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Three-dimensional structure of
cyanobacterial photosystem I
at 2.5 AÊ resolution
Patrick Jordan*, Petra Fromme², Horst Tobias Witt², Olaf Klukas*, Wolfram Saenger* & Norbert Krauû*³
* Institut fuÈr Chemie/Kristallographie, Freie UniversitaÈt Berlin, D-14195 Berlin, Takustraûe 6, Germany
² Max Volmer Laboratorium fuÈr Biophysikalische Chemie, Institut fuÈr Chemie, FakultaÈt 2; Technische UniversitaÈt Berlin, D-10623 Berlin, Straûe des 17. Juni 135,

Life on Earth depends on photosynthesis, the conversion of light energy from the Sun to chemical energy. In plants, green algae and
cyanobacteria, this process is driven by the cooperation of two large protein±cofactor complexes, photosystems I and II, which are
located in the thylakoid photosynthetic membranes. The crystal structure of photosystem I from the thermophilic cyanobacterium
Synechococcus elongatus described here provides a picture at atomic detail of 12 protein subunits and 127 cofactors comprising
96 chlorophylls, 2 phylloquinones, 3 Fe4S4 clusters, 22 carotenoids, 4 lipids, a putative Ca2+ ion and 201 water molecules. The
structural information on the proteins and cofactors and their interactions provides a basis for understanding how the high
ef®ciency of photosystem I in light capturing and electron transfer is achieved.

All higher organisms on earth receive their energy directly or provided by PSII by way of a pool of plastoquinones and the
indirectly from oxygenic photosynthesis performed by plants, cytochrome b6/f complex.
green algae and cyanobacteria, the last two representing an impor- To understand the role of the protein subunits in binding of the
tant part of the marine food web. Photosynthesis converts solar cofactors, and the interactions between the cofactors, we have
energy to chemical energy by means of two large protein complexes determined the X-ray crystal structure of PSI from the thermophilic
located in the thylakoid membranes: photosystems I (PSI) and II cyanobacterium S. elongatus and describe here the atomic model.
(PSII). They use the energy of absorbed photons to translocate
electrons across the membrane along a chain of cofactors, leading to Structure determination
a transmembrane difference in the electrical potential and in H+ The trimeric PSI, isolated from S. elongatus, was crystallized as
concentration, which drives ATP synthesis and reduction of NADP+ described elsewhere8. Detailed information on X-ray data collec-
to NADPH. In the subsequent dark reactions, NADPH and ATP are tion, evaluation and re®nement at 2.5 AÊ resolution are provided in
used to convert CO2 to carbohydrates. Table 1 and as Supplementary Information.
PSI and PSII belong to the superfamily of photosynthetic reaction In the electron density map, the 11 biochemically characterized
centres, which are divided into two classes according to their and sequenced protein subunits9 were identi®ed. Ten of these were
terminal electron acceptors: Fe4S4 clusters (type I) or quinone (type interpreted with the known amino-acid sequences, whereas the
II; for review see ref. 1). For purple bacterial reaction centres and PSII, peripheral subunit PsaK could only be modelled as polyalanine,
both belonging to the type II reaction centres, three-dimensional because the electron density becomes less well de®ned with increas-
structures are known at high and medium resolution, respectively2,3. ing distance from the centre of the PSI trimer. A twelfth polypeptide
For type I reaction centres, a structural model of cyanobacterial PSI chain containing one transmembrane a-helix could be ®tted to well
at medium resolution (4 AÊ) is available4,5 but elucidation of the de®ned electron density. Its sequence is homologous to the con-
mechanism of light capture and electron transfer in PSI has been troversial subunit PsaX identi®ed in PSI from the thermophilic
impeded by lack of more detailed structural information. cyanobacteria Synechococcus vulcanus and Anabaena variabilis10,11.
Isolated cyanobacterial PSI exists as a trimer6 (relative molecular For the 96 chlorophylls, the positions and orientations of the
mass Mr 3 ´ 356,000); this form is also present in vivo. One chlorophyll head groups were determined, leading to the assign-
monomer consists of at least 11 different protein subunits coordi- ment of the orientation of the QX and QY transition dipolar
nating more than 100 cofactors. PSI captures light energy by a large moments. For 48 of them the ring substituents, including the
internal antenna system and guides it to the core of the reaction complete phytyl side chains, could be modelled into the electron
centre with high ef®ciency. After primary charge separation density map, whereas for the remaining Chla molecules the phytyl
initiated by excitation of the chlorophyll dimer P700, the electron chain could be modelled only partially. In addition, the three Fe4S4
passes along the electron transfer chain (ETC) consisting of the clusters, two phylloquinones and for the ®rst time 22 carotenoids
spectroscopically identi®ed cofactors A0 (Chla), A1 (phylloquinone) (16 in all-trans, 5 in different cis con®gurations and one modelled
and the Fe4S4 clusters FX, FA and FB (for review see ref. 7). At the as an incomplete b-carotene molecule), 4 lipids and a putative
stromal (cytoplasmic) side, the electron is donated by FB to Ca2+ ion were identi®ed. The total of 127 cofactors located in one
ferredoxin (or ¯avodoxin) and thence transferred to NADP+ PSI monomer contributes around 30% of the molecular mass of
reductase. The reaction cycle is completed by re-reduction of PSI.
P700+ by cytochrome c6 (or plastocyanin) at the inner (lumenal)

side of the membrane. The electron carried by cytochrome c6 is Overall architecture
Trimeric PSI resembles a clover leaf (Fig. 1a). Its threefold rotation
³ Present address: Institut fuÈr Biochemie, UniversitaÈtsklinikum ChariteÂ, Medizinische FakultaÈt der axis coincides with the crystallographic C3 axis (space group P63),
Humboldt UniversitaÈt zu Berlin, Monbijoustrabe 2, D-10117 Berlin, Germany. which is perpendicular to the membrane plane (Fig. 1b). At the

NATURE | VOL 411 | 21 JUNE 2001 | © 2001 Macmillan Magazines Ltd 909

stromal subunits have been omitted. regions are shown in ribbon representation. View as in a showing stromal subunits PsaC. The organic cofactors of the ETC are arranged in two branches contacts between the monomers. PSI contains nine protein subunits featuring transmembrane a. a-helices and b-sheets are numbered in alphabetical order from the N to the C terminus. a. PsaL. the carotenoids and the lipids are bound to PsaA/B. In addition to the transmembrane a-helices of the stromal and lumenal loop site of ferredoxin. Subunits are labelled. ETC: quinones and chlorophylls in blue. arrangement Fe4S4 clusters as orange and yellow spheres. carotenoids in black. PsaD and PsaE). The large (Mr and contribute to the coordination of antenna cofactors (Fig. PsaB. PsaE (green) and the Fe4S4 clusters. 1a). All loop regions of PsaA and PsaB are named (pink). II and III). View direction indicated by according to the transmembrane helices which they connect. II. The transmembrane in yellow. PsaM and PsaX) membrane-instrinsic subunits are peripheral to the PsaA/PsaB core and three stromal subunits (PsaC. They cover some of the Six helices in extra-membranous loop regions are drawn as spirals. PsaL forms most of the axis. PsaF. along the pseudo-C2 axis. View along the membrane transmembrane a-helices (the side chains of the antenna Chla molecules have been normal from the stromal side. PsaI. PsaK.articles `trimerization domain' close to the C3 axis. iron and sulphur atoms of the three structural elements are shown in each of the three monomers (I. Side view of the arrangement of all a-helices of PsaA (blue) and PsaB (red) are named A-a to A-k (B-a to B-k) from the N to the proteins in one monomer of PSI (colours as in a). membrane-intrinsic loop regions and helices of PsaA and PsaB (light grey). b. The vertical line (right) shows the crystallographic C3 axis.nature. III. The other helices (PsaA. including the stromal subunits PsaC C terminus (capital letters omitted). For all other subunits the arrow at monomer II in a. and most of the antenna Chla molecules. respectively. PsaD and PsaE. . covering loops of PsaA. lipids in turquoise. PsaJ.5 AÊ resolution. 83K) subunits PsaA and PsaB are related by a pseudo-C2 axis located The structure of PSI suggests a docking site for cytochrome c6 or at the centre of the PSI monomer and oriented parallel to the C3 plastocyanin (donating electrons to PSI) at the lumenal side close to a PsaK III PsaA d c b A-ij(2) B-jk(1) e a f PsaJ h F-h g k i j F-c PsaF F-f I PsaL j F-i k i g PsaI h F-d f PsaM e PsaX A-jk(1) a b c B-ij(2) d PsaB II PsaC b c PsaC N PsaE PsaD C C N PsaE PsaD C N Ferredoxin/ flavodoxin Figure 1 Structural model of PS I trimer at 2. complete set of cofactors shown with the 910 © 2001 Macmillan Magazines Ltd NATURE | VOL 411 | 21 JUNE 2001 | www. I. Dashed ellipse: putative docking subunits. Antenna system: chlorophylls of the transmembrane a-helices (cylinders). Different omitted). PsaD (turquoise). For clarity.

... It exhibits divided into an amino-terminal domain (six a-helices: A/B-a to pseudo-twofold symmetry similar to bacterial 2Fe4S4 ferredoxins17.........404 Rwork/Rfree (%) 19..9) 90...........................7 Cofactors 6.........8 (95.. insertion extrudes as a large loop.602 R...0 50±3.................m............. The binding pocket for the binding interface to subunits PsaC....079 (0......064 (0..224) 0............0 Rmerge* 0...57 Re®nement statistics Re¯ections (working set) 233....065 (0.. ³ From Luzzati plot and SigmaA analyses... are close together and arranged as a crescent...... By contrast....... A/B-f) and a carboxy-terminal domain (®ve a-helices: A/B-g to but contains an insertion of 10 amino acids in the loop connecting A/B-k). b).. they QK-A may be engaged in interaction with and/or electron transfer from 8...3 (68...........3) hI/i 10.....0 30±3....s.....51 1. coordinates Mg2+..... As the shortest distance between their membrane plane..8 8. direct interaction with B...0126 Water 201 R......... consistent with the respectively....nature.... 2) interacts with PsaA/B/D and appears to be important for the harbouring a large number of the antenna Chla molecules and proper assembly of PsaC into the PSI complex... 1a..... In PsaC.... PsaD and PsaE (Fig......4) 10...... The `¯at but rugged' lumenal surface of PSI is mainly formed by loop regions connecting transmembrane a-helices of subunits PsaA and PsaB....... The base of the 14.. of heavy atom sites ± ± 4 8 Rcullis (centric)² 0..............475 Metal 1 Coordinate error (AÊ)³ Luzzati 0..... The latter form two interlocked the iron-sulphur cluster binding motifs and extensions of the N and semicircles enclosing the ETC cofactors..44 0........ FA and FB according of electron transfer in cyanobacteria14.. Rcullis (centric) and phasing power determined by the program SHARP (see Supplementary Information).. 1c)...... * Rmerge ˆ Sh Si jIi …h† 2 hI…h†ij=Sh Si Ii …h†....1 (4..5 (8....62/1.................2 eC-B2 eC-A2 cyanobacterial PSI where substitution of some of the amino acids of 11.207) 0..........3 shield the cofactors from the aqueous phase... The pairs of chlorophylls of the ETC are arranged in two branches A and helix axes and the pseudo-C2 axis is 27 AÊ.........86 0......32 SigmaA 0.. respectively (Fig... an insertion and extensions at C and N termini are green. The long C terminus of PsaC (green in distorted cylindrical region bridged by a-helices A/B-e and f and Fig...... and by numbers 1 to 3 starting from the lumenal side.. phasing and re®nement statistics Data set Native (1) Native (2) EMTS PIP Wavelength (AÊ) 0......... forming several short a-helices and b-sheets...254) Completeness (%) 97.......... PsaC in the middle and PsaE farthest out (Fig.............6 eC-A3 eC-B3 cytochrome c6 or plastocyanin to the oxidized primary electron donor P700+ ... Their indole groups are stacked at van der Waals distance and related by the 14..s.............. ref. As they point into the putative binding site.03 1......... View parallel to the brane helix F-f (Fig. Figure 2 Cofactors of the electron transfer chain (ETC) and of PsaC. eC-A1 eC-B1 Besides the lumenal loops of PsaA/B......377 Number of non hydrogen atoms Re¯ections (test set) 4..... an insertion and to their spectroscopic terms.......9) 21......9 50±3..99 1.. These subunits latter is formed by subunits PsaC.16.4 (76. bond lengths (AÊ) 0.........d..........1 (88.............1 QK-B pseudo-C2 axis..... the pseudo-C2 axis and for ferredoxin or ¯avodoxin (accepting The loops at the stromal surface of PsaA/B partly constitute the electrons from PSI) at the stromal side........... Polypeptide subunits They surround an indentation on PsaA that was proposed as the Subunits PsaA and PsaB share similarities in protein sequence and binding site for ferredoxin12.... it may be engaged in docking of brane a-helices of the smaller PSI subunits by an elliptically ferredoxin or ¯avodoxin......2 14.. 2)... followed by the letter A or B indicating whether PsaA or PsaB.............. for nomenclature see © 2001 Macmillan Magazines Ltd 911 ..... This view is supported by mutagenesis studies on X 8...... The centre-to-centre distances between the cofactors (black an extension in the N-terminal domain in PsaF of higher plants (see lines) are given in AÊ...23/1........ ² FOM (®gure of merit)........... where Ii(h) are individual intensities of any re¯ection and hI(h)i is the mean intensity. c)............. subunit PsaF contributes prominent structural features to this surface of PSI with two hydrophilic a-helices F-c and F-d at the N terminus of transmem.99 0..99 Resolution (AÊ) 30±2.......... breaking the pseudo-C2 FB FB symmetry........ NATURE | VOL 411 | 21 JUNE 2001 | www........................... as determined with CNS (see Supplementary Information)............ observation that deletion of PsaF does not in¯uence the kinetics Phylloquinones are QK-A and QK-B..........0 A/B-ij(2) including Trp affects electron transfer to P70013........3) 98.......6) 20.......81 Phasing power (iso/ano)² -/0..... 15 and references therein) are involved in plastocyanin docking........2) . carotenoids (see Fig.7 12. parts analogous to 2[Fe4S4] bacterial ferredoxins17 are pink.........0 electron carriers cytochrome c6 or plastocyanin12..... The loops..6 8..... with PsaD closest to the C3 axis. The amino-acid sequences of the loops contain segments not conserved between PsaA and PsaB..076 (0................247) 0.. 12.. 1...m......743 Protein 17.........6 (3......5 30±3...0 FOM³ 0...5 30±2...9 hollow is formed by a-helices A/B-ij(2) of loops A/B-ij in which two FX FX conserved Trp residues A655 and B631 are located.6) 93...... 1b............ 1a and `The core antenna system' section)... This core structure is C termini by 2 and 14 amino acids.36 .........8/21.....0 30±3.. Phasing statistics No.... structure........ articles Table 1 Data collection.07 Resolution (AÊ) 30±2..... Numbers in parentheses correspond to values in the highest resolution shell........... A hollow close to the FA pseudo-C2 axis has been suggested to be the binding site for the 22...... They contain 11 transmembrane helices each that are PsaC harbours the two Fe4S4 clusters FA and FB.. cytochrome c6 or plastocyanin is unlikely..... bond angles (8) 1.8 (4.d.... PsaD and PsaE.... The Fe4S4 clusters are labelled FX. As the separated from the N-terminal a-helices A/Ba-d and the transmem......... They are labelled eC...........

................................... is remarkable...18...... Subunits PsaF.................................. the C terminus of PsaL is six amino........ It might be a Ca2+ as found in Mg2+ ions are coordinated by water molecules hydrogen-bonded to trimeric but not in monomeric PSI from Synechocystis PCC6803 side chains of Asn A604 and Asn B591............................................ PsaJ.................................. The electron transfer chain The Chla molecules are coordinated to sulphur atoms of Met A688 This functionally most important part of PSI is formed by six and Met B668 (distance Mg2+ ±S = 2. One or both of the Chla molecules of the third pair of chlor- ophylls eC-A3/eC-B3 probably represents the electron acceptor A0........................................ and seems to oriented perpendicular to the membrane plane........ 23................................19............... Whereas the side chains of transmembrane molecules (Table 2).... According be localized to a larger extent on the non-hydrogen-bonded Chla to the electron density map.......................nature...................... bacteriochlorophylls in PbRC. The long loop connect.. This chlorophylls..... as suggested by the overlap partially with the Mg2+ ions separated by 6...... and the B branch coordination could contribute to the unusually low redox potential features chlorophylls eC-B1. are not engaged in any hydrogen bonds. PsaM and PsaX coordinate Chla9 molecules22...... The cofactors forming one branch hydrogen bonds are donated by the hydroxyl groups of tyrosines are not bound exclusively to one subunit of PSI.... b)....................................... 7). loop connecting the third and fourth strands contains an a-helix..... eC-B2..................... showing that <80% of the the complementary DNA sequence if a frame shift is accounted for............. PsaJ......... 4a)................ * Numbers in parentheses correspond to suspect ligands.. (eC-B1).7 AÊ) to the keto oxygens of rings V of 912 © 2001 Macmillan Magazines Ltd NATURE | VOL 411 | 21 JUNE 2001 | www................... no hydrogen bonds are found to Chla eC- In the trimerization domain..... a-helices loops a b e f N-ter³ ab g h k fg jk . PsaI................. probably because it interacts with heterodimer......................... supported by PsaI.......... two phylloquinones and three Fe4S4 clusters (Fig... Chla9 eC-A1 (Fig......... Sectioning of antenna Chla coordinated by PsA/PsaB into peripheral and central antenna domains² N-terminal sequence region C-terminal sequence region transm.. The chlorin planes of from His D95 to the C terminus is attached by numerous hydrogen these chlorophylls are parallel at 3......................................................6 AÊ)........ The structure of P700 differs from the `special pair' formed by The structure of PsaE consists of a ®ve-stranded antiparallel b............ Rings I and II help in the positioning of these subunits. the crossovers being A696 and B676 (dO-O = 2..................................................................... P700 is a different from that in solution..................... a-helices Loops transm................ in which the eC-B2 and eC-A2.......... Charge separation is initiated at the primary electron donor P700 followed by a two-stranded b-sheet............................................... ing b-strands c and d seen here........................................ personal communication).......... eC-A1/eC-B2..................................... This is consistent with chlorophyll transmembrane a-helices bind and stabilize the cofactors of the extraction experiments suggesting that P700 contains one or two core antenna system..................... PsaD forms an antiparallel...................... as interactions between the hard acid Mg2+ and the The chlorophylls and phylloquinones are arranged in two branches soft base S should be weak according to the concept of hard and soft A and B as pairs of molecules related by the pseudo-C2 axis and acids and bases............... Chitinis........articles Table 2 Coordination of the antenna Chla Central ligands of the antenna Chla His Asn Gln Asp Glu Tyr Backbone Phospho-diester Water Unknown ligand Total ............................................. (approximately -105 mV) of electron acceptor A0 (ref...3 AÊ (Fig................................ In analogy to ... eC-A2....... (P........ PsaL contributes to most contacts B1............ 3a... the C132 epimer of Chla (Mg2+ Together with PsaA and PsaB...... ³ Loops N-terminal of transmembrane a-helices A/B-a...... The A branch features chlorophylls unique in proteins.. 4a)....... the small subunits featuring coordinated to His A680)..............6 AÊ interplanar distance and bonds to the stromally exposed sides of PsaC and E... eC-A3 and phylloquinone QK-A........... 3a)....................... interface between adjacent monomers and surrounded by Asp side The chlorophylls of the second pair of Chla molecules next to chains of PsaL and PsaA may belong to a metal ion that could be P700.. Short B (for nomenclature see Fig....... Their important for trimer formation...... in agreement with mutagenesis24 and electron nuclear acid residues longer than the published sequence9 but agrees with double resonance (ENDOR) studies25....... ² Secondary structural elements are labelled according ot the scheme presented in legend to Fig... eC-B3 and phylloquinone QK. eC-A1 being chlorophyll a9 (Chla9)... 1....... central domain PsaA 3 1 1 3 2 2 3 3 1 1 2 PsaB 3 ± 1 3 1 3 3 3 1 1 2 b c d e cd de gh peripheral domain PsaA 1 4 3 2 1 5 ± ± ± 2 ± PsaB 1 4 3 2 ± 5 ± ± ± 3 ± ........................ PsaL....................... is in a conformation In contrast to the homodimeric special pair in PbRC........ PsaL........ PsaM and to a a-helices A-i and A-k and a water molecule form hydrogen bonds to lesser extent PsaK are in hydrophobic contact with the carotenoids........... where the Mg2+ separation is larger barrel similar to that found in NMR studies on PsaE from (7.. however.. The loop segment reaching formed by the chlorophyll pair eC-A1/eC-B1. spin density in P700+ is probably located on the chlorophyll bound X A high spherical electron density (at 5j (FO-FC)) located at the to PsaB........................ It remains to be elucidated whether the Mg2+¼S eC-A1........... respectively (Fig....... respectively (Fig.. the electron spin density in P700+ should X between monomers...... importance of PsaD for electron transfer from FX to FA/FB................................................................6 AÊ)20 than in P700 and p±p interaction can be assumed to be Synechococcus PCC7002 and Nostoc sp......................... All subunits 65 3 1 2 1 1 15 1 90 PsaA 32 2 1 5 40 PsaB 29 1 1 1 7 39 PsaJ 1 1 1 3 PsaK (1)* 1 2 PsaL 1 1 1 3 PsaM (1)* 1 PsaX 1 1 PG 1 1 .......... 2)......................... 2).............. To our knowledge.. The asymmetry extends to the binding pockets the Mg2+ ions of antenna Chla molecules directly or through water for the two chlorophylls.. PsaB and PsaA........... stronger because of the perfect overlap of rings I21............ eC-B1 being Chla (Mg2+ coordinated to His B660) and PsaC and the stromal sides of PsaA and PsaB....................................... PsaK.... this coordination of Mg2+ is coordinated to PsaA and PsaB.......... four-stranded b-sheet...................

respectively. e.3. d. As the latter value agrees better with the distance of Trp B677 on the stromal surface a-helices A/B-jk(1). b. Other possible explanations might relate to minor structural His A680 B-i differences not detectable at the present resolution. whereas that of the quinone QA in PbRC and in bonding to the second and third Chla pairs of the ETC are strictly PSII is around -130 mV. Tyr A735 The pseudo-C2 axis passes right through the [4Fe4S] cube of FX (ref. conserved between PsaA and PsaB from cyanobacteria to higher A controversial issue in PSI is whether one or both branches of the plants.and eC-B1+ /QK-A. (Figs 1 and 5). but the small subunits PsaJ. As in a but view along the pseudo-C2 axis.2.4 AÊ).6 Å Tyr B727 redox potential of around -0. are also shown. this phylloquinone might be QK-A. b. methoxyO-134 = 3. Seventy-nine of the antenna Chla molecules are Thr A743Og ¼ eC-A1O-131 = 3. Their quinone planes are with centre-to-centre distances of 24. p-stacked at 3. water ¼ eC-A1 bound to PsaA and PsaB (Table 2) © 2001 Macmillan Magazines Ltd 913 .3 Å to FA and FB is now clear. The corresponding amino-acid side chains in PsaB the 43 innermost Chla molecules of the antenna ®ll the volume (pink) cannot form hydrogen bonds to eC-B1. 4c. Mutation of His A680 His B660 Trp A697 in the QK-A binding site decreases the slower rate. PsaX and lipid (III). QK-B and FX. Leu B590 indicating that the A branch is the slower one31. which collects light energy through separate transmembrane a-helices (grey). respectively. a. The arrangement of the clusters with FA being closer to FX than FB suggests a sequence FX!FA!FB in electron transfer. Tyr A735Oh ¼ eC-A1 O-173 = 2.8. as the cysteine residues of PsaC B-k Ser A607 coordinating FA and FB are known from mutational studies37 and A-i Phe B719 are well de®ned in the structure.3 Å conserved loop segments A/B-hi containing two cysteines each Leu B590 (Fig. The different transfer rates may be B-i caused by the most obvious elements of asymmetry in the vicinity of eC-A1 eC-B1 the two binding pockets: Trp B673 (not conserved in PsaA) located A-i A-k A-j Rings II B-j B-k between QK-B and FX. Only the by mutagenesis studies30. PsaK.3 ´ 1010 s-1 for the corresponding Ser A607 c electron transfer steps in both branches. 25. Tyr A603 g the edge-to-edge distances (which according to the Moser±Dutton Gly A739 approximation33 determine the optimal electron transfer rates) are Rings I identical (R = 6. in agreement with spectroscopic data (ref.suggest an asymmetry of X X X edge-to-edge distances between adjacent chlorophylls of the ETC electron transfer along the ETC in PSI.4 ´ 106 s-1 for the a Tyr A735 Phe B719 electron transfer steps from each phylloquinone to FX.3 AÊ and 26.3 AÊ. FX is coordinated to both PsaA and PsaB in strictly 2. with surrounding In contrast to PbRC.nature.32 of 35 ´ 106 s-1 and 4.3 AÊ between P700+ and A1.0. 28).5 AÊ with indole rings of conserved Trp A697 and respectively. yielding X One or both of the phylloquinones QK-A and QK-B might two possible radical pairs: eC-B1+ /QK-B. Except for aC-A40 and aC-B39. as also suggested nance (EPR) data26 and quinone reconstitution studies27. suggesting that these protein±chlorophyll interactions are ETC are active (for review see refs 7. 5). PsaL. X X X X correspond to the electron acceptor A1. As the P700+ and the radical pair P700+ /A1. and would f e d Gly B594 correspond to optimal rates33 of 8. As the chlorin planes of eC-B2 and carbonyl oxygen atom in ortho position to the phytyl chain accepts eC-A2 are roughly parallel with and only . scopy at 80 K29. c.0 6 0. orders of magnitude faster b Tyr B727 than the values for the experimental rate but in agreement with an Thr A743 a estimation of 9 ´ 1010 s-1 derived from the temperature dependence of the slower experimental rate34. water ¼ Gly A739O = 3. These residues coordinate to Mg2+ of 11 Chla molecules either directly or indirectly are strictly conserved between subunits PsaA of many organisms. Rings I and II membrane-intrinsic light-harvesting complexes.32. also f. PSI features a core overlap partially. which is a rare example of an inter-polypeptide iron A-k Gly B594 sulphur cluster.7 mV (ref. a water (red sphere) antenna system formed by 90 Chla molecules and 22 carotenoids and amino acids of PsaA (turquoise) as dashed lines with distances (AÊ) lettered: a.3. hydrogen bonds from backbone NH of Leu A722 (QK-A) and A3 and eC-B3. but none of them is through water molecules (Table 2).7. The assignment of the two Fe4S4 clusters in PsaC 2.4 6 0.4 6 0. the negatively charged phospholipid (I) at 15 AÊ from QK-A. PsaM. respectively. g. they may be directly engaged in electron Leu B706 (QK-B) (Fig. the low redox potential (approximately -820 mV) of the phyllo- All the amino acids involved in Mg2+ coordination and hydrogen quinone in PSI. respectively.8 AÊ from those of eC.9. articles eC-A3 and eC-B3. P700 is the only site where a are very short (. as proposed from the amino-acid sequences35. Thr A743Og ¼ water = 2. His A680 and His B660 coordinating eC-A1 provided by the elliptically distorted cylindrical region centred on and eC-B1. View perpendicular to the chlorin planes.7.0±3.8 AÊ) between QK-A/QK-B and FX. transfer. Ser A607Og ¼ water = 2. Surprisingly. eC-A1 The core antenna system Figure 3 Local environment of P700. The spin-carrying half of P700+ is probably Chla eC-B1. Tyr A603Oh ¼ water = 2. electron transfer in PSI involves both branches of the ETC with different rate constants31. 38 His B660 B-j and refs therein). According to kinetic investigations.determined by EPR spectro- X X This agrees with modelling based on electron paramagnetic reso. we expect that each participates in electron signi®cant structural difference between the two branches is obvious. A possible Thr A743 geometrical distortion of FX associated with the unusually low 3. conserved between PsaA and PsaB. All possible hydrogen bonds between eC-A1. It remains to be seen whether the transfer from P700 to A0 and possibly affect the spectroscopic and lack of a hydrogen bond to the para-carbonyl oxygen contributes to redox properties of the third Chla pair. the pseudo-C2 axis and are separated from the chlorophylls of the NATURE | VOL 411 | 21 JUNE 2001 | www. Spectroscopic data on essential for ®ne-tuning the redox potentials of the cofactors. contrasting to the uncharged galactolipid (II) at eC-B1 the same distance from QK-B and differences in the number and b A-j arrangement of water molecules located between QK-A. eC-A1 (Chla') and eC-B1(Chla). a phosphatidylglycerol. d). 36) is not obvious at the Tyr A603 present resolution. 4b).

P700 (ref. View of the quinone binding of PsaA (turquoise) and B-hi of PsaB (pink) surround the inter-polypeptide iron sulphur site normal to the quinone plane. elongatus PSI. B574.3 AÊ. a range supporting fast for strongly excitonically coupled Chla molecules are one trimer excitation energy transfer of the FoÈrster type39. Glu and Tyr side stacked like a staircase ( .nature.7 AÊ and lateral centre-to-centre shifts of 8. aC-B31.9 AÊ between aC-B39 of the chlorins are roughly parallel. Two of the Chlas (aC-A40 and aC-B39) are special as they only aC-B31 is directly coordinated to His B470. with absorption maxima at 740 nm. a Tyr A696 b Pseudo-C2 2. Phylloquinone QK-A (yellow) in its binding pocket. It is not yet clear whether transfer of energy This extreme red shift compared to the solution state is thought to proceeds through these two Chlas from the antenna to P700. as these amino acids are conserved between PsaA and PsaB. some are membrane and close to PsaX. a. The centre-to-centre distances symmetry of this trimer implies that the transition dipole moments are 12. Pseudo-C2 axis as grey 914 © 2001 Macmillan Magazines Ltd NATURE | VOL 411 | 21 JUNE 2001 | www.8 AÊ between aC-A40 and eC-A3 and 10.0 Å Cys B574 Cys A587 eC-B2 Asp B575 eC-A1 Trp B673 c A-jk(1) Trp A697 d Leu A722 2. Otherwise. 5). 5). Only one hydrogen bond.5 Å His A680 2.6 Å eC-A3 Met A688 2. QK-B bound similarly by chain. 3.2 Å Asn B591 2. because a counterpart in PsaA related by the pseudo-C2 symmetry would interfere with the monomer±monomer contact in the PSI The `red' chlorophylls trimer and the hydrophobic segment stabilizing the Chla trimer in In S. is interactions. reminiscent of crystal structures and eC-B3. c. eC-A3. Asp. Of these Chlas. possibly both in excitation energy and in electron transfer. the Mg2+ of the structurally and perhaps functionally connect eC-A3 and eC-B3 other two being coordinated to water. isolated from each other.4 Å 2. The Chla trimer is singular in PSI. the ETC and antenna are well separated and of chlorophyll derivatives42. 5b and Table 2).5±3. with interplanar separations within chains. b. Main chain of PsaA as ribbon and a carotenoid (car) in grey. cluster FX. excitonic coupling of Chla can be loose sense. aC-B32 and aC-B33 are coordinated to oxygen atoms of Gln. coordinated by cysteines A578. d. 5c). with axial ligands and hydrogen bonds PsaB. 5c). 40). The pseudo-translational of the ETC to the antenna (Fig. Leu A722 NH to carbonyl-oxygen 4 of QK-A. eC-A2. Although most of the and three dimers.4 Å 2. Chlorophylls of the A branch of the ETC. 41). A587 and B565.7 Å Cys B565 Cys A578 2. In the B branch. to peptides or to water oxygens (Table 2). eC-A2 and eC-B3 show similar with QK-A. Among antenna Chla molecules follows the pseudo-C2 symmetry in a several causes of the red shift41.7 Å A-j Trp B673 Leu A722 QK-A Trp A697 A-k Figure 4 Local environment of membrane-intrinsic cofactors of the electron transfer vertical line. The antenna is extended by 2 light at longer wavelengths (bathochromically or `red-shifted') than sets of 18 peripheral Chla molecules bound to PsaA and PsaB. In the Chla trimer at the lumenal side of the Chla molecules are coordinated to His imidazoles. The arrangement of the PsaA/B-bound to the core of the reaction centre (for review see ref.18 AÊ (Fig.7 Å FX QK-A Car 2. Loops A-hi formed. eC-B2 and eC-B3 could be engaged tions within the stacks. Almost all of the Chla molecules are at Mg2+ ±Mg2+ most safely deduced from the present structure. possibly facilitating light energy capture under forming layer-like structures at the stromal and lumenal sides extreme environmental conditions or focussing excitation energy (Fig. A carotenoid (car) is located in the vicinity of QK-A. Trp A697 p±p stacks involving chlorophylls eC-B2 and eC-A3. If this derive from strong excitonic coupling supported by p±p interac- were the case.articles ETC by not less than . 9 to 11 Chla molecules per monomer absorb PsaB is deleted in PsaA. Putative candidates distances between 7 and 16 AÊ (Fig.3 Å 2.

The C3 axis is lipid were also identi®ed biochemically (D. The carotenoids in B7 B38 B37 (1) and (3) are roughly related by the pseudo-C2 axis to those in (2) M1 L2 L3 and (4). Clusters (5) and (6). 5) is located at the lumenal nearly parallel.nature. Ring substituents of all chlorophylls omitted for clarity. but the pseudosymmetry is less obvious for (5) and (6). Their arrangement may be subdivided into six clusters (Fig. vulcanus45. view direction as in a. aC-A38/aC-A39 to aC-A40 and aC- B37/aC-B38 to aC-B39. preventing formation of toxic singlet oxygen. probably owing to a higher degree of disorder. with (1) forming a few Peripheral Central Peripheral additional contacts to PsaK. the chlorin planes are As the Chla pair aC-A32/aC-B7 (Fig. are in contact with PsaA and PsaB. The two fatty acid chains of each lipid are with respect to a.9 AÊ.139-cis and as 13-cis carotenoids. as 9. Asterisks denote `connecting chlorophylls' (see at the stromal side of the membrane plane and form hydrogen text). PL1 is the single Chla bound to a phospholipid. antenna in grey and red. Linke. Palmitic acid chains of 16 C chlorophyll positions represented by their central Mg2+ ions. Several of the carotenoids show extended p±p stacking with chlorophylls. which is dominant in PSI43. which are lost when the trimer of S. They obey the pseudo-C2 symmetry. Clusters (1).5 AÊ interplanar distance and laterally side of the `trimerization domain' and forms hydrophobic contacts shifted with Mg2+ ±Mg2+ separation of 7.6±8. with one dimer located close to PsaF and the other close to PsaL.47. and photo- B39 eC-B3 K1 protection by quenching excited Chla triplet states by a charge eC-B1 eC-A2 transfer mechanism. thin lines. Some of the chlorophylls referred to in the text are named by a respectively. Of the carotenoids 4 IV that were modelled as complete b-carotenes. each consisting of PsaB antenna PsaA/PsaB antenna PsaA antenna six carotenoids. with only few closer to the lumenal or stromal surface. of 5 which two were modelled as 9-cis and one each as 9. elongatus is split into monomers40. 6 The two other Chla dimers aC-A38/aC-A39 and aC-B37/aC-B38 a are coordinated to PsaA and PsaB at the stromal side of the membrane. 46). A38 J1 A39 J3 J2 Lipids Four lipids are found associated with PsaA/PsaB. b. c. All atoms and stearic acid chains of 18 C atoms were modelled into Mg2+ ±Mg2+ distances . lipids (III) and (IV). PsaL and PsaM. © 2001 Macmillan Magazines Ltd 915 . respectively.6 AÊ) to 60 Chla eC-B2 eC-A3 headgroups. those bound to peripheral subunits in the colour of the coordinating subunits lipids are well de®ned in the electron density map. The pre®x aC. Two vertical lines indicate separation of the antenna Chlas coordinated anchored between transmembrane a-helices of PsaA/B and extend by PsaA/B into a central part and two peripheral parts. the phosphodiester group of lipid (III) binds with roman numerals. IV) and one is a galactolipid (II). PL1 The carotenoids might serve two major functions in photosyn- thesis (for review see ref. (5) is also bound c A32 L1 to PsaF and PsaJ and (6) to PsaI. 1). articles In the three putative red-shifted dimers. Each of the two 3 Chla pairs is close (centre-to-centre distance 16 AÊ) to one of the III `connecting' Chla molecules. The numbers b and con®gurations of these isomers agree well with results from high-performance liquid chromatography analysis on PSI from S. Three are phos- Figure 5 Spatial organization of the cofactors of the ETC and the antenna system in one pholipids (I.99-cis. it could interactions in addition to the calculated strong excitonic coupling have a role in excitation energy transfer between the monomers. 5a). The head groups of the four yellow.3. Chlas belonging to the ETC in blue.16 AÊ. putative nine munication) and immunologically in PSI to be phosphatidylglycerol excitonically coupled `red' chlorophylls in red. whereas only shorter chains could be modelled for capital letter indicating the subunits involved in axial liganding and numbered from N to C. Four lipids (turquoise) labelled bonds with PsaA/B. p-stacked at 3. Side view of PSI antenna rotated 908 about the horizontal axis the antenna Chla aC-PL1. The 22 carotenoids are arranged in clusters 1 to 6. respectively. namely light harvesting in the 450± * 570-nm range where absorption by Chla is negligible. The carotenoids are deeply inserted in the membrane. Theoretical and mutagenesis studies should * be used to show whether these dimers play a role in fast excitation II energy transfer to the ETC through the two connecting chloro- 2 I 1 omitted for clarity. thereby facilitating ef®cient energy transfer from * A40 excited carotenoids to the Chla molecules as well as quenching of Chla triplets. eC-A1 K2 The 22 carotenoids are in van der Waals contact (. (2). personal com- indicated (triangle).44. They are located (Fig. those of the the electron density map for the innermost lipids (I) and (II). * The carotenoids The 22 carotenoids identi®ed in the electron density were modelled as b-carotene. These types of monomer of PSI. due to interaction of the QY transition dipoles. These Chla molecules may be identical to chlorophylls absorbing at 719 nm. which appears ideal for ®ne-tuning B33 B32 B31 X1 the absorption properties of the antenna. (3) and (4) contain 10 carotenoids and are bound to PsaA and PsaB by hydrophobic interactions. 16 adopt the all-trans con®guration and ®ve contain one or two cis bonds. Schematic view of the towards the middle of the membrane. View from the stromal side onto the membrane plane. chlorophylls of the ETC in blue. a. The lipids are related by the pseudo-C2 symmetry: galactolipid (II) NATURE | VOL 411 | 21 JUNE 2001 | www. chlorophylls coordinated by PsaA/PsaB in and monogalactosyldiglyceride44. This suggests p±p to the C-terminal region of PsaL of the adjacent monomer.

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