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Identification of a Single Peridinin Sensing Chl-A Excitation in Reconstituted PCP by Crystallography and Spectroscopy

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Identification of a Single Peridinin Sensing Chl-A Excitation in Reconstituted PCP by Crystallography and Spectroscopy Identification of a single peridinin sensing Chl-a excitation in reconstituted PCP by crystallography and spectroscopy Tim Schultea,1, Dariusz M. Niedzwiedzkib,1,2, Robert R. Birgeb, Roger G. Hillerc, Toma´ sˇ Polívkad,e, Eckhard Hofmanna,3, and Harry A. Frankb,3 aBiophysics, Department of Biology and Biotechnology, Ruhr-University Bochum, D-44780 Bochum, Germany; bDepartment of Chemistry, University of Connecticut, Storrs, CT 06269-3060; cBiology Department, Faculty of Science, Macquarie University, NSW 2109, Australia; dInstitute of Physical Biology, University of South Bohemia, 373-33 Nove Hrady, Czech Republic; and eBiological Centre, Czech Academy of Sciences, Ceske Budejovice, Czech Republic Edited by Steven G. Boxer, Stanford University, Stanford, CA, and approved October 14, 2009 (received for review August 8, 2009) The peridinin-chlorophyll a-protein (PCP) of dinoflagellates is fied complexes has not been possible, although 2D crystals of unique among the large variety of natural photosynthetic light- reconstituted LHCII have been reported (11). harvesting systems. In contrast to other chlorophyll protein com- As noted above, a wide variety of light-harvesting complexes plexes, the soluble PCP is located in the thylakoid lumen, and the is found in nature, but the soluble peripheral antenna peridinin- carotenoid pigments outnumber the chlorophylls. The structure of chlorophyll a-protein (PCP) is unique in that it is the only system the PCP complex consists of two symmetric domains, each with a where the bound carotenoids stochiometrically outnumber the central chlorophyll a (Chl-a) surrounded by four peridinin mole- Chls. The peridinin (Per)-to-Chl ratio is 4:1 in the minimal cules. The protein provides distinctive surroundings for the pig- functional unit. A high-resolution (2.0 Å) structural determina- ment molecules, and in PCP, the specific environment around each tion of the main form of PCP (MFPCP) revealed a trimeric peridinin results in overlapping spectral line shapes, suggestive of quaternary structure, with each monomer consisting of two different functions within the protein. One particular Per, Per-614, domains connected by a loop. The domains are related by a is hypothesized to show the strongest electronic interaction with twofold pseudosymmetry axis and each encloses a central chlo- BIOPHYSICS AND rophyll a (Chl-a) surrounded by four Pers (12). the central Chl-a. We have performed an in vitro reconstitution of COMPUTATIONAL BIOLOGY pigments into recombinant PCP apo-protein (RFPCP) and into a Peridinin, along with other carotenoids possessing a carbonyl mutated protein with an altered environment near Per-614. group, exhibits the anomalous photophysical behavior of a Steady-state and transient optical spectroscopic experiments com- strong polarity-induced solvent effect on its excited-state life- paring the RFPCP complex with the reconstituted mutant protein time. This effect has been attributed to the presence of an identify specific amino acid-induced spectral shifts. The spectro- intramolecular charge transfer (ICT) state that acts in conjunc- scopic assignments are reinforced by a determination of the tion with the lowest excited singlet state S1 (13). In PCP the structures of both RFPCP and the mutant by x-ray crystallography dominant energy transfer pathway from peridinin to Chl-a is via Ϸ to a resolution better than 1.5 Å. RFPCP and mutated RFPCP are this S1/ICT state, whose lifetime is 2.5 ps in the PCP complex, unique in representing crystal structures of in vitro reconstituted corresponding to an efficiency of 80% for this preferred route light-harvesting pigment-protein complexes. (14–16). The dominance of the S1/ICT-mediated pathway may be due to the unique properties of a state that can induce light harvesting ͉ peridinin ͉ protein crystallography ͉ refolding ͉ coupling to Chl-a while maintaining an energy high enough for efficient transfer to Chl-a (17). transient absorption spectroscopy Studies on native forms of PCP have shown that the bound Pers possess distinct spectral absorption features because of any naturally occurring light-harvesting pigment-protein differences in their immediate protein environment (18–20). A Mcomplexes use chlorophyll (Chl) to collect incoming pho- notable case is Per-612 (Fig. 1), whose environment has been tons, and most of these systems rely on carotenoids to supple- postulated to result in a dramatic blue shift of its absorption ment light-capture in the spectral region of maximal solar spectrum, leading to less efficient direct energy transfer to Chl-a, irradiance from 420 to 550 nm. Carotenoids function as energy compared to that from the other bound Pers (19–23). Another donors in many different natural antenna systems and operate prominent example is Per-614, which has been assigned the with an efficiency that ranges from 30% to nearly 100%. strongest electronic interaction with Chl-a (19, 21, 24–28). This Carotenoids also fulfill a crucial photoprotective role that pre- enhanced interaction was identified from transient absorption serves the structural and functional integrity of the photosyn- measurements of the onset of bleaching of a Per absorption band thetic apparatus. A detailed knowledge of the controlling fea- tures of energy transfer in natural light-harvesting systems is critical for designing efficient artificial mimics (1). Author contributions: E.H. and H.A.F. designed research; T.S., D.M.N., and R.R.B. performed Structural determinations of several antenna complexes have research; R.G.H. contributed new reagents/analytic tools; and T.S., D.M.N., R.R.B., R.G.H., T.P., E.H., and H.A.F. analyzed data and wrote the paper. lead to theoretical treatments of the photophysical processes The authors declare no conflict of interest. undergone by the bound pigments and which control photosyn- thetic light harvesting (2). An effective approach to explore This article is a PNAS Direct Submission. light-harvesting is mutagenesis of specific residues in conjunc- Data deposition: The coordinates and structure factors have been deposited in the Protein Data Bank, www.pdb.org [PDB ID codes 3IIS (RFPCP) and 3IIU (N89L mutant)]. tion with pigment substitutions or incorporations, as shown for 1T.S. and D.M.N. contributed equally to this work. the bacterial LH2 complex (3, 4). This approach has also been 2Present address: Department of Biology, Washington University in Saint Louis, St. Louis, applied to the membrane-bound light-harvesting complex II MO 63130. (LHCII) from higher plants, for which a robust in vitro recon- 3To whom correspondence may be addressed. E-mail: [email protected] or stitution system has been developed (5). While high-resolution [email protected]. x-ray-derived structures exist for both native LH2 (6–8) and This article contains supporting information online at www.pnas.org/cgi/content/full/ LHCII (9, 10), three-dimensional (3D) crystallization of modi- 0908938106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0908938106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 29, 2021 Fig. 1. Structure of RFPCP. Two protein subunits (black and gray) form a dimer enclosing the pigment molecules (Chl-a in green and Per in orange). N- and C-terminus and Per numbers of the subunits are labeled. following Chl-a excitation (25). Per-614 is also presumed to be the main quencher of long-lived Chl-a triplet states (26–28). Although these investigations suggest a special role for individ- ual peridinins, none has been directly assigned so far. The goal of the present study is to correlate the structure of Fig. 2. Superimposition of the protein helices of RFPCP (gray) and MFPCP the PCP complex with the spectroscopic features of the bound (yellow) and the pigments of RFPCP (colored) and MFPCP (black). N- and pigments, and in particular to assign an absorbance signature to C-terminus of the MFPCP protein, as well as MFPCP Per numbers, are labeled. a single peridinin, Per-614. We performed site-directed mu- tagenesis on the PCP apo-protein changing asparagine-89, which rmsd [calculated with lsqman (30)] of the atomic positions of the is close to the conjugated ␲-system of Per-614, to leucine, and Pers and Chls are rather low (overall rmsd Ϸ0.5 Å: see Tables have refolded the modified (N89L) protein in the presence of Per S2–S4). The lipid in RFPCP is found at the same position as in and Chl-a. Through a comparative study of the spectroscopic MFPCP, but its exact coordination is changed (rmsd of 1.5 Å) properties of the reconstituted PCP (RFPCP) and the N89L (see Table S2). This change is mainly caused by the first head mutant, we have identified the steady-state and transient ab- sorption spectra associated with the single Per postulated to have group of the lipid, which is more fixed in MFPCP because of enhanced interaction with Chl-a. The structural details of the intermonomer contacts in the trimer. Additionally, the aliphatic site-directed mutagenesis are revealed by high-resolution x-ray chains of the lipid show some variations in their exact location. analyses of RFPCP and the N89L mutant. These 3D crystal In contrast to the crystal structure of MFPCP, trimerization of structures are unique in being an in vitro reconstituted light- the homodimeric RFPCP is not observed because of the iden- harvesting pigment-protein complex. tical amino acid sequence of both domains. In MFPCP, the sequences of the two domains are not identical, causing local Results differences that provide the binding patches for trimerization. Structural Model of RFPCP—Comparison with MFPCP. The crystals of RFPCP diffracted to 1.4 Å; the structural model was solved by N89L Mutant Structure: Probing the Binding Site of a Single Peridinin. molecular replacement and could be refined to an R-factor of The primary reason for making the N89L mutation of RFPCP was to alter the environment of Per-614 without affecting the 15.2 and a Rfree-factor of 18.7 (crystallographic statistics are given in Table S1).
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