Structure of light-harvesting antenna complexes of photosynthetic bacteria, cyanobacteria and red algae

TIBS 11 - October 1986

414

Reviews St ructure o f light -harves ti n g antenna

complexes o f

photosynthetic cyanobacteria a n d

bacteria red

algae

H. Zuber S~aural analysis of the various antenna complexes from photosynthetic organisms reveals a multiplicity of antenna structures. In spite of this structural variety, however, available data indicate that general structural principles exit for &ese energy absorbing and transferring systems,

In the photosynthetic apparatus of the various photosynthetic organisms, fightharvesting antennae trap light energy, This energy is directed to the photochemical reaction center (RC) with high efficiency and little energy dissipation. A special chlorophyll (Chl) dimer in the reaction center traps the energy whereupon charge separation results in a photochemical potential (see TIBS, Ref. l). The excited electron is passed irreversibly to electron acceptor molecules in an electron transport chain. In this way, the reaction center initiates two light-driven metabolic processes involving redox reactions. (1) Reductive electron transport; ATP production and the generation of reducing power results in photoassimilation of CO 2, leading to the synthesis of glucose. (2) Oxidation of the substrate H2A; for example, H20 in aerobic photosynthesizing organisms or H2S in anaerobic photosynthesizing organisms, yield oxygen or sulphur, respectively, plus an electron, Structural featuresof light-harvesting antennae In order to understand the physical

antenna systems in bacteria, cyanobacteria, algae and higher plants. Studies have revealed the following general structural principles, (1) Antennae contain numerous pigmerit molecules (Chl, bilins or carotenoids- between 25 and 1000 pigments per reaction center) that are highly ordered2, 3. Their position and orientation follow defined laws of symmetry, (2) On the basis of this highly ordered arrangement of pigments, energy passes between the pigment molecules in the form of excited singlet states through random walk within 10 -13 s (Refs 4-7). Processes which would break down the excited singlet states, such as non-radiative relaxation or fluorescence emission, do not occur due to a combination of mechanisms: (i) when the distances between the pigments are greater than 20 A energy moves by slow inductive resonance transfer (Frrster); (ii) at distances of less than 20 ~ pigments can be more strongly electron-coupled and form excitons 3. (3) Pigment molecules form clusters

within the antenna complexes 7. These clusters can have differing absorption mechanism of this directed energy trans- maxima and, as energy flows from shortfer to the reaction center, knowledge of wavelength-absorbing clusters to longthe structures and, particularly, general wavelength-absorbing clusters, form a structure principles of antenna systems system for heterogeneous (i.e. directed) are important. In particular, what is the energy transfer to the reaction center 2,8. basis of the high efficiency of this In this way, and by spatial separation of cooperative antenna-reaction center pigment clusters in the antenna comsystem, adapted to prevailing light plexes, random walk is minimized. This conditions? In recent years, interest directed transfer of energy is reinforced has focused on the structure of the by built-in energy traps (longwavelength-absorbing excitons). Energy H. Zuber is at the lnstitute for Molecular Biology and traps (localized exeitons) in the form of Biophysics, Eidgen Technical University, ETH- pigment dimers are found within the Hrnggerberg-HPM, CH4?O93Ziirich, Switzerland. antenna complexes. In this way, the ¢~ 1986, Elsevier Science Publishers B.V.,Amsterdam

0376 5067/86/$(12.00

special pigment pair of the reaction centerI also functions as an energy trap of thesystem, center cooperative antenna-reaction Fundamental to the formation of pigmerit clusters in the antenna complexes reaction center are the structure and organization of the antenna polypeptides2, 3. Structural analysis has shown that all pigment molecules are bound at defined binding sites to relatively small

or

polypeptides (6-30 kDa); Chl, bacteriochlorophyU (BChl) and carotenoids are non-covalently bound and bilins are covalently bound. Polypeptides determine the type, number, position, orientation, distance and environment of the pigments, i.e. the three-dimensional organization of the pigments for energy transfer. The regular arrangement of the pigments is based on a regular and symmetrical arrangement of antenna polypeptides within the antenna complexes with repeating basic elements (for exampie, ct-fl-polypeptidepairs). The absorption range of antenna systems of the diverse photosynthetic organisms runs from 400 nm (carotenoids) to 1000 nm (BChl). There is a clear distinction between the spectral range of oxygenic photosynthetic organisms (500-700 rim, in cyanobacteria, algae and plants) and anoxygenic photosynthetic organisms (700-1000 rim, in bacteria). The position of the antenna complexes and the antenna polypeptides within the photosynthetic apparatus is important for the structure of the antenna system. In general, antenna complexes are located within the photosynthetic membrane surrounding the reaction center (core antennae, peripheral antennae). In addition, for the extension of heterogeneous energy transfer down to shorter wavelengths into the blue range (700-760 nm or 5(10670 nm, respectively), green photosynthetic bacteria and cyanobacteria have localized antenna systems (peripheral antennae) on the surface of the membrane - the chlorosomes or phycobilisomes. Four main types of antenna polypeptides have been differentiated so far in the various antenna complexes. (1) Hydrophobictransmembranepolypeptides in intramembrane antennae of bacteria (Rhodospirillacae, Chromatiaceae, Chlorobiaceae and Chloroflexaceae).

TIBS 11 - October 1986 (2) Mixedtypes of polypeptides, having a transmembrane part and a large, globular part lying in the membrane surface, in the intramembrane complexes of algae and higher plants, (3) Globular polypeptides (phycobiliproteins) in the extramembrane systems of phycobilisomes in cyanobacteria, red algae and Cryptophyceae. (4) Fibrillary polypeptides in extramembrane antennae of chlorosomes in green photosynthetic bacteria (Chlorobiaceae and Chloroflexaceae). Light-harvesting antennae of photosynthetic bacteria The simplest antenna system is found within the photosynthetic membranes of bacteria. In green bacteria this is in the cytoplasmic membrane, whereas in purple bacteria it is in the intracytoplasmic membrane in the form of vesicular, lamellar and rod shaped structures, sometimes filling the entire cell. In Rhodospirillaceae and in Chromatiaceae three types of antenna complexes have been found in the photosynthetic membrane, each having different absorption maxima9: complex B870 (absorption maximum 870 nm) in direct

415 proximity with the reaction center (core complex) and complexes B800-850 (800, 850 nm), and B800-820 (800,820 nm), at increasing distances from the reaction center (peripheric antennae). Thus, a concentric circular arrangement of the antenna complexes in the environment of the reaction center forms a system for heterogeneous energy transfer (see above) from the outside (B800-820) via B800-850 to the inside (B870 and reaco tion center). The individual types of purple bacteria vary in the extent of their heterogeneous energy transfer systems, Rhodospirillum rubrum and Rhodopseudomonas viridis have only one complex (B870 or B1020). Rhodopseudomonas sphaeroides has two complexes (B870, B800-850) and Chrornatium vinosurn and Rhodopseudomonas acidophila have three complexes (B870, B800-850, B8(X)~820). The basic structural and functional element of antenna complexes is a heterodimer of small c(and 13-polypeptides, each consisting of 50--60 amino acid residues2. 3. Primary structure analyses of the ct- and [3polypeptides of a number of photosynthetic bacteria show these polypeptides to have a typical three-domain

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structure 2,3,1°-12 (Fig. 1). The central, hydrophobic domain indicates a transmembrane orientation of the u- and 13polypeptides in (1-helix form (Fig. 2a). The predicted location of the C- and Nterminal domains is on the surface of, or in the polar head region of the membrane. Cleavage of part of the N-terminal domains of the it- and 13-polypeptides on the cytoplasmic side of the membrane by partial hydrolysis with proteolytic enzymes demonstrates their orientation in the membrane 13. The binding sites for BChl molecules (via the central magnesium atom) are probably the conserved histidine residues found in all u- and 13-polypeptide chains in the hydrophobic domain. Thus, a pair of exciton-coupled BChl molecules (separation 10--15 ~ ) is formed in the u-13heterodimer2, 3. An individual BChl, probably bound at the second conserved histidine of the 13-chain (near the Nterminus) serves to provide additional photon trapping (energy migrates to the central BChl pair). A number of other conserved amino acid residues have been found which are probably of structural or functional importance, e.g. aromatic amino acid residues at a certain

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Fig. 1. Primary structures of the (1- and ~-antenna polypeptides from various antenna complexes (B870, B1015, 6800-850, B 8 0 0 ~ 5 ) from various purple and green (Chloroflexus aurantiacus) photosynthetic bacteria. Typical aromatic amino acid residues in homologous positious in the primary structure are found in all a- and~or ~-polypeptides (11); in the polypeptides of B870, B806~65, B1015 (X), B870 of Rhodopseudomonas sphaeroides or Rhodopseudomonas capsulata (e); and 6800~50 o f R p . sphaeroides or Pp. capsulata (o).

416

TIBS 11 - October 1986 PK

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distance from the pigment (BChl, carotenoid) binding sites. Like the membrane itself, the hydrophobic domain of the antenna polypeptides has an asymmetric structure. The part exposed to the periplasmic side carries the BChl pair, and the part exposed to the cytoplasmic side is probably the interaction site for tt- and 13-polypeptides, leading to the formation of the heterodimers and to the association of the heterodimers into the larger aggregates of the antenna polypeptides (antenna complexes)2,3. It is probable that cyclichexamers (peripheral antennae, 12 polypeptides in B800~50; Fig. 2b) and cyclic dodecamers (24 polypeptides in B870/890) are formed in the environment of the reaction center (core antennae). Electron microscopic studies (including image processing) also show this dodecamer structure (Rp. viridis) 14. In this way, cyclic BChl clusters arise for energy transfer within the antenna complexes. The specific interaction of the N- and C-terminal domains of the antenna polypeptides result in the concentric arrangement of the diverse antenna complexes, corresponding to the absorption maxima gradient, and yield the system for heterogeneous directed energy transfer to the reaction center. In addition to an intramembrane

chlorosomes15. These large particles lie on the inner side of the cytoplasmic membrane 15 and carry approximately 10 000 BChl molecules. They have an absorption maximum at740nm(Chloro-

flexus aurantiacus), so that, in terms of heterogeneous energy transfer, energy migrates from the chlorosomes via the intramembrane antennae (808-865 nm) to the reaction center (865 nm). The

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417

T I B S 11 - October 1986

antenna complex B808-865 in the cyto- tron microscopy 15, the a-helices carrying plasmic membrane of C. aurantiacus the BChl c are associated in aggregates contains approximately 20-25 BChl a of 12 (fibrillary basic elementsl8; Fig. per reaction center 16, probably com- 3b). Through a side-by-side arrangeposed of a- and [3-antenna polypeptides ment of the fibrillary rod shaped ele(heterodimers). Studies of sequence ments, a system for heterogeneous homology (three-domain structure) energy transfer is built (Fig. 3c). A water show that they are phylogenetically soluble BChl a-protein complex (809 related to the a- and J3-polypeptides of nm, base plate complex), probably the B870 complex of purple bacteria 17. located between the chlorosomes and An antenna polypeptide was isolated the intramembrane antenna complex, from the chlorosomesin C. aurantiacus 16 was isolated from Prosthecochloris aesand its primary structure determined 18. tuarii, and its three-dimensional strucUnlike the intramembrane antenna ture determined ~9. The complex is a 150 polypeptides, this polypeptide (51 amino kDa polypeptide trimer, each one of the acid residues) does not show a three- three subunits (50 kDa)containing seven domain structure; its primary structure BChl molecules bound within a cylinder suggests that it probably forms an a-helix of mainly [3-pleated sheet structure. (Fig. 3a). This is also suggested by the Energy transfer between the BChl a asymmetric and helical distribution of molecules, spaced at an average of 12,~, glutamine and asparagine residues, can be described on the basis of an which are possible binding sites for the exciton model. BChl molecules. In such a conformation, seven BChl molecules can specifically Light-harvesting antennae of interact over the carbonyl function of cyanobacteria, red algae and Ring V and the hydroxyethyl group of Cryptophyceae Ring I (typical for BChl c) (Fig. 3a). In The phylogenetically ancient cyanothis way a cluster of seven BChl c bacteria, probably the first to produce molecules, which are exciton-coupled, is oxygen, and the younger, eukaryotic red formed. It is thought that in the so-called algae and Cryptophyceae have three anrod shaped elements identified by elec- tenna systems: the antenna complexes

PSI and PSII (similar to green algae and higher plants) located in the thylakoid membrane, and the extramembrane antennae of the phycobilisomes8,2°. The phycobilisomes lie in a regular arrangement on the surface of the thylakoid membrane and contain, as hemi-ellipsoidal or hemi-discoidal (Fig. 4b) polypeptide aggregates, approximately 300800 phycobilin pigments (blue or red open-chain tetrapyrroles). This antenna system is made up of various antenna complexes containing phycobiliproteins of varying absorption maxima 2,8,2°. In the phycobilisome, a phycobiliprotein core region is surrounded by phycobiliproteins in the form of stacked disc shaped (rod region) polypeptide aggregates. In the cyanobacterium Mastigocladus laminosus 21 (Fig. 4b), the longestwavelength-absorbing allophycocyanin (AP, 670 nm) lies inside the core region of the hemi-discoidal phycobilisome. The shorter-wavelength-absorbing phycocyanin (PC, 620 nm) lies further away in the rod region; and the shortest-wavelength-absorbing phycoerythrocyanin (PEC, 568 rim) lies on the periphery. Thus, a system for heterogeneous energy transfer is formed with a directed flow of energy from the outside to the inside and

(a) 84

Fig, 4, (a) ~ree-dirr~nsio~l structure and arrangen'~nl of the a-helic~ (X, Y,A,B,E,F, G,H) in the (a-~) monomer of C-phyc~:yanin from Mastigoclad~ laminosus.84, 155, positions of the bilinpigments. (b) Structure and organization of the phycobilisome of M. laminosusand arrangement of the phycocyanin (PC) and phycoerythrin (PEC) hexamers (linkerpolypeptide complexes) in the rod region and of allophycocyanin (AP) trimers in the core region. The linker polypeptides are located in the central cavity of the hexamers.

418

T I B S 11 - October 1986 tl

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X-ray structure analysis of phycocyanin from M. laminosus reveals that it Pc PE(PEC) is the folding of the polypeptide chain I I } I ~ and the aggregation of folded ct- and 13polypeptide chains, that brings bilin pig1 ~ PE(PEC) pcAP PE~43 m ~(~C) ments into positions and orientations (a) suitable for heterogeneous energy transfer1, 2s. This analysis shows the structure (or-helices) of the monomer (Fig. 4a) and ~" 1'| 143 of the cyclic PC trimer, made up of three (ct-13) monomers (six polypeptide chains) (Fig. 5b). In the trimers the t184 ['1155 phycobilins ct84 and 1384are located close together (heterodimers), ct84 lying o u t ~ A t150-61 ~.~" side and 1384 lying inside, pointing _, ? towards the hollow interior of the trimer. ~ /r The binding site at position 13155 (PC, PEC, PE) and the additional sites for 1"t84 ~ "4"" binding bilins 1350/60 and ct143 of PE ['1155 from FremyeUa diplosiphon are also on I1 50 - 61 the outside 27. The function of such external pigments is to trap energy (sen~ ~ ~ sitize)2,3,22. Their spectral characteris~ 0 84 tics, position and orientation result in a < ~ heterogeneous, directed energy transfer to bilin 1384 (fluorescing pigment) in the 143 .~ 17 ~ " ~" center of the complex 3. As a result of the " specific way in which the two trimers are • associated in the hexamers, the 1384 pig~ ments become functionally coupled, "~ ~ ~ possibly to a special exciton system. • ,/~ A ~ ' ~ Similarly, the way that the hexamers are ' ~ arranged in the rods of the phycobilia 84 , f] 143 ~ a50-61 # ,~ some may result in the coupling of the , /r energy transfer systems of the hexamers. (13) ~ 1"t155 Energy can pass among the various hexamers of PC and PEC, with different Fig. 5. (a) Covalent binding sites (positions) of the bilin pigments in the primary structure of the ct- and absorption maxima, in the direction of ~-polypeptidechains(160--17Oaminoacidresidues) of the phycobiliproteins. Numbers indicatepositions in the core region (AP). Linker polypepthe primary structure. Binding sites in allophycocyanin (AP), in phycocyanin (PC), in phycoerythrin (PE), tides, which do not carry pigments, play in phycoerythrocyanin (PEC). (b) Three-dimensional structure of C-phycocyanin from Mastigocladus a significant role in correctly arranging laminosusa cyclic trimer of (a-[I) monomeric units. 084, ~84, [ff55, positions of the bilin pigments in the the phycobiliprotein hexamers in the three-dimensional structure ofC-phycocyanin (phycoerythrocyanin andphycoerythrin), o,50~l, [~143,posphycobilisome and in conferring specific sible additional bilin binding sites in phycoerythrin trimers. Numbers indicate positions in the primary struc- spectral characteristics on the hexature. mers s,2° (Fig. 4b). The various linker polypeptides (~30 kDa) bind in the hollow center of the trimers/hexamers (Fig. 4b) of PEC or PC and thus determine then to the reaction center in the mem- or hexamers (ct-13)6, which are important their position within the phycobilisome brane 2,3,22. Each of the antenna com- for the structure of the phycobilisome, rod. At the same time, they modulate plexes, AP, PC and PEC, is made up of Also, they all have open-chain tetra- the spectral characteristics of the hexathe basic elements of the ct- and [3- pyrroles (bilins) covalently bound via mers according to their location in the polypeptide chainsS2L The ct- and 13- thioether bonds to cysteine residues rod region (e.g. in PC, the 29.5 kDa polypeptide chains of AP 23, PC 24 and (Fig. 5a). The most important conserved linker polypeptide-PC complex absorbs PEC 2s in M. laminosus have homo- bilin binding site that is found in all at a shorter wavelength than the 34.5 Iogous sequences 22,26 (Fig. 5a). From phycobiliproteins (see also Refs 8 and kDa linker polypeptide-PC complex). these homologies a phylogenetic relation- 20) is at cysteine 84. Bilin binding sites Linker polypeptides in the core region ship and phylogenetic tree can be derived are found in position 155 (13) in the case (8-10 kDa) have a similar function (Fig. for the evolution of the phycobiliproteins of PC and PEC, but not in AP (M. 4b). Also in the core are specific energy and the phycobilisomes26. On the basis laminosus). Other cyanobacteria and traps, such as AP-B and the 89 kDa of their similar primary structure, the red algaeS,20,27 contain another type of polypeptide with bilins that absorb at phycobiliproteins have similar structural short-wavelength-absorbing phycobili- very long wavelengths (670 nm). From and functional characteristics; for protein, phycoerythrin (PE), which shows here, the entire energy of the phycobiliexample, they all form (by specific aggre- additional phycobilin sites (phycoerythro- some is passed to Chl a (mainly PSII) in gation) monomers (ct-13), trimers (ct-13)3 bilin) at positions 50/61 ([~)and 143 (ct). the thylakoid membrane. PE

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419

T I B S 11 - O c t o b e r 1986

The following points are of interest, (1) Phycobiliproteins have homologOUS sequences to and are phylogenetically related to the linker polypeptides 29, suggesting that they all evolved from the same one-chain globin precursor molecule, (2) The three-dimensional structure, i.e. the type and arrangement of the uhelices of the u - o r [3-polypeptides, of PC (and the other pbycobiliproteins) of the old, probably original oxygen-producing cyanobacterium M . l a m i n o s u s (and the other cyanobacteria), is very similar and phylogenetically related to that of myoglobin and hemoglobin, younger roammalian proteins which bind and transport oxygen (Fig. 4a). In eukaryotic Cryptophyceae (cryptomonads) the phycobiliprotein antenna complexes do not form large phycobilisomes on the thylakoid surface; rather, they are located as small particles in the intrathylakoid lumen, and are composed of only one type of phycobiliprotein (PC or PE). Thus, they represent small, heterogeneous energy transfer units conraining two ct- and two 13-polypeptide chains30, 31. T h i s particular quaternary s t r u c t u r e probably arises because the Nterminal region of the ct-polypeptide chain up to position 61, present in the sequence homologous phycobiliproteins in cyanobacteria and red algae is absent (as was found, for example, in phycocyanin 645 from C h r o o m o n a s 31) •

Due to the absence of the helices X, Y, A and B of the ~t-chain (Fig. 4a), it appears that dimers, rather than cyclic trimers of the (ct-13) m o n o m e r s , are formed. Conclusion The large antenna systems of all photosynthetic organisms consist of basic u n i t s o f polypeptides which bind pigment molecules in a specific and highly ordered manner. These antenna polypeptides determine the type, number, position, orientation, distance and environment of the pigments. The polypeptide-pigment units aggregate to large, highly structured polypeptide-

pigment arrays for directional energy transfer to the reaction center. This directed energy transfer is based on a series of antenna complexes containing pigment clusters with different absorption maxima (heterogeneous energy transfer) and on exciton-coupled dimers or oligomers of pigment molecules (energy traps) within the antenna cornplexes. An important structural unit in all antenna systems seems to be the polypeptide pair, which may be the basis for the formation of specific (localized) excited states of the pigment clusters within the antenna complexes. In recent years knowledge of the structural organization oftheantennasystems has grown rapidly. For future research it will be important to take into account these general structural principles and to concentrate on the detailed molecular structure of the antenna complexes and their specific arrangement in the whole antenna. Only on this basis will biophysical studies and theoretical considerations lead to an understanding of the physics of energy transfer and energy transduction in photosynthesis.

10 Brunisholz, R. A., Suter, F. and Zuber, H. (1984) Hoppe-Seyler's Z. Physiol. Chem. 365, 67~688 11 Brunisholz, R.A., Jay, F., Suter, F. and Zuber, H. (1985) Hoppe-Seyler's Z. Physiol. Chem. 366, 87-88 12 Theiler, R., Suter, F., Wiemken, V. and Zuber, H. (1984) Hoppe-Seyler's Z. Physiol. Chem. 365,703-719

13 Brunisholz, R. A., Wiemken, V., Suter, F., Bachofen,R. and Zuber, H. (1984) HoppeSeyler's Z. Physiol. Chem. 365,689-701 14 Stark, W., Kfihlbrandt, W., Wildhaber, H., j.Wehrli'3,777-783E" and Miihlethaler,K. (1984) E M B O 15 Staehelin,L. A., Golecki,J. R., Fuller,C. and Drews, G. (1978) Arch. Microbiol. 119, 269-277 16 Feick,

R.G.

Biochem.

and Fuller,

R.C.

(1984)

23, 3693-3700

17 R.Wechsler' andT"zuber,Brunish°lZ' c. (1985)R" H. FEBsSUteF.,Lett.Fuller,191, r'

34-38 18 Wechsler, T., Suter, F., Fuller, R.C. and Zuber, H. (1984) FEBS Lett. 181,173-178 19 Matthews, B. W., Fenna, R. E., Bolognesi, M.C., Schmid,M. F. and Olson, J. M. (1979) J. Mol. Biol. 131,259-285 20 Glazer, A. N. (1984) Biochim. Biophys. Acta 768,29-51

21 Niess, M. and Wehrmeyer, W. (1981) Arch. Microbiol.

129,374-379

22 Zuber, H. (1985) In Optical Properties and Structure of Tetrapyrroles (Blauer, G. and Sund, H., eds), pp. 425~141, Walter de

References 1 Deisenhofer, J., Michel, H. and Huber, R. (1985) Trends Biochem. Sci. I0, 243-248 2 Zuber, H. (1985) Photochem. Photobiol. 42,

821-844 3 Zuber, H. (1985) in Antennas and Reaction Centers of Photosynthetic Bacteria (Springer Series in Chemical Physics Vol. 42) (MichelBeyerle, M. E., ed.), pp. 2-14, Springer-Verlag 4 Knox, R. S. (1977) in Topics in Photosynthesis (Vol. 2) (Barber, J., ed.), pp. 55-97, Elsevier 5 Pearlstein, R. M. (1982) Photochem. Photobiol. 35,835~44 6 Van Grondelle, R. (1985) Biochim. Biophys. Acta 811,147-195

7 Pearlstein, R. M. and Zuber, H. (1985) In Antennas and Reaction Centers of Photosynthetic Bacteria(Springer Series in Chemical Physics Vol. 42) (Michel-Beyerle, M.E. ed.), pp. 53~1, Springer-Verlag 8 Glazer, A. N. (1983)Annu. Rev. Biochem. 52, 125-157 9 Thornber,.1. P.,Cogdell, R. J.,Pierson,B. K. and Seftor, R. E. B. (1983) J. Cell. Biochem.

23,159-169

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