysis with redox enzymes. J Am Chem Soc 138(51):16722–16730

    Article  CAS  PubMed  Google Scholar 

  • Iwuchukwu IJ, Vaughn M, Myers N, O’Neill H, Frymier P, Bruce BD (2009) Self-organized photosynthetic nanoparticle for cell-free hydrogen production. Nat Nanotechnol 5:73

    Article  PubMed  CAS  Google Scholar 

  • Iwuchukwu IJ, Iwuchukwu E, Le R, Paquet C, Sawhney R, Bruce B, Frymier P (2011) Optimization of photosynthetic hydrogen yield from platinized photosystem I complexes using response surface methodology. Int J Hydrogen Energy 36(18):11684–11692

    Article  CAS  Google Scholar 

  • Jasieniak J, Califano M, Watkins SE (2011) Size-dependent valence and conduction band-edge energies of semiconductor nanocrystals. ACS Nano 5(7):5888–5902

    Article  CAS  PubMed  Google Scholar 

  • Kamat PV (2012) Manipulation of charge transfer across semiconductor interface. A criterion that cannot be ignored in photocatalyst design. J Phys Chem Lett 3(5):663–672

    Article  CAS  PubMed  Google Scholar 

  • King PW (1827) Designing interfaces of hydrogenase–nanomaterial hybrids for efficient solar conversion. Biochim Biophys Acta (BBA) 8:949–957

    Google Scholar 

  • Kornienko N, Zhang JZ, Sakimoto KK, Yang P, Reisner E (2018) Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis. Nat Nanotechnol 13(10):890–899

    Article  CAS  PubMed  Google Scholar 

  • LeBlanc G, Chen G, Jennings GK, Cliffel DE (2012) Photoreduction of catalytic platinum particles using immobilized multilayers of photosystem I. Langmuir 28(21):7952–7956

    Article  CAS  PubMed  Google Scholar 

  • Lee JW, Tevault CV, Blankinship SL, Collins RT, Greenbaum E (1994) Photosynthetic water splitting: in situ photoprecipitation of metallocatalysts for photoevolution of hydrogen and oxygen. Energy Fuels 8(3):770–773

    Article  CAS  Google Scholar 

  • Lee JW, Collins RT, Greenbaum E (1998) Molecular ionic probes: a new class of Hill reagents and their potential for nanofabrication and biometallocatalysis. J Phys Chem B 102(11):2095–2100

    Article  CAS  Google Scholar 

  • Liu C, Gallagher JJ, Sakimoto KK, Nichols EM, Chang CJ, Chang MC, Yang P (2015) Nanowire–bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals. Nano Lett 15(5):3634–3639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubitz W, Chrysina M, Cox N (2019) Water oxidation in photosystem II. Photosynth Res. https://doi.org/10.1007/s11120-019-00648-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubner CE, Grimme R, Bryant DA, Golbeck JH (2009) Wiring photosystem I for direct solar hydrogen production. Biochemistry 49(3):404–414

    Article  CAS  Google Scholar 

  • Lubner CE, Knörzer P, Silva PJN, Vincent KA, Happe T, Bryant DA, Golbeck JH (2010) Wiring an [FeFe]-Hydrogenase with photosystem I for Light-Induced Hydrogen Production. Biochemistry 49(48):10264–10266

    Article  CAS  PubMed  Google Scholar 

  • McConnell I, Li G, Brudvig GW (2010) Energy conversion in natural and artificial photosynthesis. Chem Biol 17(5):434–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller M, Robinson WE, Oliveira AR, Heidary N, Kornienko N, Warnan J, Pereira IAC, Reisner E (2019) Interfacing formate dehydrogenase with metal oxides for the reversible electrocatalysis and solar-driven reduction of carbon dioxide. Angew Chem 131(14):4649–4653

    Article  Google Scholar 

  • Mora SJ, Odella E, Moore GF, Gust D, Moore TA, Moore AL (2018) Proton-coupled electron transfer in artificial photosynthetic systems. Acc Chem Res 51(2):445–453

    Article  CAS  PubMed  Google Scholar 

  • Nichols EM, Gallagher JJ, Liu C, Su Y, Resasco J, Yu Y, Sun Y, Yang P, Chang MC, Chang CJ (2015) Hybrid bioinorganic approach to solar-to-chemical conversion. Proc Natl Acad Sci 112(37):11461–11466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noji T, Suzuki T, Kondo M, Jin T, Kawakami K, Mizuno T, Oh-oka H, Ikeuchi M, Nango M, Amao Y, Kamiya N, Dewa T (2016) Light-induced hydrogen production by photosystem I-Pt nanoparticle conjugates immobilized in porous glass plate nanopores. Res Chem Intermed 42(11):7731–7742

    Article  CAS  Google Scholar 

  • Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41(26):8518–8527

    Article  CAS  PubMed  Google Scholar 

  • Ratzloff MW, Wilker MB, Mulder DW, Lubner CE, Hamby H, Brown KA, Dukovic G, King PW (2017) Activation thermodynamics and H/D kinetic isotope effect of the Hox to HredH + transition in [FeFe] hydrogenase. J Am Chem Soc 139(37):12879–12882

    Article  CAS  PubMed  Google Scholar 

  • Reisner E, Armstrong FA (2011) A TiO2 nanoparticle system for sacrificial solar H2 production prepared by rational combination of a hydrogenase with a ruthenium photosensitizer. In: Wang P (ed) Nanoscale biocatalysis: methods and protocols. Humana Press, Totowa, pp 107–117

    Chapter  Google Scholar 

  • Reisner E, Fontecilla-Camps JC, Armstrong FA (2009) Catalytic electrochemistry of a [NiFeSe]-hydrogenase on TiO2 and demonstration of its suitability for visible-light driven H2 production. Chem Commun 5:550–552

    Article  Google Scholar 

  • Sakai T, Mersch D, Reisner E (2013) Photocatalytic hydrogen evolution with a hydrogenase in a mediator-free system under high levels of oxygen. Angew Chem Int Ed 52(47):12313–12316

    Article  CAS  Google Scholar 

  • Sakimoto KK, Wong AB, Yang P (2016) Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351(6268):74–77

    Article  CAS  PubMed  Google Scholar 

  • Seefeldt LC, Hoffman BM, Dean DR (2009) Mechanism of Mo-dependent nitrogenase. Annu Rev Biochem 78:701–722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokol KP, Robinson WE, Oliveira AR, Warnan J, Nowaczyk MM, Ruff A, Pereira IA, Reisner E (2018a) Photoreduction of CO2 with a formate dehydrogenase driven by photosystem II using a semi-artificial Z-scheme architecture. J Am Chem Soc 140(48):16418–16422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokol KP, Robinson WE, Warnan J, Kornienko N, Nowaczyk MM, Ruff A, Zhang JZ, Reisner E (2018b) Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase. Nat Energy 3(11):944

    Article  CAS  Google Scholar 

  • Szabó I, Bergantino E, Giacometti GM (2005) Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO Rep 6(7):629–634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tachibana Y, Vayssieres L, Durrant JR (2012) Artificial photosynthesis for solar water-splitting. Nat Photonics 6:511

    Article  CAS  Google Scholar 

  • Torella JP, Gagliardi CJ, Chen JS, Bediako DK, Colón B, Way JC, Silver PA, Nocera DG (2015) Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system. Proc Natl Acad Sci 112(8):2337–2342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Utschig LM, Dimitrijevic NM, Poluektov OG, Chemerisov SD, Mulfort KL, Tiede DM (2011) Photocatalytic hydrogen production from noncovalent biohybrid photosystem I/Pt nanoparticle complexes. J Phys Chem Lett 2(3):236–241

    Article  CAS  Google Scholar 

  • Utschig LM, Soltau SR, Tiede DM (2015) Light-driven hydrogen production from photosystem I-catalyst hybrids. Curr Opin Chem Biol 25:1–8

    Article  CAS  PubMed  Google Scholar 

  • Utschig LM, Soltau SR, Mulfort KL, Niklas J, Poluektov OG (2018) Z-scheme solar water splitting via self-assembly of photosystem I-catalyst hybrids in thylakoid membranes. Chem Sci 9(45):8504–8512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Li Z, Chen J, Li C (2017a) Crucial roles of electron-proton transport relay in the photosystem II-photocatalytic hybrid system for overall water splitting. J Phys Chem C 121(5):2605–2612

    Article  CAS  Google Scholar 

  • Wang B, Zeng C, Chu KH, Wu D, Yip HY, Ye L, Wong PK (2017b) Enhanced biological hydrogen production from Escherichia coli with surface precipitated cadmium sulfide nanoparticles. Adv Energy Mater 7(20):1700611

    Article  CAS  Google Scholar 

  • Wilker MB, Shinopoulos KE, Brown KA, Mulder DW, King PW, Dukovic G (2014) Electron transfer kinetics in CdS nanorod–[FeFe]-hydrogenase complexes and implications for photochemical H2 generation. J Am Chem Soc 136(11):4316–4324

    Article  CAS  PubMed  Google Scholar 

  • Wilker MB, Utterback JK, Greene S, Brown KA, Mulder DW, King PW, Dukovic G (2017) Role of surface-capping ligands in photoexcited electron transfer between CdS nanorods and [FeFe] hydrogenase and the subsequent H2 generation. J Phys Chem C 122(1):741–750

    Article  CAS  Google Scholar 

  • Williams PJLB, Laurens LM (2010) Microalgae as biodiesel & biomass feedstocks: review & analysis of the biochemistry, energetics & economics. Energy Environ Sci 3(5):554–590

    Article  CAS  Google Scholar 

  • Willkomm J, Orchard KL, Reynal A, Pastor E, Durrant JR, Reisner E (2016) Dye-sensitised semiconductors modified with molecular catalysts for light-driven H 2 production. Chem Soc Rev 45(1):9–23

    Article  CAS  PubMed  Google Scholar 

  • Winkler M, Kawelke S, Happe T (2011) Light driven hydrogen production in protein based semi-artificial systems. Biores Technol 102(18):8493–8500

    Article  CAS  Google Scholar 

  • Woolerton TW, Sheard S, Reisner E, Pierce E, Ragsdale SW, Armstrong FA (2010) Efficient and clean photoreduction of CO2 to CO by enzyme-modified TiO2 nanoparticles using visible light. J Am Chem Soc 132(7):2132–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y-H, Zhang H-S, Ma M, Guo X-F, Wang H (2009) The influence of ligands on the preparation and optical properties of water-soluble CdTe quantum dots. Appl Surf Sci 255(9):4747–4753

    Article  CAS  Google Scholar 

  • Zhang H, Liu H, Tian Z, Lu D, Yu Y, Cestellos-Blanco S, Sakimoto KK, Yang P (2018) Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production. Nat Nanotechnol 13(10):900–905

    Article  CAS  PubMed  Google Scholar 

  • Zhao F, Conzuelo F, Hartmann V, Li H, Nowaczyk MM, Plumeré N, Rögner M, Schuhmann W (2015) Light induced H2 evolution from a biophotocathode based on Photosystem 1–Pt nanoparticles complexes integrated in solvated redox polymers films. J Phys Chem B 119(43):13726–13731

    Article  CAS  PubMed  Google Scholar 

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Brown, K.A., King, P.W. Coupling biology to synthetic nanomaterials for semi-artificial photosynthesis. Photosynth Res 143, 193–203 (2020). https://doi.org/10.1007/s11120-019-00670-5

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