Structural and Functional Hierarchy in Photosynthetic Energy Conversion—from Molecules to Nanostructures
© Szabó et al. 2015
Received: 29 August 2015
Accepted: 23 November 2015
Published: 1 December 2015
Basic principles of structural and functional requirements of photosynthetic energy conversion in hierarchically organized machineries are reviewed. Blueprints of photosynthesis, the energetic basis of virtually all life on Earth, can serve the basis for constructing artificial light energy-converting molecular devices. In photosynthetic organisms, the conversion of light energy into chemical energy takes places in highly organized fine-tunable systems with structural and functional hierarchy. The incident photons are absorbed by light-harvesting complexes, which funnel the excitation energy into reaction centre (RC) protein complexes containing redox-active chlorophyll molecules; the primary charge separations in the RCs are followed by vectorial transport of charges (electrons and protons) in the photosynthetic membrane. RCs possess properties that make their use in solar energy-converting and integrated optoelectronic systems feasible. Therefore, there is a large interest in many laboratories and in the industry toward their use in molecular devices. RCs have been bound to different carrier matrices, with their photophysical and photochemical activities largely retained in the nano-systems and with electronic connection to conducting surfaces. We show examples of RCs bound to carbon-based materials (functionalized and non-functionalized single- and multiwalled carbon nanotubes), transitional metal oxides (ITO) and conducting polymers and porous silicon and characterize their photochemical activities. Recently, we adapted several physical and chemical methods for binding RCs to different nanomaterials. It is generally found that the P+(QAQB)− charge pair, which is formed after single saturating light excitation is stabilized after the attachment of the RCs to the nanostructures, which is followed by slow reorganization of the protein structure. Measuring the electric conductivity in a direct contact mode or in electrochemical cell indicates that there is an electronic interaction between the protein and the inorganic carrier matrices. This can be a basis of sensing element of bio-hybrid device for biosensor and/or optoelectronic applications.
Photosynthesis, the conversion of light energy into chemical energy by living organisms, is the energetic basis of virtually all life on Earth; also, fossil fuels are energy deposits of photosynthesis of past million years. The photosynthetic utilization of light energy requires a machinery organized in a structural and functional hierarchy from molecules through protein complexes to entire organisms . One of the major goals of photosynthesis research, conducted worldwide in academic laboratories and industrial institutes, is to find biomimetic and biotechnological applications and technologies of utilization of the environmentally safe and essentially inexhaustible solar energy. One interesting concept is green synthesis of nanoparticles for diverse application in almost all fields of medicine, agriculture and technology reviewed by Husen and Siddiqi . In addition, new generations of light-harvesting and photoactive intelligent materials are also of high interest [3–10]. Bio-nano-composite materials are considered the materials for the future [11, 12]. Biological systems offer inherently good examples for phenomena in nanotechnology, since the length scales of functional molecular assemblies, such as protein complexes and membrane fragments, fall in the 5–10-nm range. In the following sections, examples of nanotechnological applications of photosynthetic systems will be presented, with our attention focused mainly on systems containing purple bacterial reaction centres.
The Basic Molecules of the Photosynthetic Energy Conversion Are the Chlorophylls
The importance of the molecular structure in determining the biological function can be understood when the properties of the chlorophylls are compared with those of bacteriochlorophylls, found in un-oxygenic photosynthetic prokaryotes. In bacteriochlorophyll, the conjugation of the electron shells is disrupted (Fig. 1). The lower degree of delocalization increases the energy level of HOMO and decreases, in turn, that of LUMO. This change in the energy difference is reflected by spectroscopic features. The S0 → S1 transition for bacteriochlorophyll-a corresponds to λ = 760 nm in organic solution (in contrast to λ = 660 nm for chlorophyll-a), and the oxidizing power is smaller, E m = 400 mV (as opposed with 500 mV for chlorophyll-a) in organic solution. When bacteriochlorophylls form the special pair in the RC protein, E m is shifted only moderately (from 400 to 450 mV); this is far too low with respect to the energetic requirement of water oxidation.
It is important to note that the difference in the E m values between the excited and ground state couples of the primary donors are ΔE m = 1840 mV (corresponding to a free energy difference, ΔG = 177.6 kJ/mol) and ΔE m = 1370 mV (ΔG = 132.2 kJ/mol) for chlorophyll-a and bacteriochlorophyll-a, respectively. These values coincide with the S0 → S1 transitions in the red (λ = 660 nm (ΔG = 180 kJ/mol)) and near infrared λ = 800 nm (ΔG = 148.5 kJ/mol) for chlorophyll-a and bacteriochlorophyll-a, respectively. For summary, see Fig. 2.
Organization of the RC Protein
The photosynthetic pigments (chlorophylls and bacteriochlorophylls, together with other molecules) are arranged in special pigment-protein complexes (light-harvesting antenna complexes and RC proteins) in which efficient light absorption, energy transfer, charge separation and stabilization are warranted. Upon excitation by light primary charge, separation takes place in the photosynthetic RCs, which are the most efficient light energy converter systems in nature [6, 13]. Although different types of RCs have been evolved in nature (photosystem I (PS-I) and photosystem II (PS-II) in plants, algae and cyanobacteria and type I and type II RCs in green and purple photosynthetic bacteria, respectively), they all perform very similar basic processes: pigment excitation upon the absorption of light, charge separation and stabilization, rearrangements of charges, and hydrogen bonding interactions within and around the RC proteins.
The time constant of the redox cycle of the RC is determined by the redox components bound to it. By changing the appropriate redox component, a wide range of RC turnover rates can be designed (from 1012 to 10−1 s−1). From a practical point of view, it is important to note that every redox cofactor component of the RC can be artificially changed (washed out from the RC and chemically or genetically modified; see e.g. [17, 18]). In general, proteins can be designed and constructed at will, in a broad range, to generate redox processes with different turnover times and conditions.
The Photosynthetic Membrane
Here n is the number of moles, ΔE h is the redox potential according to the Nernst equation, F is the Faraday constant (=0.0965 kJ/mol mV), R is the universal gas constant, T is the absolute temperature, U is the membrane potential. The p.m.f. serves the driving force of the ATP synthesis [19, 23].
RCs in Nanostructures
It is interesting to note that even though the RC proteins—called the “nature’s solar power stations”—have changed the surface of our globe, these are “real nano-systems”. Their size represents only nanometre scale in the cells (about 10 nm [24–26]), and their work is also only “nano” (one photon initiates one charge separation ). This protein possesses such technical properties that unique applications are possible, for example, its use in the nanostructures or in the optoelectronic systems [3, 4, 27–29]. These properties prompted huge efforts for creating bio-nanocomposite materials and using RCs attached to different carrier matrices and led to numerous publications. The physico-chemical properties (photochemical activity, electric conductivity) of the bio-nanocomposite materials containing RCs and different carrier matrices have been investigated. A couple of examples will be presented in the following paragraphs.
Artificial Lipid Membranes (Proteo-liposomes)
Biological materials are developed by nature for extremely efficient, sensitive and specific functions. When they are isolated from their natural environment, their activity is usually decreased. One obvious possibility is to combine them with nano-systems which mimic the in vivo conditions. For this purpose, artificial lipid membranes (liposomes) seem to be good and obvious choices [30, 31]. On the one hand, RC is a transmembrane protein, so that lipid membrane environment resembles the in vivo conditions [32–35]. In addition, the liposome/RC nanosystem can be a good model for the Mitchell chemiosmotic hypothesis (awarded by Nobel Prize in Chemistry in 1978 ), which is the basis of the cell bioenergetics. The radius of the specifically prepared liposome embedding the RCs is about 100 nm , which falls in the range of the systems usually called “nano”. Note that this size is about one fourth of the wavelength of the visible light. When the liposome/RC system is illuminated by light, the electromagnetic field is inherently heterogeneous because of the commensurate sizes of the diameter of proteo-liposomes and the wavelength of the visible light.
Recently, we have shown that RC proteins can be attached to functionalized and non-functionalized, single-walled (SWCNT [37, 38]) and multiwalled (MWCNT ) carbon nanotubes (CNTs). In addition to the physical binding, different strategies have been elaborated for the chemical attachment of the RC protein to CNTs (). The successful binding was visualized by EM and AFM measurements, and the functioning of the RC was checked by flash photolysis experiments. We found that (a) RCs can be attached to CNTs effectively, while they largely retain their activity; (b) this binding induces changes in the intra-protein electron transport (stabilization of the charge-separated state); and (c) there is an electronic communication between the SWCNTs and RCs. Circular dichroism (CD) measurements indicate that the binding of the protein to CNT does not alter the excitonic interactions, i.e. there is no substantial change in the RC structure after the binding .
Transitional Metal Oxide/RC Complexes
Transparent conducting oxides (TCOs) are made of indium oxide (In2O3), tin oxide (SnO2) and ITO, and their combination has been widely used in semiconductor and electronic device industry [41–43]. ITO as a component of the composite electrode in bio-hybrid systems offers unique possibility for application due to its transparency in the visible range. Realization of protein-based bio-nanocomposite materials (among them RC protein-based ones) will lead to conceptual revolution in the development of integrated optical devices, e.g. optical switches, micro-imaging systems, sensors, telecommunications technologies or energy harvesting [44–46].
The spectroscopic properties and electric conductivity of ITO/RC composite provide direct evidence that the RC keeps its photochemical activity even if it is dried on ITO. A direct electric contact between the metal oxide layer and the protein is shown by the light-induced conductivity change of the composite. This bio-nanocomposite provides a model for new generations of applications, e.g. in integrated optoelectronic devices .
Porous Silicon/RC Complexes
Among the different carrier matrices (carbon-based materials, conductive polymers, different metal oxides like ITO), silicon-based materials have special interest during the engineering of bio-inspired materials [47–56]. Due to its environmental, optical and electronic properties, porous silicon (PSi) is one of the most promising materials not only for biosensors and novel drug delivery systems but also for energy conversion and integrated optoelectronic devices [57–59]. Combination of RC and PSi can offer new possibilities in the field of bio-hybrid systems in nano-bionics.
In an earlier publication, we have shown that the donor and acceptor sites of the RC remained active and accessible for externally added donor (horse heart cytochrome c) and acceptor (UQ-0) agents after binding to PSi. We also predicted a possible redox interaction between the protein and the PSi to be proven directly by an independent experiment [60, 61].
Conducting Polymer/RC Complexes
The photochemical or photophysical activity of the RC/PTAA/MWCNT complex can be characterized by the absorption change at 860 nm. At this wavelength, the redox state of the primary electron donor bacteriochlorophyll dimer (P+/P) can be monitored. The decay curves could be analysed by a multi-exponential fit of sum of first-order reactions: A (t) = Σ A (0,i)exp(−t/τ (i)), where A (0,i) and τ (i) are the contribution and the lifetime of the ith component, respectively. However, the monophasic decay, with the lifetime of τ = 480 ms, indicates the homogenous functional binding of the RC to the complex. It is expected that the presence of the PTAA increases the electronic coupling between the RC and the MWCNT. In addition, the absorption cross section, which is a determining factor for the power of the energy converter system, is enhanced by the larger local concentration of the RC (i.e. by the larger chromophore density).
Different biological organizations are used to create new-generation light-harvesting systems. In these composites, the advantages of the biological organizations and the carrier matrices are combined so that these composites can be a state-of-the-art, really smart, modern and innovative device. Photosynthetic RC proteins offer unique applications, for example, their use in the nanostructures or in the optoelectronic systems. In these systems, the electron—arising from charge separation—is trapped in the redox components of the RC or its molecular environment and, among other things, can participate in electric circuits. The fabrication of systems for efficient light energy conversion (e.g. photovoltaics), integrated optoelectronic systems or biosensors (e.g. for specific detection of pesticides) can be visualized for the near future.
Nano-bionics in Photosynthesis
Nanotechnology offers new and potential direction for using interface between biological (as well as photosynthetic) structures and non-biological nanostructures with enhanced functions for harvesting solar energy or functioning as sensitive photonic chemical sensors .
Biological materials and photosynthetic RCs are structured for extremely efficient, sensitive and specific functions. The RC proteins own such technical properties that many unique applications are envisaged, for example, their use in nanostructures or in optoelectronic systems [3, 60]. Different types of RCs found in nature are investigated in different photoconverter applications, and their photoconversion power efficiency is far from the performance in vivo up to now. η ≈ 10−4 and 10−7 are found for bacterial reaction centres in electrochemical cell and dried in semiconductor layer structures, respectively . These values are comparable with the one found for photosystem one (PS-I) in Z-scheme-inspired biophotovoltaics in redox hydrogels (η ≈ 10−5 ).
Although the photoconversion efficiency is very small in these systems up to now, the use of the RCs in bio-nano-systems is a real challenge. This protein assures the energy supply for the whole earthly life (including the fossil fuels as well), and we have this protein in our hand. It can be purified, fully engineered and can be designed to our wish. The function of the RC can be mimicked in many photo-senzibilization and photocatalytic processes in which the charge separation capacity of the protein is substituted by an inorganic analogue.
There is a versatile possibility to construct 2D or even 3D hybrid materials based on graphene and some organic materials in which electron–hole pairs are created upon light irradiation with oxidation and reduction power capability. The special hierarchical semiconductor-based heterogeneous organizations of these organic semiconductor catalysts can mimic the energetic schemes of the photosynthetic RCs which fulfil the conditions of separation and stabilization of light-driven charges by chain of redox reactions [66–68].
Due to its remarkable mechanical, thermal, optical and excellent electron conductivity, high transparency and unique two-dimensional (2D) morphology graphene became a promising material as a component of many optoelectronic assemblies. Coupling with proper semiconductor materials, the exceptional properties of graphene provide the possibility of designing new-generation high performance hierarchically structured artificial photosynthetic systems. The enhanced photochemical activity of these highly structured composites can be utilized in many fields of optoelectronics like environmental remediation, water splitting, CO2 photoreduction and selective organic transformation, reviewed, e.g. in .
In this review we have shown that the vectorial charge transfer within the photosynthetic organisms initiated by light is assured in a system organized hierarchically from molecules to molecular complexes. The energy of light which is captured in the form of redox free energy of cofactors can be used for useful work either wiring out the electron in electric circuits or reducing chemical equivalents. This can be a basis of constructing artificial light-energy converting molecular devices like sensing element of bio-hybrid device for biosensor and/or for opto-electronic applications. Future researches should aim to find the most efficient energy converter system (the biological and the inorganic parts), the highest reproducibility and stability of the function.
The work was supported by grants from Switzerland through the Swiss Contribution (SH/7/2/20), from the National Research, Development and Innovation (NKFI) Fund (OTKA K112688 and PD116739) and from TÁMOP-422D-15/1/KONV-2015-0024 (Creating the Center of Excellence at the “University of Szeged” supported by the European Union and co-financed by the European Social Fund). Thanks are due to the helpful discussions with members of European Cooperation in Science and Technology network, PHOTOTECH COST TD1102 and to Ms. Judit Tóth for the valuable technical assistance.
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- Govindjee, Beatty JT, Gest H, Allen JF (2006) Discoveries in photosynthesis. Advances in photosynthesis and respiration. Springer, BerlinGoogle Scholar
- Husen A, Khwaja Salahuddin Siddiqi KS (2014) Phytosynthesis of nanoparticles: concept, controversy and application. Nanoscale Res Lett 9:229View ArticleGoogle Scholar
- Nagy L, Hajdu K, Fisher B, Hernádi K, Nagy K, Vincze J (2010) Photosynthetic reaction centres—from basic research to application possibilities. Notulae Scientia Biologica 2:7–13Google Scholar
- Nagy L, Hajdu K, Torma S, Csikós S, Szabó T, Magyar M, Fejes D, Hernádi K, Kellermayer M, Horváth E, Magrez A, Forró L (2014) Photosynthetic reaction centre/carbon nanotube bundle composites. Phys Status Solidi B 251:2366–2371View ArticleGoogle Scholar
- Scholes GD, Fleming GR, Olaya-Castro A, van Grondelle R (2011) Lessons from nature about solar light harvesting. Nature Chem 3:763View ArticleGoogle Scholar
- Jones MR (2009) The petite purple photosynthetic powerpack. Biochem Soc Trans 37:400–407View ArticleGoogle Scholar
- Cogdell RJ, Gardiner AT, Molina PI, Cronin L (2013) The use and misuse of photosynthesis in the quest for novel methods to harness solar energy to make fuel. Phil Trans R Soc A 371:20110603View ArticleGoogle Scholar
- Cogdell RJ, Lindsay JG (1998) Can photosynthesis provide a ‘biological blueprint’ for the design of novel solar cells? Trends Biotechnol 16:521–527View ArticleGoogle Scholar
- Mongwaketsi NP, Kotsedi L, Nuru ZY, Sparrow R, Garab G, Maaza M (2014) Porphyrin nanorods-polymer composites for solar radiation harvesting applications. J Porph Phtalloc 18:1145–1156View ArticleGoogle Scholar
- Chappaz-Gillot C, Marek PL, Blaive BJ, Canard G, Bürck J, Garab G, Hahn H, Jávorfi T, Kelemen L, Krupke R, Mössinger D, Ormos P, Reddy CM, Roussel C, Steinbach G, Szabó M, Ulrich AS, Vanthuyne N, Vijayaraghavan A, Zupcanova A, Balaban TS (2012) Anisotropic organization and microscopic manipulation of self-assembling synthetic porphyrin micro-rods that mimic chlorosomes: bacterial light-harvesting systems. J Am Chem Soc 134:944–954View ArticleGoogle Scholar
- Darder M, Aranda P, Ruiz-Hitzky E (2007) Bionanocomposites: a new concept of ecological, bioinspired and functional hybrid materials. Adv Mater 19:1309–1319View ArticleGoogle Scholar
- Shoseyov O, Levy I (2008) Nanobiotechnology: bioinspired devices and materials of the future. Humana Press. Inc, TotowaView ArticleGoogle Scholar
- Wraight CA, Clayton R (1974) The absolute quantum efficiency of bacteriochlorophyll photooxidation in reaction centres of Rhodopseudomonas sphaeroides. Biochem Biophys Acta 333:246–260Google Scholar
- Wraight CA (2004) Proton and electron in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter Sphaeroides. Front Biosci 9:309–337View ArticleGoogle Scholar
- Allen JP, Williams JC (1998) Photosynthetic reaction centers. FEBS Lett 438:5–9View ArticleGoogle Scholar
- Paddock ML, Feher G, Okamura MY (2003) Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett 555:45–50View ArticleGoogle Scholar
- Okamura MY, Isaacson RA, Feher G (1975) Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas sphaeroides. Proc Natl Acad Sci U S A 72:3491–3495View ArticleGoogle Scholar
- Maróti P, Kirmaier C, Wraight CA, Holten D, Pearlstein R (1985) Photochemistry and electron transfer on borohydride-treated photosynthetic reaction centers. Biochim Biophys Acta 810:132–139View ArticleGoogle Scholar
- Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148View ArticleGoogle Scholar
- Zuber H, Cogdell RJ (1995) Structure and organization of purple bacterial reaction antennae complexes. In: Blankenship RE, Madigan TM, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publisher, Dordrecht, pp 315–348Google Scholar
- Vermeglio A, Joliot P, Joliot A (1995) Organization of electron transfer components and supercomplexes. In: Blankenship RE, Madigan TM, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publisher, Dordrecht, pp 279–295Google Scholar
- Blankenship RE, Madigan TM, Bauer CE (1995) Anoxygenic photosynthetic bacteria. In: Advances in photosynthesis. Kluwer Academic Publishers, DordrechtGoogle Scholar
- Gromet-Elhanan Z (1995) The proton-translocating F0F1 ATP synthase–ATPase complex. In: Blankenship RE, Madigan TM, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publisher, Dordrecht, pp 807–820Google Scholar
- Dorogi M, Lambrev PH, Magyar M, Hernádi K, Horváth E, Magrez A, Forró L, Nagy L, Garab Gy. Photosynthetic reaction center structures in nanocomposite systems—what you can see with polarization spectroscopy. Cost Phototech, Training School Advanced Laser Spectroscopy in Green Phototechnology, October 18–23, 2014 Szeged, Hungary, P15Google Scholar
- Palazzo G, Mallardi A, Francia F, Dezi M, Venturoli G, Pierno M, Vignatid E, Piazzad R (2004) Spontaneous emulsification of detergent solubilized reaction center: protein conformational changes precede droplet growth. Phys Chem Chem Phys 6:1439–1445View ArticleGoogle Scholar
- Nagy L, Maroti P, Terazima M (2008) Spectrally silent light induced conformation change in photosynthetic reaction centers. FEBS Lett 582:3657–3662View ArticleGoogle Scholar
- Giardi MT, Pace E (2006) Biotechnological applications of photosynthetic. In: Giardi MT, Piletska EV (eds) Proteins: Biochips, Biosensors and Biodevices. Springer, New York, pp 47–154Google Scholar
- Hollander MJ, Magis JG, Fuchsenberger P, Aartsma TJ, Jones MR, Frese RN (2011) Enhanced photocurrent generation by photosynthetic bacterial reaction centers through molecular relays light-harvesting complexes and direct protein gold interactions. Langmuir 27:10282View ArticleGoogle Scholar
- Kamran M, Delgado JD, Friebe V, Aartsma TJ, Frese RN (2014) Photosynthetic protein complexes as bio-photovoltaic building blocks retaining a high internal quantum efficiency. Biomacromolecules 15:2833–2838View ArticleGoogle Scholar
- Hellingwerf KJ (1987) Reaction centers from Rhodopseudomonas sphaeroides in reconstituted phospholipid vesicles. I. Structural studies. J Bioenerg Biomembr 19(3):203–223View ArticleGoogle Scholar
- Ollivon M, Lesieur S, Gabrielle-Madelmont C, Paternostre M (2000) Vesicle reconstitution from lipid-detergent mixed micelles. Biochim Biophys Acta 1508:34–50View ArticleGoogle Scholar
- Milano F, Agostiano A, Mavelli F, Trotta M (2003) Kinetics of the quinone binding reaction at the QB site of reaction centers from the purple bacteria Rhodobacter sphaeroides reconstituted in liposomes. Eur J Biochem 270:4595–4605View ArticleGoogle Scholar
- Milano F, Italiano F, Agostiano A, Trotta M (2009) Characterisation of RC-proteoliposomes at different RC/lipid ratios. Photosynth Res 100:107–112View ArticleGoogle Scholar
- Nagy L, Fodor E, Tandori J, Rinyu L, Farkas T (1999) Lipids affect the charge stabilization in wild type and mutant reaction centers of Rhodobacter sphaeroides. Austr J of Plant Physiol 25:465–473View ArticleGoogle Scholar
- Nagy L, Milano F, Dorogi M, Trotta M, Laczkó G, Szebényi K, Váró G, Agostiano A, Maróti P (2004) Protein/lipid interaction in bacterial photosynthetic reaction center: the role of phosphatidylcholine and phosphatidylglycerol in charge stabilization. Biochemistry 43:12913–12923View ArticleGoogle Scholar
- Milano F, Trotta M, Dorogi M, Fischer B, Giotta L, Agostiano A, Maróti P, Kálmán L, Nagy L (2012) Light induced transmembrane proton gradient in artificial lipid vesicles reconstituted with photosynthetic reaction centers. J Bioenerg Biomembr 44:373–384View ArticleGoogle Scholar
- Dorogi M, Bálint Z, Mikó C, Vileno B, Milas M, Hernádi K, Forró L, Váró G, Nagy L (2006) Stabilization effect of single-walled carbon nanotubes on the functioning of photosynthetic reaction centers. J Phys Chem B 110:21473–21479View ArticleGoogle Scholar
- Magyar M, Hajdu K, Szabo T, Hernadi K, Dombi A, Horvath E, Magrez A, Forró L, Nagy L (2011) Long term stabilization of reaction center protein photochemistry by carbon nanotubes. Phys Status Solidi B 248:2454–2457View ArticleGoogle Scholar
- Hajdu K, Szabó T, Magyar M, Bencsik G, Németh Z, Nagy K, Magrez A, Forró L, Váró G, Hernádi K, Nagy L (2011) Photosynthetic reaction center protein in nano structures. Phys Status Solidi B 248:2700–2703View ArticleGoogle Scholar
- Nagy L, Magyar M, Szabo T, Hajdu K, Giotta L, Dorogi M, Milano F (2014) Photosynthetic machineries in nano systems. Curr Protein Pept Sci 15:363View ArticleGoogle Scholar
- Granqvist CG, Hultaker A (2002) Transparent and conducting ITO films: new developments and applications. Thin Solid Films 411:1–5View ArticleGoogle Scholar
- Lany S, Zunger A (2007) Dopability, intrinsic conductivity, and nonstoichiometry of transparent conducting oxides. Phys Rev Lett 98:045501View ArticleGoogle Scholar
- Szabó T, Bencsik G, Magyar M, Visy C, Gingl Z, Nagy K, Váró G, Hajdu K, Kozák G, Nagy L (2013) Photosynthetic reaction centers/ITO hybrid nanostructure. Mater Sci Eng C 33:769–773View ArticleGoogle Scholar
- Fábián L, Heiner Z, Mero M, Kiss M, Wolff EK, Ormos P, Osvay K, Dér A (2011) Protein-based ultrafast photonic switching. Opt Express 19:18861View ArticleGoogle Scholar
- Der A, Valkai S, Fabian L, Ormos P, Ramsden JJ, Wolff EK (2007) Integrated optical switching based on the protein bacteriorhodopsin. Photochem Photobiol 83:393–396View ArticleGoogle Scholar
- Vsevolodov N (1998) Biomolecular electronics. Birkhauser, BostonGoogle Scholar
- Agarwal V, del Río JA (2003) Tailoring the photonic band gap of a porous silicon dielectric mirror. Appl Phys Lett 82:1512–1514View ArticleGoogle Scholar
- Estevez JO, Arriaga J, Méndez Blas A, Agarwal V (2009) Enlargement of omnidirectional photonic bandgap in porous silicon dielectric mirrors with a Gaussian profile refractive index. Appl Phys Lett 94:061914View ArticleGoogle Scholar
- Martin M, Palestino G, Cloitre T, Agarwal V, Zimanyi L, Gergely C (2009) Three-dimensional spatial resolution of the nonlinear photoemission from biofunctionalized porous silicon microcavity. Appl Phys Lett 94:223313View ArticleGoogle Scholar
- Thompson CM, Nieuwoudt M, Ruminski AM, Sailor MJ, Miskelly GM (2010) Electrochemical preparation of pore wall modification gradients across thin porous silicon layers. Langmuir 26:7598–7603View ArticleGoogle Scholar
- Estephan E, Saab MB, Agarwal V, Cuisinier FJG, Larroque C, Gergely C (2011) Peptides for the biofunctionalization of silicon for use in optical sensing with porous silicon microcavities. Adv Funct Mater 21:2003–2011View ArticleGoogle Scholar
- Palestino G, Legros R, Agarwal V, Pérez E, Gergely C (2008) Functionalization of nanostructured porous silicon microcavities for glucose oxidase detection. Sens Actuators B 135:27–34View ArticleGoogle Scholar
- Xiao L, Gu L, Howell SB, Sailor MJ (2011) Porous silicon nanoparticle photosensitizers for singlet oxygen and their phototoxicity against cancer cells. ACS Nano 5:3651–3659View ArticleGoogle Scholar
- Wu EC, Andrew JS, Buyanin A, Kinsella JM, Sailor MJ (2011) Suitability of porous silicon microparticles for the long-term delivery of redox-active therapeutics. Chem Commun 47:5699–5701View ArticleGoogle Scholar
- Kilian KA, Böcking T, Ilyas S, Gaus K, Jessup W, Gal M, Gooding JJ (2007) Forming antifouling organic multilayers on porous silicon Rugate filters towards in vivo/ex vivo biophotonic devices. Adv Funct Mater 17:2884–2890View ArticleGoogle Scholar
- Orosco MM, Pacholski C, Miskelly GM, Sailor J (2006) Protein-coated porous-silicon photonic crystals for amplified optical detection of protease activity. Adv Mater 18:1393–1396View ArticleGoogle Scholar
- Noji T, Kamidaki C, Kawakami K, Shen JR, Kajino T, Fukushima Y, Sekitoh T, Itoh S (2011) Photosynthetic oxygen evolution in mesoporous silica material: adsorption of photosystem II reaction center complex into 23 nm nanopores in SBA. Langmuir 27:705–713View ArticleGoogle Scholar
- Oda I, Hirata K, Watanabe S, Shibata Y, Kajino T, Fukushima Y, Iwai S, Itoh S (2006) Function of membrane protein in silica nanopores: incorporation of photosynthetic light-harvesting protein LH2 into FSM. J Phys Chem B 110:1114–1120View ArticleGoogle Scholar
- Oda I, Iwaki M, Fujita D, Tsutsui Y, Ishizaka S, Dewa M, Nango M, Kajino T, Fukushima Y, Itoh S (2010) Photosynthetic electron transfer from reaction center pigment-protein complex in silica nanopores. Langmuir 26:13399–13406View ArticleGoogle Scholar
- Hajdu K, Gergely C, Martin M, Cloitre T, Zimányi L, Tenger K, Khoroshyy P, Palestino G, Agarwal V, Hernádi K, Németh Z, Nagy L (2012) Porous silicon/photosynthetic reaction center hybrid nanostructure. Langmuir 28:11866–11873View ArticleGoogle Scholar
- Hajdu K, Gergely C, Martin M, Zimányi L, Agarwal V, Palestino G, Hernádi K, Németh Z, Nagy L (2012) Light-harvesting bio-nanomaterial using porous silicon and photosynthetic reaction center. Nanoscale Res Lett 7:400View ArticleGoogle Scholar
- Szabó T, Magyar M, Németh Z, Hernádi K, Endrődi B, Bencsik G, Visy C, Horváth E, Magrez A, Forró L, Nagy L (2012) Charge stabilization by reaction center protein immobilized to carbon nanotubes functionalized by amine groups and poly(3-thiophene acetic acid) conducting polymer. Phys Status Solidi B 12:2386–2389View ArticleGoogle Scholar
- Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Reuel NF, Hilmer AJ, Sen F, Brew JA, Stranno M (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13:400–408View ArticleGoogle Scholar
- Szabó T, Nyerki E, Tóth T, Csekő R, Magyar M, Horváth E, Hernádi K, Endrődi B, Cs V, Forró L, Nagy L (2015) Generating photocurrent by nanocomposites based on photosynthetic reaction centre protein. Phys Status Solidi B 252:2614–2619View ArticleGoogle Scholar
- Hartmann V, Kothe VT, Poller S, El-Mohsnawy E, Nowaczyk MM, Plumere N, Schuhmann W, Rogner M (2014) Redox hydrogels with adjusted redox potential for improved efficiency in Z-scheme inspired biophotovoltaic cells. Chem Phys 16:11936–11941Google Scholar
- Zhang N, Yang MQ, Liu S, Sun Y, Xu YJ (2015) Waltzing with the versatile platform of graphene to synthesize composite photocatalysts. Chem Rev 115:10307–10377View ArticleGoogle Scholar
- Han C, Yang MQ, Wengab B, Xu YJ (2014) Improving the photocatalytic activity and anti-photocorrosion of semiconductor ZnO by coupling with versatile carbon. Phys Chem Chem Phys 16:16891–16903View ArticleGoogle Scholar
- Han C, Chen Z, Zhang N, Colmenares JC, Xu YJ (2014) Hierarchical hybrids: hierarchically CdS decorated 1D ZnO nanorods-2D graphene hybrids: low temperature synthesis and enhanced photocatalytic performance. Adv. Funct. Mater. doi:10.1002/adfm.201570010
- Yang MQ, Zhang N, Pagliaro M, and Xu YJ (2014) Artificial photosynthesis over graphene–semiconductor composites. Are we getting better? Chem. Soc. Rev. doi:10.1039/c4cs00213j