Structure and function of photosystem I and its application in [PDF]

Journal of Plant Physiology 169 (2012) 1639–1653

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Structure and function of photosystem I and its application in biomimetic solar-to-fuel systems Joanna Kargul ∗ , Julian David Janna Olmos, Tomasz Krupnik Department of Plant Molecular Physiology, Faculty of Biology, University of Warsaw, ul. Miecznikowa 1, 02-096 Warsaw, Poland

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Article history: Received 30 January 2012 Received in revised form 9 May 2012 Accepted 11 May 2012 Keywords: Artificial photosynthesis Hydrogen Light harvesting complex I Photosystem I Photosynthetic reaction centre

a b s t r a c t Photosystem I (PSI) is one of the most efficient biological macromolecular complexes that converts solar energy into condensed energy of chemical bonds. Despite high structural complexity, PSI operates with a quantum yield close to 1.0 and to date, no man-made synthetic system approached this remarkable efficiency. This review highlights recent developments in dissecting molecular structure and function of the prokaryotic and eukaryotic PSI. It also overviews progress in the application of this complex as a natural photocathode for production of hydrogen within the biomimetic solar-to-fuel nanodevices. © 2012 Elsevier GmbH. All rights reserved.

Introduction Oxygenic photosynthesis, the fundamental process of conversion of sunlight into chemical energy, sustains life on earth. The first step in this process, the light-driven charge separation, is conducted by photosystems (PS) I and II, two large multimeric chlorophyll (Chl)-binding protein complexes embedded in the thylakoid membranes of cyanobacteria, algae and higher plants. PSI and photosystem II (PSII) evolved from a common ancestor and are constructed around an exquisitely designed basic blueprint. Both contain a reaction centre (RC) protein complex coupled to a light harvesting (LH) system made up of several hundred pigment molecules (Blankenship, 2010; Kargul and Barber, 2011). The energy of photons captured by the LH systems of PSII and PSI is rapidly transferred to the photochemical reactions centres, the so-called P680 and P700 Chla molecules, respectively, where it powers the vectorial movement of electrons across a membrane, thus generating an electrical gradient, as well as a chemical potential gradient in the form of ‘redox’ energy (Kargul and Barber, 2011). The P680+ cation is the strongest, most abundant oxidizing species

Abbreviations: Asc, ascorbate; CET, cyclic electron transport; Chl, chlorophyll; cyt, cytochrome; DCPIP, 2,6-dichlorophenolindophenol; ETC, electron transfer cofactors; Fd, ferredoxin; FNR, ferredoxin-NADP+ reductase; H2 ase, hydrogenase; LHCI, light harvesting complex of PSI; LHCII, light harvesting complex of PSII; MA, mercaptoacetic acid; MV, methyl viologen; PC, plastocyanin; PMS, Nmethylphenazonium methyl sulphate; PSI, photosystem I; PSII, photosystem II; RC, reaction centre; ROS, Reactive Oxygen Species. ∗ Corresponding author. Tel.: +48 225542005; fax: +48 225543910. E-mail address: [email protected] (J. Kargul). 0176-1617/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.jplph.2012.05.018

known in biology (with a midpoint potential estimated at +1.25 eV) (Rappaport et al., 2002; Grabolle and Dau, 2005) that generates the most positive redox potential found in natural systems required for the thermodynamically demanding reaction of water oxidation. In contrast, P700 upon light excitation generates the most powerful naturally occurring reductant in the form of P700* (Em ∼ −1.26 eV) (Blankenship, 2002). In this way, PSI largely determines the global amount of enthalpy achievable in the living systems (Nelson, 2011). The photosynthetic RCs P680 and P700 are coupled, so as to use two photons to drive each electron through the system, providing sufficient energy to oxidize water and to reduce CO2 . Photocatalytic oxidation of substrate water molecules conducted by PSII generates not only the reducing equivalents used for production of biomass, but also the vast majority of molecular dioxygen that sustains the aerobic atmosphere on our planet. The redox coupling between both RCs occurs through the action of the cytochrome b6 f complex (cyt b6 f), which donates water-derived electrons to a soluble electron carrier plastocyanin (PC) or cytochrome c6 (cyt c6 ), and maintains formation of the electrochemical gradient across the thylakoid membrane. Photosystem I (PSI) catalyzes the light-driven vectorial electron transfer from PC or cyt c6 at the lumenal side of the thylakoid membrane, to ferredoxin (Fd) at the stromal side. Under some stress conditions that lead to cellular ATP depletion, a cyclic electron flow (CEF) around PSI is activated, whereby the reduced acceptors of PSI donate electrons to the cyt b6 f complex to produce exclusively ATP and proton gradient across the thylakoid membrane. Although significant progress has been made in identifying the molecular components of CEF, the precise molecular pathways and physiological relevance of this process in various types of photosynthetic

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organisms, especially in higher plants, are still a matter of debate. As this regulatory process is beyond the scope of this review, readers are referred to some excellent recent reviews on this topic (Kramer et al., 2004; Shikanai, 2007; Alric, 2010; Peltier et al., 2010; Johnson, 2011; Rochaix, 2011). Although a wide range of techniques has been applied to obtain structural and functional details of the PSI and PSII RCs and all the other molecular components of the photosynthetic machinery, by far the most informative has been X-ray crystallography. There are now medium-to-high resolution crystal structures of prokaryotic PSI (Jordan et al., 2001), eukaryotic PSI supercomplex with its light harvesting antenna system (LHCI-PSI) (Ben-Shem et al., 2003; Amunts et al., 2007, 2010), prokaryotic PSII (Zouni et al., 2001; Kamiya and Shen, 2003; Ferreira et al., 2004; Loll et al., 2005; Guskov et al., 2009; Umena et al., 2011), cyt b6 f (Kurisu et al., 2003; Stroebel et al., 2003; Yan et al., 2006; Yamashita et al., 2007; Baniulis et al., 2009), trimeric and monomeric light harvesting antenna systems of PSII (LHCII) (Liu et al., 2004; Standfuss et al., 2005; Pan et al., 2011), and the soluble electron carriers, including PC (Guss and Freeman, 1983; Moore et al., 1991; Redinbo et al., 1993), cyt c6 (Frazao et al., 1995; Kerfeld et al., 1995), Fd (Morales et al., 1999; Kameda et al., 2011) and ferredoxin-NADP+ reductase (FNR) (Karplus et al., 1991; Serre et al., 1996; Deng et al., 1999; Kurisu et al., 2001; Tejero et al., 2003; Muraki et al., 2010). These structures have facilitated great advancement in our detailed mechanistic knowledge of photosynthetic electron transfer, and in particular, the fundamental processes of photocatalytic water splitting and charge separation in the PSI and PSII RCs (Haumann et al., 2005; Brudvig, 2008; Cogdell et al., 2008; Sproviero et al., 2008; Siegbahn, 2011). The LH antenna systems associated with RCs of PSI and PSII allow them to operate efficiently under relatively low light intensities. The nature of the LH systems varies considerably among phototrophs, but all function to intercept light and transfer the excitation energy rapidly to the photochemical RCs. In order for the process to be efficient, the overall transfer rate must be faster than the singlet lifetimes of the pigments, which are typically in the nanosecond time domain (Cogdell et al., 2008). In fact, overall transfer times of energy migration from the LH system to the RC are in the sub-nanosecond time domain (Cogdell et al., 2008; Collins et al., 2011). The different spectral properties of the wide range of LH pigments, coupled with fine-tuning by interactions with the proteins to which they bind, allow photosynthetic organisms to absorb at all the wavelengths available in the visible part of the solar spectrum at the Earth’s surface spanning between 350 and 1000 nm (Archer and Barber, 2004; Blankenship et al., 2011).

Structure and function of PSI Protein subunits and bound cofactors The two major breakthroughs in revealing the detailed molecular organization of PSI were the 2.5-Å X-ray structure of prokaryotic PSI from the cyanobacterium Thermosynechococcus elongatus (Jordan et al., 2001; shown in Fig. 1A) and the 4.4-Å X-ray structure of the eukaryotic PSI complex with its associated light-harvesting antenna system from pea (Pisum sativum) that was subsequently refined to 3.3 A˚ (Ben-Shem et al., 2003; Amunts et al., 2007, 2010; see Fig. 1B). Detailed structural comparison of the protein backbone, inbound redox cofactors and the pigment systems in the prokaryotic and eukaryotic PSI complexes that are separated 1.5 billion years apart provided important insights into the evolution of this complex (reviewed in Schubert et al., 1998; Nelson and Ben-Shem, 2005; Sadekar et al., 2006; Amunts and Nelson, 2009; Nelson, 2011).

Fig. 1. X-ray crystal structures of prokaryotic and eukaryotic PSI. (A) 2.5-Å X-ray crystal structure of the cyanobacterial PSI from T. elongatus. Shown are the helices of several of the protein subunits, PsaA (yellow), PsaB (blue), PsaC (green), PsaD (cyan), PsaE (orange), PsaL (red), PsaF (grey), PsaK (magenta) and the cofactors (green apart from [4Fe–4S] clusters shown in red). For clarity, some subunits and cofactors are omitted. Only one monomer of the biologically active trimer is shown. The view is approximately with the threefold symmetry axis of the protein in the membrane plane. (B) 3.3 A˚ X-ray crystal structure of the higher plant LHCI-PSI from P. sativum. View is from the stromal side. Shown are the helices of several of the protein subunits with color coding as above, as well as 3 novel core subunits: PsaG (wheat), PsaH (cyan), and PsaN (pink) and the Lhca1-Lhca4 antenna subunits (green). For clarity, the stromal extrinsic subunits and some small core subunits are not shown. Figure produced from PDB coordinates 1JB0 (Jordan et al., 2001) and 3LW5 (Amunts et al., 2010) using the MBT Protein Workshop software (Moreland et al., 2005).

Cyanobacterial PSI exists predominantly as trimers in vivo (Kruip et al., 1994; Karapetyan et al., 1999; Jordan et al., 2001), although monomeric, dimeric and tetrameric forms of this complex have also been reported in prokaryotic phototrophs (Rögner et al., 1990; Kruip et al., 1994; Karapetyan et al., 1999; El-Mohsnawy et al., 2010; Watanabe et al., 2011). In contrast, eukaryotic PSI is always monomeric (Scheller et al., 2001; Busch and Hippler, 2011). The LHCI-PSI supercomplex has a molecular mass of ∼600–770 kDa (including the inbound cofactors) and is composed of two structural and functional domains: the core (or reaction centre complex of estimated molecular mass of 310–356 kDa excluding the inbound cofactors), in which the bulk of light capturing and charge separation occurs, and the external (peripheral) antenna system that increases the light-harvesting capacity of PSI and transmits quanta of solar energy to the core antenna, and ultimately, to the P700 RC. While the PSI core is highly conserved throughout evolution, with differences mainly in some small intrinsic core subunits (Jordan et al., 2001; Ben-Shem et al., 2003), the light-harvesting system varies considerably between species with respect to its subunit and pigment composition, and stoichiometry, reflecting

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evolutionary adaptation of photosynthetic organisms to diverse ecological niches (Collins et al., 2011; Busch and Hippler, 2011). In green algae and higher plants, the outer antenna is composed of at least 4 nuclear-encoded Chla/b-binding Lhca proteins that form the crescent-shaped light harvesting complex I (LHCI) asymmetrically attached to the core domain (Scheller et al., 2001; Ben-Shem et al., 2003; Kargul et al., 2003, 2005; Drop et al., 2011; Busch and Hippler, 2011). In chromalveolates, the LHCI complex is formed by the Chla/c-binding proteins, for example the diatom fucoxanthin-chlorophyll-proteins (FCPs), which bind Chlc instead of Chlb and fucoxanthin instead of lutein (Durnford et al., 1999; Veith and Büchel, 2007; Veith et al., 2009; Neilson and Durnford, 2010). In the red algae Rhodophyta the LHCI antenna is composed of a varying number of exclusively Chla-binding Lhcr proteins (Gardian et al., 2007; Busch et al., 2010; Thangaraj et al., 2011; see Fig. 2A). For a more detailed overview of the various types of the LHCI antenna systems, the reader is advised to refer to an excellent recent review by Busch and Hippler (2011). In the crystallographic model of a higher plant LHCI-PSI supercomplex, the outer LHCI antenna “belt” is composed of 4 Lhca subunits that asymmetrically attach to the core domain on the PsaF/PsaJ side, as shown in Fig. 1B (Ben-Shem et al., 2003; Amunts et al., 2007, 2010). This is the central building block of the plant and green algal outer light-harvesting antenna, which is organized as two functional heterodimers composed of Lhca1–Lhca4 and Lhca2–Lhca3 subunits (Croce et al., 2002; Ben-Shem et al., 2003), although 2–7 additional Lhca subunits may associate with this basic peripheral antenna system (Germano et al., 2002; Kargul et al., 2003, 2005; Ganeteg et al., 2004; Storf et al., 2004; Lucinski et al., 2006; Stauber et al., 2009; Drop et al., 2011). In addition to its function in light harvesting, the LHCI complex has an important role in photoprotection, since the production of the Reactive Oxygen Species (ROS) and photoinhibition are unavoidable outcomes of oxygenic photosynthesis at all light intensities (Ruban and Johnson, 2010). LHCI has been suggested to act as a safety valve under the conditions of high light illumination, when overexcitation of both photosystems can occur. This is due to the presence of the red-shifted Chl molecules in the LHCI complex and the PSI core antenna that absorb light above 700 nm and act as excitation sinks enabling an uphill energy transfer to the P700 reaction centre (Croce et al., 2000; Ihalainen et al., 2002; Jennings et al., 2003; Melkozernov et al., 2004, 2005). In cyanobacteria, the peripheral light harvesting antenna is formed by large water-soluble phycobilisome complexes that attach to the PSI core on the stromal side of the thylakoid membrane (Glazer, 1985; MacColl, 2004; Murray et al., 2006). Under some conditions such as low availability of iron, the peripheral antenna system is dominated by an intrinsic Chla-binding protein complex made up of 1–2 rings of 18–43 copies of the CP43-like IsiA subunits (Bibby et al., 2001a,b; Boekema et al., 2001; Nield et al., 2003; Yeremenko et al., 2004; Kouril et al., 2005a; Chauhan et al., 2011) that enclose trimeric PSI. A similar antenna system is found in the cyanobacteria known as prochlorophytes, which use Chla/Chlb-binding Pcb proteins, as shown in Fig. 2D (Bibby et al., 2001c, 2003a,b). The Pcb and IsiA proteins are structurally related to each other and to CP43, CP47 and the N-terminal domains of the PSI RC proteins, PsaA and PsaB (La Roche et al., 1996; Green and Durnfold, 1996; Barber et al., 2006). Iron limitation leads to fast degradation of photosynthetic RCs, which all contain iron in haem and [4Fe–4S] clusters. The most severely affected is cyanobacterial PSI, as it is the largest sink of iron, with 36 Fe atoms in nine [4Fe–4S] clusters per PSI trimer, associated with additional [2Fe–2S] clusters in multiple copies of Fd (Jordan et al., 2001). During iron deprivation, induction of IsiA expression occurs by de-repressing the isiAB operon which encodes the IsiA (CP43 ) antenna subunit and IsiB (flavodoxin) proteins.

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The latter functionally replaces Fe-containing Fd. The main role of the multiple IsiA rings is to significantly increase the functional antenna or absorption cross-section, which compensates for degradation of PSI RCs under Fe limitation (Andrizhiyevskaya et al., 2002; Melkozernov et al., 2003; Chauhan et al., 2011). Significant remodeling of the photosynthetic apparatus upon iron starvation also occurs in photosynthetic eukaryotes. Iron limitation in the green alga Chlamydomonas reinhardtii results not only in pronounced degradation of the PSI RCs, but also in gradual dissociation of the LHCI antenna subunits and a transient increase of the functional LHCII antenna, the latter acting as a pigment buffer and storage (Moseley et al., 2002; Naumann et al., 2005, 2007). A similar phenomenon is observed in red algae and diatoms, whereby the iron stress induces reduction of the functional antenna of PSI (Desquilbet et al., 2003; Doan et al., 2003; Allen et al., 2008; Juhas and Büchel, 2012). Thus, a decrease of the PSI absorption cross-section seems to serve as a general mechanism of reducing photo-oxidative damage to the eukaryotic photosynthetic apparatus. While the cyanobacterial PSI core complex in the absence of IsiA or Pcb proteins comprises 12 subunits harboring 96 Chls per monomer (Jordan et al., 2001), the higher plant PSI is considerably larger, containing at least 15 core subunits (PsaA to PsaL and PsaN to PsaP, with the PsaO and PsaP proteins absent in the currently available the X-ray structures), at least 4 stably associated Lhca antenna subunits and a total of 173 Chl and 15 carotenoid molecules, as shown in Fig. 1B (Ben-Shem et al., 2003; Amunts et al., 2007, 2010). Most of the additional Chls present in the plant LHCIPSI supercomplex over and above those within the cyanobacterial PSI are associated with the four Lhca antenna subunits or belong to the “linker” and “gap” Chls that facilitate energy transfer within the LHCI antenna and between the LHCI antenna and the RC (Ben-Shem et al., 2003). The twelve subunits of the cyanobacterial core domain include 9 intrinsic polytopic subunits (PsaA, PsaB, PsaF, PsaI, PsaJ, PsaK, PsaL, PsaM and PsaX) and 3 extrinsic stromal subunits (PsaC, PsaD and PsaE), as presented in Fig. 1A. The central part of the core complex is formed by a highly conserved heterodimer of the PsaA and PsaB subunits which bind the majority of the electron transfer cofactors (ETCs), antenna and lipid cofactors. The N-termini of both RC subunits are oriented toward the stroma, whereas the C-termini are exposed toward the thylakoid lumen. Both subunits contain 11 transmembrane helices that are divided into the N-terminal domain composed of six ␣helices (A/B-a to A/B-f) and a C-terminal domain containing five ␣-helices (A/B-g to A/B-k; nomenclature according to Jordan et al., 2001). The latter form two interlocked semicircles enclosing the ETCs, including 6 Chla molecules, two phylloquinones, and a single [4Fe–4S] iron–sulphur cluster, termed FX (Jordan et al., 2001; Ben-Shem et al., 2003). Two other [4Fe–4S] clusters (FA and FB ) are bound to the PsaC subunit located on the stromal side of the complex. This subunit is evolutionarily related to the class of bacterial Fds (Antonkine et al., 2003). Fifteen ␤-carotenoids were identified in the 3.3 A˚ structure of the higher plant PSI (Amunts et al., 2010), whereas 30 ␤-carotenoids were built into the model of the cyanobacterial PSI (Jordan et al., 2001). All the ETCs are arranged in two symmetric branches along the crystallographic pseudo-C2 axis, as depicted in Fig. 3. The other intrinsic subunits are peripheral to the PsaA/B heterodimer and coordinate some of the inner antenna cofactors (Jordan et al., 2001; Amunts et al., 2010). While the higher plant core domain retains the location and orientation of the ETCs and its protein backbone is structurally very similar to the cyanobacterial PSI RC, it does not have the X and M subunits. Instead, 4 additional core subunits are present exclusively in higher plants and green algae, namely subunits PsaG, PsaH, PsaN, and PsaO (Scheller et al., 2001; Green and Durnfold, 1996; Knoetzel et al., 2002). These subunits play specific roles in association of the

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Fig. 2. Top view projections of various types of LHC-PSI supercomplexes derived from electron microscopy and single particle analysis. (A) Stromal top view of the LHCI-PSI supercomplex from the thermoacidophilic red alga Galdieria sulphuraria with an overlay of the X-ray structure of plant LHCI-PSI (Thangaraj et al., 2011). The crescent-shaped area highlighted in green is suggested to contain 4–5 additional Lhcr subunits over and above the four Lhca subunits in the plant X-ray structure. Scale bar, 10 nm. (B) Projection map for the LHCI–PSI supercomplex isolated from Chlamydomonas reinhardtii cells induced to State 2 with an overlay of the plant PSI X-ray structure (Kargul et al., 2005). Modeling is based on higher plant PDB coordinates 1QZV (Ben-Shem et al., 2003) with PSI core (green), LHCI antenna (red), PsaJ (yellow), PsaK (magenta), PsaG (purple), PsaI (orange), PsaL (cyan) and PsaH (white). Chlorophylls are shown in yellow. The additional density observed in State 2 LHCI–PSI supercomplex is able to accommodate an additional LHC subunit (blue) attributed to phospho-CP29. Scale bar, 5 nm. (C) Stromal top view projection map of the IsiA–PSI supercomplex isolated from iron-starved cyanobacterium Synechocystis PCC 6803 with an overlay of the X-ray crystal structure of the trimeric PSI from T. elongatus. The supercomplex is formed by a PSI trimer within the centre of an 18-mer ring of the Chla-containing the IsiA subunits (Bibby et al., 2001a). Scale bar, 5 nm. (D) Projection of the top view of the Pcb–PSI supercomplex isolated from marine oxyphotobacteria Prochlorococcus marinus, strain SS120. The antenna ring of 18 Pcb Ca/b subunits surrounds a trimeric PSI reaction centre (Bibby et al., 2001c). Scale bar, 5 nm.

LHCI antenna complex (such as PsaG; Ben-Shem et al., 2003) or docking of a mobile fraction of the LHCII complex, during photosynthetic state transitions (subunits PsaH, and PsaO; Kargul and Barber, 2008). Interestingly, a single transmembrane helix adjacent to PsaL and corresponding to the PsaH subunit has been shown to bind one Chl molecule (Ben-Shem et al., 2003; see Fig. 1B). This subunit most likely forms a docking site for the mobile LHCII complex that transiently attaches with the PSI core during state transitions, under conditions favoring excitation of PSII (Lunde et al., 2000; Kouril et al., 2005b; Kargul et al., 2005; Kargul and Barber, 2008). On the opposite side of the core complex the 2-TM PsaG subunit provides the contact surface area for the association of the belt-shaped LHCI (Ben-Shem et al., 2003), as shown in Fig. 1B. The precise role of the lumenal PsaN subunit is still debatable. In the latest 3.3-Å X-ray structure of plant LHCI-PSI, it seems to interact with the Lhca2 and Lhca3 subunits, thus potentially stabilizing the formation of this antenna heterodimer (Amunts et al., 2010). It has also been suggested to be indirectly involved in binding of PC by providing the correct orientation of the N-terminal domain of PsaF, the docking site for this electron carrier (Haldrup et al., 1999, 2000; Jensen et al., 2007), although the 3.3-Å X-ray structure of LHCI-PSI seems to preclude the direct interaction of PsaN and PsaF.

PsaN has also been proposed to bind the minor Lhca subunit Lhca5 (Storf et al., 2005; Lucinski et al., 2006) which, together with Lhca6, is important for the formation of the PSI-NADH dehydrogenase-like (NDH) complex during the cyclic electron transport (CET) around PSI in higher plants (Peng et al., 2008, 2009; Peng and Shikanai, 2011). Interestingly, some cyanobacterial core subunits have been retained in the PSI core of the eukaryotic chromalveolates and red algae. In contrast to higher plants, the plastid genome of the diatom P. tricornutum contains the PsaM subunit, which is suggested to enable trimerization of PSI in cyanobacteria and facilitate energy transfer between monomers of the cyanobacterial PSI trimer (Grotjohann and Fromme, 2005), albeit with sequence identity of only 50% (Veith and Büchel, 2007). Similar to diatoms, red algae retained the cyanobacterial PsaM subunit, as shown by the recent plastid genome analysis of a primitive unicellular red microalga Galdieria sulphuraria (Vanselow et al., 2009). Notably, some higher plant PSI RC subunits are absent in other eukaryotic PSI complexes. The PsaG subunit that provides a docking site for the LHCI antenna assembly in higher plants and green algae has not been identified in diatoms (Armbrust et al., 2004) or red algae (Matsuzaki et al., 2004; Vanselow et al., 2009). Similarly,

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Fig. 3. Electron transfer cofactors of PSI. Arrangement of the electron transport cofactors (ETCs) in cyanobacterial PSI from T. elongatus viewed along the membrane plane. The cofactors of the ETCs are related by the pseudo-symmetry C2 axis passing through FX , and oriented normal to the paper plane. Nomenclature according to Jordan et al. (2001). eC-A1/B1: a primary electron donor; eC-A2/B2, accessory Chls; eC-A3/B3 Chls, A0 primary electron acceptor in P700; QK -A and QK -B, A1 phylloquinones which are secondary electron acceptors in P700; FX , FA , FB : [4Fe–4S] clusters, the latter two shown within the backbone of PsaC (pink). Figure produced from PDB coordinates 1JB0 (Jordan et al., 2001) using the PyMOL molecular graphics system (DeLano, 2002).

the PsaH subunit, important in state transitions in green algae and higher plants, is also absent in the genomes of diatoms and red algae. In addition, green algae lack a gene coding for PsaP (Jensen et al., 2007). In red algae, the PsaL and PsaF core subunits are of a chimeric nature. While the cyanobacterial PsaL, with its extended Cterminus protruding from the RC, is essential for PSI trimer formation (Chitnis and Chitnis, 1993; Jordan et al., 2001), its higher plant counterpart forms, together with the PsaH subunit, the mobile LHCII docking site during the adaptation process of state transitions (Haldrup et al., 2000). This extended C-terminal domain of PsaL is absent in plants and algae (Ben-Shem et al., 2003), in agreement with the exclusively monomeric character of eukaryotic PSI. The conserved sequences required for PSI trimerization in cyanobacteria (the C-terminal helix and the Ca2+ -binding site) and the plant-specific motifs for PsaH interaction are absent in the PsaL subunit of G. sulphuraria (Vanselow et al., 2009). The chimeric nature of PsaF in G. sulphuraria is emphasized by a striking homology of its N-terminal domain to the higher plant counterpart and the presence of the conserved cyanobacterial-like motifs at the C-terminus. The N-terminal domain of G. sulphuraria PsaF contains the positively charged Lys-rich motif that is essential for tight docking of PC and cyt c6 in plants and green algae (Hippler et al., 1996, 1998, 1999). The conserved C-terminal extension of G. sulphuraria PsaF has been suggested to interact with the peripheral antenna composed of both LHCI subunits and phycobilisomes (Vanselow et al., 2009), although the latter remains to be confirmed experimentally. Similar to cyanobacteria, G. sulphuraria and other red algae such as Cyanidioschyzon merolae lack a gene for PC, but exclusively use the more ancient cyt c553 as a soluble electron carrier donating electrons to the photo-oxidized P700+ (Matsuzaki et al., 2004; Vanselow et al., 2009). The majority of the core pigments (87 and 90 Chla, as well as 15 and 22 ␤-carotenoid molecules in higher plants and cyanobacteria,

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Fig. 4. Structural similarity of the N-terminal domain of PSI and PSII RC. The N-terminal domain of the PSI RC heterodimer composed of 6 TMs of the inner peripheral antenna of PSI is aligned with the CP43/CP47 inner antenna complex of PSII. Shown are the backbones of the protein subunits: D1 (cyan), D2 (blue), CP43 (red), CP47 (orange), N-terminal domain of PsaA (deep purple) and N-terminal domain of PsaB (yellow). The views are approximately with the twofold symmetry axis of the protein in the membrane plane. The coordinates are 1S5L (Ferreira et al., 2004), and 1JB0 (Jordan et al., 2001). Figure produced from PDB coordinates using the PyMOL molecular graphics system (DeLano, 2002). Figure adapted from Kargul and Barber (2011).

respectively) act as light-harvesting antenna coordinated mainly by the PsaA/B heterodimer aided by some small intrinsic core subunits (Jordan et al., 2001; Ben-Shem et al., 2003; Amunts et al., 2007, 2010). Two types of inner antenna can be distinguished in the PSI RC: the innermost ‘central antenna’ of 43 Chls forming a circle around the ETCs at a distance not less than ∼18 A˚ flanked by 2 layers of ‘peripheral inner antenna’ of 18 Chls each that are bound predominantly to the N-terminal domains of the PsaA/B heterodimer (Jordan et al., 2001). The crystal structure of plant LHCI-PSI indicates that the majority of the RC Chls retained the same position and tilting angle as in the cyanobacterial PSI, indicating a high degree of conservation of the PSI RC even after 1.5 billion years of evolution (Jordan et al., 2001; Ben-Shem et al., 2003). The structures of the N-terminal domains of PsaA and PsaB are equivalent to those of CP43 and CP47 inner antenna subunits of PSII, whereas, the organization of the five TM helices of the C-terminal domains of PsaA and PsaB is similar to that of the D1 and D2 subunits of the PSII RC (Schubert et al., 1998; Barber et al., 1999; Kargul and Barber, 2011; see Fig. 4), indicating a common evolutionary origin of both types of RCs (Ben-Shem et al., 2004; Nelson and Ben-Shem, 2005; Amunts and Nelson, 2009; Hohmann-Marriott and Blankenship, 2011; Kargul and Barber, 2011). Moreover, distribution of the peripheral antenna Chls bound to the N-terminal domains of PsaA and PsaB is similar to that of the CP43 and CP47. The C-terminal domains of PsaA and PsaB jointly coordinate 25 Chla molecules of the peripheral and central antenna (Jordan et al., 2001) whose position is optimized to mediate energy transfer to P700 and fast trapping of excitation energy in the PSI RC. On the lumenal (donor) side of PSI, the docking site for the mobile electron donors, cyt c6 or PC is formed by the ␣-helices of loops A/B-ij of the PsaA/B heterodimer containing 2 conserved Trp residues, as shown in Fig. 5. The plant PsaF subunit contains the N-terminal domain that is longer compared to its cyanobacterial counterpart. This extended domain forms the amphipathic Lys-rich ‘helix–loop–helix’ motif (Ben-Shem et al., 2003) that enables strong electrostatic interaction with the acidic regions (negative patch) of PC and, as a consequence, two orders of magnitude faster electron transfer from this mobile electron carrier to P700+ in higher plants compared to cyanobacteria (Hippler et al., 1996, 1998).

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transfer between the [2Fe–2S] cluster of Fd and the distal FB cluster of PSI (Fischer et al., 1998, 1999; Ruffle et al., 2000; Bottin et al., 2001; Sétif et al., 2002; Antonkine et al., 2003). The P700 RC and electron transfer chain

Fig. 5. Structural basis of PSI interaction with plastocyanin and ferredoxin. Presented is 3.3-Å X-ray crystal structure of higher plant photosystem I (Amunts et al., 2010; PDB coordinates 3LW5). Shown are P700 reaction centre and the electron transfer cofactors (color coding as in Fig. 3) coordinated by subunits PsaA (yellow) and PsaB (blue). For clarity all but two of 11-transmembrane helices of the PsaA and PsaB protein bundle are omitted. At the vertex of the P700-coordinating helices shown are Trp658 of PsaA and Trp625 of PsaB (both in black) forming lumenal hydrophobic patch. Functionally important N-terminal Lys residues (Lys16, Lys23 and Lys30; Hippler et al., 1998) of PsaF (gray) are indicated. They form a positively charged patch of electrostatic potential (marked as blue mesh). Both electrostatic and hydrophobic interactions are important for docking of cyt c6 or plastocyanin, PC (cyan). Plastocyanin 1.50-Å X-ray crystal structure (Redinbo et al., 1993; PDB coordinates 2PLT) shows two negatively charged patches Asp42/Glu43/Asp44 and Asp59/Asp60, generating negatively charged electrostatic potential (red mesh). Mutation in the first patch impairs binding to PSI (Hippler et al., 1996). Binding of electron donor occurs when the negatively charged residues in the first patch interact with positively charged residues in the PsaF subunit aided by the hydrophobic area formed by Trp659 and Trp625 residues of the PsaA/B heterodimer. The electrons are then energized and transported further to iron–sulphur clusters in sequence FX , FA , and FB (red cubes) where they arrive at the electron acceptor docking side formed by extrinsic subunits PsaC, PsaD and PsaE. All three units contribute to the ferredoxin (Fd) docking with positively charged residues. The key-charge residues (black) in PsaC are Lys35/Gly36/Lys51/Arg52, in PsaC His97/Asp98/Lys103/Arg108 and PsaE Arg40. Those residues form a dent on the stromal side of PSI and generate positively charged electrostatic potential shown as blue mesh. The 1.46-Å X-ray crystal structure (Kameda et al., 2011, PDB coordinates 3AV8) of Fd (magenta) is placed in the vicinity of the docking site and faces toward PSI with negatively charged residues generating electrostatic potential (shown as red mesh). Mutations in residues Asp66/Asp67 (not shown) deplete efficiency of binding with FNR. The iron–sulphur cluster of Fd acts as the electron acceptor centre (red rectangle).

On the stromal (acceptor) side of PSI, the binding pocket for the mobile electron acceptors Fd or flavodoxin is formed jointly by the extrinsic PsaC, PsaD and PsaE subunits, as shown in Fig. 5. These three stromal subunits, which are highly conserved throughout evolution, play distinctive roles in binding of Fd, with PsaD providing the electrostatic guidance of Fd into the PSI binding pocket, PsaE (with its Arg39) stabilizing the molecular electron transfer complex of Fd and PSI, and PsaC (with its Lys35), forming a close protein-protein interaction that is essential for fast electron

As briefly discussed in the previous section, comparison of the crystallographic structures of cyanobacterial and higher plant PSI complexes shows a remarkable similarity in the organization and specific binding sites of the ETCs. This functionally most important part of PSI is formed by six Chla molecules, two phylloquinones and three [4Fe–4S] clusters, as shown in Fig. 3. The Chls and phylloquinones are arranged along two branches, A and B, as pairs of pseudo-dimers related by the pseudo-symmetry C2 axis and coordinated to the side chains of the PsaA/B heterodimer (Jordan et al., 2001; Ben-Shem et al., 2003). Branch A is composed of Chls eC-A1, eC-B2, eC-A3 and a phylloquinone QK -A, whereas branch B contains Chls eC-B1, eC-A2, eC-B3 and a phylloquinone QK -B (nomenclature according to Jordan et al., 2001). The two branches join again at the [4Fe–4S] cluster FX which is followed by the two additional [4Fe–4S] clusters FA and FB , both of which are coordinated by side chains of the stromal extrinsic subunit, PsaC. It is now widely accepted that both branches in the PSI RC are active in electron transfer, albeit operating with different kinetics, as shown by numerous transient optical spectroscopy measurements coupled to mutagenesis of the ETC coordinating ligands (Guergova-Kuras et al., 2001; Ramesh et al., 2004; Bautista et al., 2005; Dashdorj et al., 2005; Poluektov et al., 2005; Santabarbara et al., 2005, 2008; Li et al., 2006; Müller et al., 2010). The rate constants are 35 × 106 × s−1 and 4.4 × 106 s−1 for the electron transfer steps from each phylloquinone to FX (Joliot and Joliot, 1999; Guergova-Kuras et al., 2001). It appears that branch A is about 10-fold slower than branch B, despite the faster initial charge separation (Guergova-Kuras et al., 2001; Müller et al., 2010). Although both branches participate in electron transfer, branch A appears to be a dominating one with a branch A/branch B ratio varying from 3:3 in green algae to ∼4:1 in cyanobacteria (Ramesh et al., 2004; Dashdorj et al., 2005; Li et al., 2006; Müller et al., 2010). The photochemical RC of PSI comprises a cluster of 6 Chla molecules that function as the primary electron donors and primary electron acceptors. The primary electron donor of PSI RC, the so-called P700 (Em of ∼0.5 eV), is formed by the ‘special’ pair of the eC-A1/eC-B1 Chls that are excitonically tightly coupled with a Mg–Mg distance of 6.6 A˚ (Jordan et al., 2001). The chlorin planes of the P700 Chls are oriented perpendicular to the membrane plane and form a stacked dimer with a 3.6 A˚ interplanar distance. This organization varies from the ‘special pair’ of the purple bacterial RC where the Mg–Mg distance is larger at 7.6 A˚ (Allen et al., 1987; Deisenhofer et al., 1995). In contrast to the homodimeric bacterial special pair, P700 Chls form a heterodimer, with eC-A1 being Chla 13 -epimer (Watanabe et al., 1985; Jordan et al., 2001). The heterodimeric nature of P700 primary electron donor is also reflected by the presence of hydrogen bonds within the binding pocket of eC-A1 and lack of those in the binding site of eC-B1 (Jordan et al., 2001). The other two Chla pairs are composed of the eC-B2/eC-A2 and eC-A3/eC-B3 (Jordan et al., 2001). The eC-A/B-2 Chls represent the so-called ‘accessory’ Chls, which despite being resolved in the X-ray structures were functionally resolved by spectroscopic methods only recently (Slavov et al., 2008; Müller et al., 2010). The eC-A/B-3 Chls are commonly referred to as A0 (Em of −1.0 eV), which represents the primary electron acceptor reduced in less than 10 ps, as observed by the spectroscopic measurements (Santabarbara et al., 2010). Recently, Holzwarth and colleagues proposed an alternative mechanism for the primary charge separation, whereby the first radical pair would form within the accessory Chls

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Table 1 Rates of hydrogen production from various types of PSI-hybrid nanodevices. PSI-biomimetic nanoconstruct

Maximum rate of H2 production (␮mol H2 mg Chl−1 h−1 )

References

Covalently linked PC to platinized S. oleracea PSI PSI and T. roseopersicin [NiFe]-H2 ase in-solution system PSI-R. eutropha [NiFe]-H2 ase hybrid complex Platinized S. oleracea PSI Au nanoparticle wired to PsaC-rebuilt Synechococcus sp. PCC 7002 PSI Platinized T. elongatus PSI, cyt c6 In vitro PC/PSI/PetF/HydA1 reconstitution system Pt nanoparticle wired to PsaC-rebuilt PSI of Synechococcus sp. PCC 7002, cyt c6 PC-PSI-Pt nanoparticle complex with 1,6-hexanedithiol molecular wire Cobaloximized S. leoploliensis/S. lividus PSI, cyt c6 PC-PSI-Pt nanoparticle complex with 1,4-benzenedithiol molecular wire cyt c6 -PSI-C. acetobutylicum [FeFe]-H2 ase complex Au electrode-immobilized PSI-R. eutropha [NiFe]-hydrogenase hybrid complex

0.09 0.50 0.58 2.0 3.4 5.5 16 49.3 100.6 246 312 2200 3000

Evans et al. (2004) Qian et al. (2008) Ihara et al. (2006) Millsaps et al. (2001) Grimme et al. (2008) Iwuchukwu et al. (2010) Winkler et al. (2009) Grimme et al. (2008) Grimme et al. (2009) Utschig et al. (2011a) Grimme et al. (2009) Lubner et al. (2011) Krassen et al. (2009)

eC2+ eC3− of either branch rather than in the P700 ‘special pair’ (Holzwarth et al., 2006). This radical pair would then be re-reduced by the P700. This postulate is based on ultrafast transient absorption measurements in intact LHCI-PSI particles from a green alga C. reinhardtii (Holzwarth et al., 2006) and a higher plant Arabidopsis thaliana (Slavov et al., 2008). The A0 Chls are adjacent to a pair of phylloquinone molecules (often referred to as A1 ) termed QK -A and QK -B according to Jordan et al. (2001). The A1 phylloquinones (Em of −0.8 eV) act as secondary electron acceptors that are rapidly reduced to the phyllosemiquinone radicals in ∼20–40 ps (Santabarbara et al., 2010). All the amino acid ligands coordinating the eC-2 and eC-3 Chla pairs are highly conserved within PsaA and PsaB from cyanobacteria to higher plants, indicating that throughout evolution these interactions are essential for fine-tuning the redox potentials of the ETC. An interesting exception is the marine cyanobacterium Acaryochloris marina which carries out oxygenic photosynthesis but contains over 95% red-shifted Chld (with the in vivo absorbance maximum of ∼710 nm) and only trace amounts of Chla in both photosystems (Miyashita et al., 1996; Hu et al., 1998; Tomo et al., 2007). Chld provides a potential selective advantage because it enables Acaryochloris to use infrared light (700–750 nm) that is not absorbed by Chla in the far-red light-enriched habitat of this organism (Chen and Blankenship, 2011). Consequently, the primary donor of PSI, the so-called P740, is a dimer of Chld molecules. Similarly, Chld replaces Chla for A0 and A1 . The electron acceptor from A1 is the [4Fe–4S] cluster, the socalled FX (Evans and Cammack, 1975; Evans et al., 1976; Golbeck et al., 1987; McDermott et al., 1989), which, similar to P700, is located at the interface of the PsaA/B heterodimer. The FX cluster (Em of −0.7 eV) is ligated by 4 strictly conserved Cys residues present in the loop segments A/B-hi of the PsaA/B heterodimer (Jordan et al., 2001). The two terminal [4Fe–4S] iron–sulphur clusters FA and FB , which operate in series, are coordinated by Cys residues present within the conserved regions of the stromal extrinsic PsaC subunit (Jordan et al., 2001). PSI in biomimetic solar-to-fuel nanodevices In-solution PSI-hybrid systems for solar-to-hydrogen production PSI operates with a quantum yield close to 1.0 and to date, no man-made synthetic system has approached this remarkable efficiency. Despite high structural complexity, PSI operates as an almost perfect Einstein photoelectric device (Nelson, 2009; Amunts and Nelson, 2009). This means that each quantum of light harvested by the PSI antenna system reaches the P700 photochemical RC, ultimately creating the primary radical pair species and an ultrafast charge separation within a few picoseconds (Diner and

Rappaport, 2002; Santabarbara et al., 2010). As a result, for each quantum of light absorbed by P700, a single electron is ejected from the primary electron donor. These inherent light-harvesting and electron-transfer properties of natural PSI make this macromolecular complex amenable for hydrogen production in the solar-to-fuel biomimetic devices. As PSI forms an exceptionally long-lived charge-separated state P700+ FB − (∼60 ms) and is characterized by an exceptionally low redox potential associated with the distal FB cluster (Em of −0.58 eV), it provides a sufficient driving force to reduce protons to H2 at neutral pH (Lubner et al., 2010a). For these reasons, there is significant interest in utilizing the highly stable natural PSI for generation of solar fuels (Blankenship et al., 2011). Over the last decade, the reported H2 -evolving PSI-hybrid systems consisted of solubilized individual components of electron transfer. Consequently, the rates of electron transfer between the interacting constituents were severely limited by diffusion. Nonetheless, these in vitro systems have provided the chemical and biochemical blueprints for development of the more efficient solidstate systems that operate at significantly improved H2 -evolution rates, as summarized in Table 1 and Fig. 6. One of the early examples of such in vitro H2 -evolving systems was based on platinization of the native PSI RCs isolated from Spinacia oleracea (Millsaps et al., 2001). At neutral pH and room temperature metallic platinum can be photoprecipitated on the reducing side of PSI according to the chemical reaction: [PtCl6 ]2− + 4e− + 4hv

Pt(s) + 6Cl−

The Hill reaction of photosynthesis, which reduces ferric ions to ferrous ions, forms the basis for the photoprecipitation of metallic platinum onto the external surfaces of isolated PSI complexes (Lubner et al., 2010a). Subsequently, in the four-step reducing process, PSI-derived electrons interact with Pt clusters to generate molecular H2 . Following illumination of the mixture containing hexachloroplatinate ([PtCl6 ]2− ), purified spinach PSI cores, PC (as a soluble natural electron donor to photooxidized P700+ ) and an ascorbate (Asc) (as a sacrificial electron donor to PC), the Pt cations underwent a four-step reduction to metallic Pt(s). Overall, such a system achieved a rather modest rate of 2 ␮mol H2 mg Chl−1 h−1 (Millsaps et al., 2001). Nevertheless, it exceeded 10-fold the efficiency of the previously reported platinized thylakoid-based systems (Greenbaum, 1985; Lee et al., 1994, 1998). A rather elegant diffusion-based system for biomimetic H2 production was reported by Bruce and colleagues who employed platinized highly stable trimeric PSI complexes from the thermophilic cyanobacterium T. elongatus as a photocathodic component of the system (Iwuchukwu et al., 2010). By employing cyt c6 as a natural electron donor to photooxidized PSI RC, the authors

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Fig. 6. Biomimetic H2 -producing PSI nanodevices. (A) Photocatalytic system of H2 production from a PSI-cobaloxime hybrid complex. Two successive photogenerated electrons are necessary for the catalyst to produce one H2 molecule. The electron donors depicted are Asc and cyt c6 (Utschig et al., 2011a). (B) In-solution hydrogen evolution system composed of PSI, H2 ase, MA as electron donor and MV as electron acceptor (Qian et al., 2008). (C) Photocatalytic H2 -evolving system of platinized PSI with covalently linked plastocyanin (PC). The covalent linker is 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide hydrochloride (blue stick). Ascorbate serves as a sacrificial electron donor (Evans et al., 2004). (D) PSI-molecular wire-[FeFe]-H2 ase nanodevice. The wire here is 1,6-hexanedithiol (red line). Cyt c6 was cross-linked with a zero-length cross-linking agent to limit diffusion-based electron transfer to P700+ . The arrow indicates the directionality of electron transfer, including reduction of protons to H2 by H2 ase (Lubner et al., 2011). (E) Bioconjugate consisting of PC cross-linked to PSI, 1,4-benzendithiol as the molecular wire (red line) and a platinum nanoparticle catalyst, DCPIP was employed as the sacrificial electron donor (Grimme et al., 2009). (F) Au surface-immobilized PSI-[NiFe]-H2 ase photocathode. The Ni-NTA functionalized Au electrode strongly binds His-tagged PSI (His6 -tag engineered on PsaF illustrated as a yellow anchor) and provides electrons to reduce the oxidized form of PMS as the electron donor to P700+ . Functionality of PsaE-null mutant of Synechocystis PSI is restored by binding the MBH-PsaE fusion protein from Ralstonia eutropha. The electrons transfer from the FB cluster at the PSI acceptor side to the distal iron–sulphur cluster of the [NiFe]-H2 ase and further to its active site, where protons are reduced to molecular hydrogen (Krassen et al., 2009). Biomimetic devices depicted in panels A, B, D and F include the 2.5-Å X-ray crystal structure of the cyanobacterial PSI from T. elongatus (Jordan et al., 2001). Shown are the helices of PsaA (yellow), PsaB (blue), PsaC (green), PsaD (cyan), PsaE (light brown), PsaF (grey), PsaL (red), PsaK (magenta) and the cofactors (Chls, green; [4Fe–4S] clusters, red). Only one monomer of the biologically active trimer is shown. Panels C and E show the 3.3 A˚ X-ray crystal structure of higher plant PSI from P. sativum

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reported increased efficiency of hydrogen production compared to the system without cyt c6 . The hydrogen production, although of a modest rate of ∼5.5 ␮mol H2 h−1 mg Chl−1 , was remarkably stable and sustained for over 85 days at temperatures elevated to 55 ◦ C, with no apparent decrease in hydrogen yield when tested intermittently. Recently, Utschig, Tiede and colleagues reported an alternative H2 -producing in vitro system using a self-assembled complex of cyanobacterial PSI isolated from Synechococcus and cobaloxime as the efficient proton reduction electrocatalysts (Utschig et al., 2011a) in the presence of cyt c6 as a natural electron donor to P700+ (see Fig. 6A). Cobaloximes are pseudomacrocyclic bis(dimethylglyoxamato)cobalt complexes that were originally developed as vitamin B12 alternative and discovered to perform electrochemical proton reduction (Bakac et al., 1986; Razavet et al., 2005). In this way, inexpensive and earth-abundant metal was used for the first time as the proton reduction module operating in tandem with natural PSI as the photocatalytic module. Notably, the hydrogen evolution rate for the PSI-cobaloxime hybrid complex was shown to match that of the best reported for the cyt c6 -PSIPt nanoparticle hybrid system (246 ␮mol H2 mg Chl−1 h−1 ), when recorded by the same authors under equivalent illumination conditions (Utschig et al., 2011a,b). Another group of attractive molecular catalysts that has been widely used in the biomimetic H2 -producing nanodevices are the hydrogenase (H2 ase) enzymes, which can be linked with synthetic photosensitizers or PSI as the natural photocatalytic module. H2 ases are generally divided into three independently evolved classes termed [Fe]-, [FeFe]- and [NiFe]-H2 ases (Lubitz et al., 2007; Vignais and Billoud, 2007; Fontecilla-Camps et al., 2007, 2009). [FeFe]-H2 ases are found in bacteria and Eucarya, whereas [NiFe]H2 ases are found in bacteria and Archaea. A third type of H2 ases, mononuclear [Fe]-H2 ase does not contain any iron–sulphur clusters and has been found only in some methanogenic Archaea. H2 ases are the only molecular catalysts that are capable of catalyzing both proton reduction and hydrogen oxidation with efficiencies comparable to the platinum catalyst (Jones et al., 2002). Only [NiFe]- and [FeFe]-H2 ases have been employed in the biomimetic H2 -evolving systems, as the [Fe]- (also termed Hmd) H2 ases are light sensitive, and thus, not useful in solar-tofuel biomimetic devices. [NiFe]- and [FeFe]-H2 ases are structurally different, but catalyze the same reaction employing structurally different catalytic sites (Fontecilla-Camps et al., 2009). Prokaryotic cyanobacteria usually employ [NiFe]-H2 ases, which are usually less sensitive to irreversible inactivation by O2 . [FeFe]-H2 ases are expressed in microalgae (e.g., C. reinhardtii) and anaerobic bacteria (e.g., Chlamydomonas acetobutylicum) that produce H2 during fermentation or anaerobic respiration. The [FeFe]-H2 ases are rapidly and often irreversibly inhibited by O2 , a feature that has hampered the efficient use of these enzymes in biomimetic photocatalytic nanodevices. The high-resolution X-ray structures of both types of H2 ases revealed important features of the catalytic sites (Volbeda et al., 1995, 1996; Peters et al., 1998; Nicolet et al., 1999; FontecillaCamps et al., 2007, 2009). Their active site is a bi-nuclear metal complex based either on exclusively iron, or on a combination of nickel and iron ions in a sulphur-rich environment, with Fe ions also coordinated by cyanide and carbon monoxide (Ogata et al., 2002; Fontecilla-Camps et al., 2009). Both catalytic sites usually include multiple [4Fe–4S] clusters that participate in electron transfer

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reactions between the active site and the electron acceptor or donor molecules that interact with the surface of the protein (Lubner et al., 2010a). Although [NiFe]-H2 ases are 10–100 times less biologically active in H2 production compared to [FeFe]-H2 ases, the major advantage of employing them in the solar-to-fuel biometric systems is their oxygen tolerance. Additionally, these O2 -tolerant H2 ases are very attractive candidates as the molecular catalysts of proton reduction in the solid-state biomimetic photodevices, as discussed below. In 2002, Rögner and colleagues proposed a model for a complete photo-hydrogen producing nanodevice that would include PSI, PSII and a H2 ase in a modular configuration, allowing for the combination of respective highly active proteins from various extremophilic organisms. Such a modular system would be easily exchangeable and should be separately characterized and optimized for all the components (Wenk et al., 2002). As the first step toward the complete device, the authors reported optimization of the [NiFe]-H2 ase from Thiocapsa roseopersicina. The isolated H2 ase was deposited as Langmuir–Blodgett films on quartz glass or indium–tin oxide (ITO) electrodes, and its H2 -evolving activity was measured with respect to counter ions, presence of oxygen and the number of protein layers immobilized on an electrode (Wenk et al., 2002). The authors demonstrated that poly-l-lysine and poly-butyl-viologen as counter ions on the sub-phase stabilized the H2 ase on quartz glass. The presence of Ca2+ , oxygen, excess amount or multiple layers of protein on the surface of the electrode resulted in a significant loss of H2 production. The maximal hydrogen production rate was achieved at 0.35 nmol H2 min−1 per monolayer of H2 ase (Wenk et al., 2002). The first example of a direct light-to-hydrogen conversion system using both H2 ase and PSI was reported in 2006 by the groups of Okura and Friedrich (Ihara et al., 2006). The authors designed an artificial fusion protein composed of the membrane-bound [NiFe]-H2 ase (MBH) from the soil bacterium Ralstonia eutropha and the PsaE extrinsic subunit of T. elongatus PSI. Both proteins were connected by a small amino acid linker that replaced the membrane-anchor at the C-terminus of the smallest H2 ase subunit, HoxK. After spontaneous association with the PsaE-null mutant of PSI, the resulting H2 ase-PsaE-PSI hybrid complex displayed lightdriven hydrogen production at a rate of 0.58 ␮mol H2 mg Chl−1 h−1 , in presence of ascorbic acid, dithiothreitol and tetramethyl phenylene diamine (TMPD) as the exogenous electron donors and acceptors (Ihara et al., 2006). In this fusion complex, the most distal [4Fe–4S] FB cluster of PSI was located approximately at a 14 A˚ distance to the distal accessory [4Fe–4S]-cluster of the H2 ase, allowing for an efficient direct electron transfer between both ETCs. A similar approach was used by Lenz, Rögner and colleagues, who constructed a functional highly homogeneous hybrid complex of the MBH-PsaE fusion protein and the PsaE-null mutant of Synechocystis PSI (Schwarze et al., 2010). Ihara et al. (2006) discovered that such a hybrid complex had the ability to interact with the native Fd, which acted as a competitive electron acceptor, and therefore, also an inhibitor of electron transport between PSI and the MBH H2 ase. As the authors aimed at improving in vivo H2 production rates using a hybrid complex of PSI and the MBH, they attempted to diminish the inhibitory effects of the Fd-dependent electron transfer pathway. To this end, they engineered a fusion protein of PsaE and cyt c3 from Desulfovibrio vulgaris (Ihara et al., 2006), which

(Amunts et al., 2010). Presented are the helices of several of the protein subunits, PsaA (yellow), PsaB (light turquoise), PsaC (dark blue), PsaD (light purple), PsaE (tangerine) PsaF (black), PsaG (indigo), and the cofactors (color coding as in A, B, D, F). Other subunits and cofactors have been omitted for clarity. The views of PSI are approximately with the threefold and twofold symmetry axis of the cyanoPSI and plant LHCI-PSI, respectively, in the membrane plane. The PDB coordinates are 1JB0 (cyanoPSI; Jordan et al., 2001), 3LW5 (higher plant LHCI-PSI; Amunts et al., 2010), 2FRV and 1UBO ([NiFe]-hydrogenases; Volbeda et al., 1996; Ogata et al., 2002), 1FEH ([Fe]-hydrogenase; Peters et al., 1998), 1C6S (cyt c6 ; Beissinger et al., 1998) and 9PCY (PC; Moore et al., 1991). Asc, ascorbate; DCPIP, 2,6-dichlorophenolindophenol; H2 ase, hydrogenase; MBH, membrane-bound hydrogenase; MV, methyl viologen; MA, mercaptoacetic acid; PC, plastocyanin; PMS, N-methylphenazonium methyl sulphate.

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is the natural electron donor for H2 ases in Desulfovibrio species (Matias et al., 2001). This fusion protein was employed to reconstitute the activity of PSI lacking the PsaE subunit, resulting in a hybrid complex that was able to interact with the specific H2 ase while simultaneously exhibiting a decreased affinity for Fd (Ihara et al., 2006). A promising new approach toward efficient H2 photoproduction is based on the use of [FeFe]-H2 ases with a natural affinity to Fd. Under anaerobiosis, several species of green algae such as C. reinhardtii undergo hydrogen photo-production catalyzed by a group of [FeFe]-H2 ases termed HydA. Happe and colleagues demonstrated that Fd is critical for efficient electron transport between PSI and HydA1 in Chlamydomonas by employing an elegant in vitro reconstitution system for H2 production composed of PC (as a natural electron donor to P700+ ), LHCI-PSI supercomplex, Fd (PetF protein) and a wild-type HydA1 H2 ase (Winkler et al., 2009). Kinetic analyses of several site-directed mutants of HydA1 and PetF allowed mapping of the key amino acids essential for electrostatic interactions and electron transfer between both proteins. In particular, a conserved HydA1 lysine residue Lys396 seems to play a critical role for interaction with the C-terminus of PetF, while the PetF residue Glu122 is essential for docking the N-terminus of HydA1. The maximum H2 production rate was reported at ∼90 ␮mol H2 mg Chl−1 h−1 (Winkler et al., 2009). Although this yield is still in the range of in-solution systems, it demonstrates a potential of this O2 -sensitive [FeFe]-H2 ase for the use in solar-to-hydrogen production systems. One advantage of employing the diffusion-based H2 -producing systems is the ability to vary and fine-tune the individual components without employing their specific chemical modifications for immobilization within solid devices. A rather interesting variation of the diffusion-based biomimetic system for H2 production has been reported, whereby hydrogen evolution was catalyzed by the O2 -tolerant [NiFe]-H2 ase from the phototrophic purple sulphur bacterium T. roseopersicina operating in tandem with PSI from cyanobacterium Synechocystis sp. PCC 6803. In this in vitro system, H2 evolution was sustained in the presence of mercaptoacetic acid (MA) as the sacrificial electron donor and methyl viologen (MV) as the exogenous electron acceptor (and donor to the H2 ase), as shown in Fig. 6B (Qian et al., 2008). This system evolved up to 0.5 ␮mol H2 mg Chl−1 h−1 . Despite such a low H2 evolution rate, the system confirmed feasibility of a direct in-solution electron transfer between an exogenous electron donor, PSI and a catalytic centre of the H2 ase.

A major advancement of the PSI-based H2 -producing in vitro and solid-state systems has been achieved through application of the “molecular wiring” technology developed by Golbeck, Bryant and colleagues (Grimme et al., 2008, 2009; Lubner et al., 2010a,b, 2011). This approach employs a “molecular wire” compound to connect a terminal [4Fe–4S] cluster of PSI (FB cluster) directly to a H2 producing catalyst, which can be either the distal [4Fe–4S] cluster of an [FeFe]- or [NiFe]-H2 ase (see Fig. 6D) or a noble metal nanoparticle (as depicted in Fig. 6E). The methodology involves constructing mutant variants of both PSI and a H2 ase so that a molecular wire can be attached to their surface-located iron–sulphur clusters. The most distal surface-located iron–sulphur clusters in PSI and H2 ase are each ligated by 4 cysteine residues, one of which can be altered via site-directed mutagenesis to a glycine residue. These changes expose iron atoms both in PSI and in H2 ase, allowing the –SH rescue ligands from the molecular wire (usually a thiolate derivative) to form two strong covalent disulphide bonds with the photocatalytic (PSI) and proton-reducing (H2 ase or Pt/Au nanoparticle) modules. Upon absorption of two photons by P700, the photoactivated electrons are efficiently transferred through the molecular wire from PSI to the proton-reducing catalyst, which in turn reduces two protons to molecular hydrogen. Very recently, molecular wiring of cyanobacterial PSI with the [FeFe]-H2 ase from C. acetobutylicum allowed for light-induced H2 production at a spectacular rate of 2200 ␮mol mg Chl−1 h−1 , i.e. at greater than two-fold electron throughput by this hybrid nanoconstruct compared to in vivo oxygenic photosynthesis (Lubner et al., 2011). An important improvement of this technology was covalent cross-linking of the natural electron donor, cyt c6 to the donor side of PSI to ameliorate diffusion-based limitations of electron transfer on the donor side (see Fig. 6D). In contrast to high rates of H2 production when using wired H2 ase as the proton reducing catalysts, molecular wiring of the noble metal nanoparticles to the terminal FB cluster of PSI resulted in rather modest rates of H2 production of 3.4 ␮mol H2 mg Chl−1 h−1 with a gold catalyst and 9.6 ␮mol H2 mg Chl−1 h−1 when platinum nanoparticles were used (Grimme et al., 2008). Importantly, when cyt c6 was used as a natural electron donor to the photooxidized dithol-wired PSI, the H2 evolution yield increased 5-fold to 49.3 ␮mol H2 mg Chl−1 h−1 (Grimme et al., 2008), reiterating the importance of limiting the diffusion-based donor side electron transfer to ensure higher rates of hydrogen production. PSI-based solid-state systems for H2 production

Hybrid biological/organic photochemical systems for H2 production The approach of selective covalent modification of PSI and its natural or synthetic electron donors and acceptors overcomes the limitations of diffusion-based electron transfer processes. Evans et al. (2004) reported covalent linking of PC to platinized PSI by employing a cross-linking reagent 1-ethyl-2-(3dimethylaminopropyl) carbodiimide hydrochloride, as depicted in Fig. 6C. Compared to the diffusion-based setup, covalent linking of PC and the donor side of PSI resulted in a 3-fold increased rate of H2 evolution at an initial rate of 0.09 ␮mol H2 mg Chl−1 −1 (Evans et al., 2004), demonstrating the importance of limiting diffusionbased electron transfer on the donor side for maximization of the H2 production. The relatively low H2 production rate is most likely due to the fact that diffusion limitation still applies to the reduction of PC by Asc (sacrificial electron donor). Another possibility is that at least a fraction of the spinach LHCI-PSI supercomplex used in the study is likely to undergo photoinhibition or a fraction of Pt-PSI conjugates may precipitate under experimental conditions applied in the study, possibly leading to a significant loss of H2 production.

The hybrid systems described above have paved the way for the development of immobilized PSI-bioconjugates within the solidstate systems for H2 production. The field is new, and so far a rather limited number of efforts have employed such an attractive stateof-the art technology. To date, most in solido efforts have focused on the application of photosynthetic complexes as photodetectors or photovoltaic cells. For instance, Das et al. (2004) reported the integration of spinach PSI and purple bacterial RC from Rhodobacter sphaeroides in solid state devices, creating photodetectors and photovoltaic cells with internal quantum efficiencies of approximately 12%, an efficiency highly desirable for the purposes of H2 photo-evolution. They achieved a proper electronic integration of the device by self-assembling an oriented monolayer of each photosynthetic RC. These were in turn stabilized with surfactant peptides and coated with a protective organic semiconductor to ensure efficient electron flow between each half-cell. Recently, several groups reported application of cyanobacterial PSI as a photocathode that was molecular-wired to the protonreduction centre within the half-cell cathodic solid devices. Miyachi et al. (2009) reported a novel molecular wire derived from vitamin

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K1 (VK1 ) with a napthoquinone moiety that can connect to the FB cluster of the T. elongatus PSI and a terpyridine moiety for connection to the Co (II) proton-reducing catalyst. A self-assembled monolayer of PSI and the VK1 molecular wire was immobilized on an indium tin oxide (ITO) electrode. This bioconjugate complex showed the photocurrent action spectrum with a profile consistent to that of PSI, reflecting its suitability for H2 -production, although H2 production itself was not investigated in this study (Miyachi et al., 2009). Similarly, Terasaki et al. (2009) describe a novel molecular ‘connector’ system, whereby an artificial wire (a napthoquinone-viologen derivative NQC15 EV) assembled on a gold electrode is plugged into one of the PSI redox active cofactors, the A1 phylloquinone. The authors successfully obtained the desired output of electrons from photo-activated PSI and demonstrated the effectiveness of the molecular wiring technology for efficient coupling of PSI with the electrode by photoelectric transfer kinetics analysis of the wire molecule (Terasaki et al., 2009). Recently, Heberle and colleagues generated a H2 -evolving photoelectrode by immobilizing the PSI-[NiFe]-H2 ase hybrid complex on the surface of a Ni-NTA-functionalized gold electrode, and orienting the donor side of PSI (through the His-tagged PsaF subunit) at a close distance to the electrode (Krassen et al., 2009), as shown in Fig. 6F. In this study, the full functionality of the PsaE-null mutant of PSI from Synechocystis sp. PCC 6803 was rescued by binding a fusion of the PsaE subunit and the membrane-bound/oxygen tolerant [NiFe]-H2 ase (MBH) from R. eutropha, a similar fusion complex to that reported by Ihara et al. (2006). The estimated distance between the FB cluster of PSI and the distal Fe-S cluster of the ˚ indicating tight electronic coupling between MBH was 14–25 A, both ETCs in the engineered PSI-H2 ase hybrid complex. As a result, more than 5000-fold enhanced light dependent H2 production rate of 3000 ␮mol H2 mg Chl−1 h−1 was achieved. Unfortunately, the assembly appears to be unstable, as half-life of the photocurrent was only 30 min. In addition, in order to maintain the reduced state of the exogenous electron donor N-methylphenazonium methyl sulphate (PMS), overpotential of −90 mV had to be applied. Nonetheless, the system reflects the quintessential advantage of solid state tightly coupled assemblies over diffusion-based systems. Moreover, Krassen and colleagues clearly demonstrated that electron supply on the PSI donor side appears to be the major bottleneck for this type of H2 -producing solid-state assemblies.

Future outlook The two X-ray structures of cyanobacterial PSI and higher plant LHCI-PSI supercomplex have revolutionized biophysical and biochemical studies on this molecular complex aimed at dissecting the precise sequence of molecular events from light capture by the antenna pigments through excitation of the P700 dimer, charge separation and charge migration to the acceptor side of this complex. In particular, kinetic studies of electron transfer within PSI and the discovery of two active branches of electron transfer in PSI RCs have been aided tremendously by the detailed knowledge of the exact ligand environment of the ETCs of PSI obtained through Xray crystallography combined with site-directed mutagenesis. Both crystal structures have proven invaluable for probing interaction with other components of the photosynthetic machinery during adaptation responses to varying light conditions and stress factors. Nevertheless, a number of challenges remain to be addressed, including dissecting the molecular regulatory pathways of CET around PSI and its functional importance in higher plants, the exact modes of interaction between PSI and the mobile LHCII antenna during short-term adaptation of state transitions, and identification of the putative CET megasupercomplex in higher plants. The biggest challenge of all is to obtain X-ray structures of extremely

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labile supercomplexes of PSI together with the other components of photosynthetic machinery, such as the mobile LHCII antenna, Fd, FNR and PC/cyt c6 . There is no doubt that the inherent light-harvesting and electron-transfer properties of natural PSI make this macromolecular complex particularly attractive for application in the solar-to-fuel biomimetic devices reviewed in this article. The longlived charge-separated state P700+ FB − and an exceptionally low redox potential associated with the distal FB cluster generate sufficient reducing power for production of molecular hydrogen in man-made devices at neutral pH. While the H2 production yields of the early semi-artificial systems could not compete with contemporary commercial hydrogen generation techniques, tremendous progress in revealing the structure and function of PSI and H2 ases, and a growing demand for a sustainable H2 source have led to a recent revival of this research field. Nevertheless, this field is still at the stage of experimental laboratory work and lacks any in-depth knowledge regarding costs and large scale applications. Bruce and colleagues argued that their self-assembling in vitro Pt-PSI-cyt c6 solar collector system could produce hydrogen with an energy yield equivalent to that of 300 liters of gasoline per hectare per day. This predicted yield would be more than one order of magnitude higher than the gross yield of gasoline equivalents produced by contemporary agricultural biomass systems (Iwuchukwu et al., 2010). The authors postulate that this system is capable of converting approximately 6% of solar radiation into usable fuel, the efficiency much higher than that of the natural photosynthesis. At present, it is difficult to predict with certainty the success of commercial-scale application of biomimetic solar-to-fuel PSI-based devices. Nevertheless, some general aspects that affect system efficiencies should be considered while engineering such large-scale biomimetic devices. While systems based on noble metal additives and those based on H2 ases exhibit comparable efficiencies, the major disadvantage is the high cost of noble metal catalysts, as well as oxygen sensitivity of the most active H2 ases. Understanding the precise kinetics of electron transfer within photosensitizer (PSI) module and a hydrogen-evolving catalyst (H2 ase or synthetic proton reduction catalyst) and their inter-molecular interactions is a prerequisite for the design of biomimetic hydrogen producing systems which have the potential to be economically promising. Very recently, the significant interest in utilizing the highly stable natural PSI for generation of hydrogen as a clean solar fuel has resulted in engineering vastly improved biomimetic devices with some of the highest light-driven turnover yields of H2 ever observed. The pioneering work by Golbeck, Bryant and colleagues on development of the molecular wiring technology, reviewed in this article, emphasizes the importance of minimizing energy losses due to diffusion-based electron transfer within solarto-fuel devices. Similarly, tight electronic coupling between the terminal FB cluster of PSI and the distal Fe–S cluster of the oxygentolerant H2 ase in a solid-state system, such as the system developed by Heberle, Lenz and colleagues (Krassen et al., 2009), represents an attractive approach for improved solar-to-fuel devices. Thus, the critical issue of amelioration of losses due to the donor and acceptor side rate limitation around PSI has been successfully addressed in small-scale solid-state and in vitro systems. We firmly believe that the next few years will bring considerable technological advances that will lead to construction of the complete highly stable and electronically coupled solid-state H2 -evolving biomimetic device utilizing PSI as a photocathodic module which, in conjunction with the biological or synthetic proton reducing centre, will use electrons and protons produced through photooxidation of water in the anodic half-cell for production of molecular hydrogen at a high yield. In this way, electron diffusion obstacles and artificial donor/acceptor availability will be overcome. Undoubtedly, the biggest challenge of all will be to

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