For ma tion of Bacteriochlorophyll Anion Band at 1020 nm Produced by Nu clear Wavepacket Motion in Bacterial Reaction Cen ters

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1 Jour nal of the Chi nese Chem i cal So ci ety, 2000, 47, For ma tion of Bacteriochlorophyll Anion Band at 1020 nm Produced by Nu clear Wavepacket Motion in Bacterial Reaction Cen ters A. G. Yakovlev a and V. A. Shuvalov a,b * a Lab o ra tory of Photobiophysics, Belozersky In sti tute for Chem i cal and Phys i cal Bi ol ogy of Mos cow State Uni ver sity, Mos cow , Rus sian Fed er a tion b In sti tute of Ba sic Bi o log i cal Prob lems, Rus sian Acad emy of Sci ences, Pushchino, Mos cow Re gion , Rus sian Fed er a tion For ma tion of a nu clear wavepacket on the po ten tial en ergy sur face of the pri mary elec tron do nor P* in duced by 30fs ex ci ta tion of pheophytinmodified Rhodobacter sphaeroides R26 re ac tion cen ters leads to a re vers ible and ir re vers ible ap pear ance of the state P + B A mon i tored by the mea sure ments of the 1020nm band which is char ac ter is tic of the rad i cal an ion band of bacteriochlorophyll mono mer B A. The re vers ible ap pear ance of the state P + B A is char ac ter ized by two (130 and 320 cm 1 ) vi bra tion modes and re lated to the cre ation of max i mal value of the FranckCondon fac tor when the wavepacket is near an in ter sec tion of the P* and P + B A po ten tial en ergy sur faces. The ir re vers ible for ma tion of the state P + B A with a time con stant of 3 ps is ac com pa nied by os cil la tions with fre quen cies of 9 and 33 cm 1. These re sults show that the nu clear vi bra tion modes (9 and 33 cm 1 ) on the P * po ten tial en ergy sur face have near their bot tom the in ter sec tion with the P + B A sur face as well. The elec tron trans fer time be tween P* and B A was es ti mated to be in the range of 700 fs. This is larger than the wavepacket in ter sec tion time for the 130 cm 1 mode (~100 fs) and com pa ra ble with that for the 33 cm 1 mode (~600 fs). There fore the re vers ible elec tron trans fer with small am pli tude can be ob served for the 130 cm 1 mode, while the ir re vers ible one is al lowed for the 33 cm 1 mode that is prob a bly im por tant for the pri mary charge sep a ra tion. IN TRO DUC TION The pri mary charge sep a ra tion in bac te rial re ac tion cen ters (RCs) re sults in the ox i da tion of the pri mary elec tron do nor, bacteriochlorophyll dimer P, and in the re duc tion of bacteriopheophytin H A with a ~3 ps time con stant at 20 o C (see Refs. 1 and 2). The par tic i pa tion of bacteriochlorophyll mono mer B A (ac tive pig ment branch A) in elec tron trans fer (ET) be tween P* and H A was sug gested on the ba sis of pi co sec ond mea sure ments in Since that time this prob lem was stud ied in many fur ther works. 414 Re cent mea sure ments in pheophytin amod i fied RCs 68,1214 and in the mu tant 10 have shown that the en ergy of the P + B A state in these RCs is close to or even be low that of P * by cm 1. 15,16 The time con stant for ET from P* to B A is about 1.6 ps at 5K in mod i fied RCs 14 which is sim i lar to that for na tive RCs. These ob ser va tions strongly sup port the model in which B A is a dis tinct in ter me di ate and a pri mary elec tron ac cep tor. In pre vi ous works it was found that the ex ci ta tion of bac te rial re ac tion cen ters (RCs) at 870 nm by 30fs pulses in duces a nu clear wavepacket mo tion on a P * po ten tial en ergy sur face. This leads to fsoscillations with fre quen cies in the range of cm 1 in an emis sion from P* 1722 and in an ab sorp tion band of B A at 800 nm. 23 It was shown 24 that in pheophytin modified RCs the 130 cm 1 os cil la tions are ac com pa nied by the re vers ible for ma tion of the 1020nm band that is char ac ter is tic of the rad i cal an ion band of bacterio chlorophyll mono mer B A. 7,14,25 It was sug gested 24 that the re mark able and re vers ible for ma tion of the 1020nm band at 120fs de lay is in duced by a wavepacket mo tion near an in ter sec tion of P* and P + B A po ten tial en ergy sur faces. At this in ter sec tion a max i mal value of the FranckCondon fac tor (close to 1) is cre ated. It was also sug gested that ir re vers ible elec tron trans fer (ET) from P* to B A is prob a bly con nected to lower fre quency modes that form their po ten tial sur faces hav ing the in ter sec tion with the P + B A sur face. In the pres ent study we ex am ined ki net ics of absorbance changes ( of the 1020nm band in the wide range of de lays from 50 fs to 7 ps in the pheophytinmodified RCs ex cited by 30fs pulses at 870 nm. The re vers ible and ir re vers ible for ma tion of the state P + B A mon i tored by the 1020 nm band mea sure ments was found. The ir re vers ible for ma tion of P + B A Ab bre vi a tions: A, lightminusdark absorbance changes; B A and H A, bacteriochlorophyll and bacteriopheophytin mono mers, re spec tively, lo cated in ac tive branch A; ET, elec tron trans fer; F, FranckCondon fac tor; P, pri mary elec tron do nor; Q, quinon; RC, re ac tion center.

2 710 J. Chin. Chem. Soc., Vol. 47, No. 4A, 2000 Yakovlev and Shuvalov with a time con stant of 3 ps is ac com pa nied by os cil la tions with fre quen cies of 9 and 33 cm 1 which were ob served ear lier in the 800nm band of B A. 23 These modes were found to have the po ten tial en ergy sur face in ter sect ing the P + B A sur face. The in ter sec tion time (~600 fs) for the 33 cm 1 mode is com pa ra ble with the ex change in ter ac tion time be tween P* and B A. This al lows for com ple tion of the charge sep a ra tion in con trast to the 130 cm 1 mode for which the in ter sec tion time (~100 fs) is too short for the com plete ET. MATERIALS AND METHODS RCs of Rhodobacter sphaeroides R26 were iso lated as de scribed in Ref. 28, and were pheophytinmodified as de scribed in Ref. 29. The ab sorp tion of the sam ples was ad justed to an op ti cal den sity of 0.5 at 860 nm at 293K (op ti cal path length of 1 mm). The dithionite (5 mm) was added and the sam ples were il lu mi nated by nonfocused light of a fil a ment lamp dur ing ~ 1 min to prereduce the elec tron ac cep tor Q A. All mea sure ments were car ried out at room tem per a ture. For the mea sure ments of dif fer ence ab sorp tion spec tra at dif fer ent femto second (fs) de lays the fs spec trom e ter was used. It is based on a homemade cw modelocked Ti:sap phire la ser (26 fs pulse du ra tion, ~200 mwt out put power, ~100 MHz rep e ti tion rate) pumped by cw ar gon ion la ser (Spec traphysics, USA). Af ter ex pand ing to ps time scale the sin gle pulses were ex tracted by Pockels cell. Then the pulses were am pli fied in an 8pass Ti: sap phire am pli fier pumped by sec ond har monic of nano sec ond homemade YAG:Nd 3+ la ser. The am pli fied ps pulses were com pressed to their ini tial fs du ra tion in a pulse com pres sor. Then the am pli fied fs pulses were fo cused in a wa ter cell to pro duce a con tin uum. Wave lengths shorter than 850 nm were cut off with a RG 850 fil ter (Melles Griot). A small frac tion (~4%) of the con tin uum were used as probe and ref er ence pulses, and a main part of the con tin uum as a pump pulse. The pump and probe pulses prop a gated through de lay line and the sam ple. Then the probe and ref er ence pulses passed through a polychromator con nected to OMA (Oriel, France). The op er at ing fre quency of the spec trom e ter was 1 Hz. Crosscorrelation func tion of the pump and probe pulses showed ~ 30 fs pulse du ra tion. The rel a tive po si tion of the zero time de lay within a nm range was es ti mated to change by less than 30 fs. The de lay be tween pump and probe pulses was changed with an ac cu racy of ~20 fs. The probe pulses were de po lar ized. The dif fer ence (lightminusdark) timeresolved absorbance spec tra were a re sult of av er ag ing of ~50 mea sure ments in the range and ~600 mea sure ments in the range. The am pli tudes of absorbance changes ( A) of the spec tral bands on the broad back ground were mea sured at max i mum. RE SULTS Fig. 1 shows the dif fer ence (lightminusdark) absorb ance spec tra in the range of nm (Fig. 1A) and nm (Fig. 1B) at 293K for pheophytinmodified RCs from Rhodobacter sphaeroides R26 at dif fer ent de lays af ter ex ci ta tion by ~30fs pulses at 870 nm. In agree ment with pre vi ous mea sure ments 1721 the stim u lated emis sion from P * has a time de pend ent po si tion of the max i mum. At 50 fs de lay the absorbance changes due to stim u lated emis sion have a peak near 900 nm (895 nm 20 ). Then the emis sion peak is shifted to 930 nm (see 118fs de lay). Af ter wards the emis sion max i mum shifts back to the blue ap proach ing again the po si tion near 900 nm at 250 fs, etc. In phase with os cil la tions at 930 nm the spec trum of A near 1020 nm at dif fer ent de lays (Fig. 1B) shows the ap pear ance and dis ap pear ance of the 1020nm band of bacteriochlorophyll rad i cal an ion (B A ). Af ter 500 fs de lay the 1020 nm band is in creased con stantly due to ex po nen tial growth of the state P + B A. Fig. 2A shows the ki net ics of A at 1020 nm de rived from the spec tra of A (Fig. 1) for the 1020 nm band on the Fig. 1. Dif fer ence (lightminusdark) absorbance spec tra mea sured at var i ous de lays at 293K in pheophytinmodified Rhodobacter sphaeroides R26 RCs ex cited by 30fs pulses at 870 nm. (A) The spec tra of A of stim u lated emis sion of P* in the nm range. (B) The spec tra of of B A (state P + B A ) in the range. Note the dif fer ence of ver ti cal scales of A and B.

3 Co her ence in Re ac tion Cen ters J. Chin. Chem. Soc., Vol. 47, No. 4A, broad back ground. An os cil la tory part of the ki net ics was ob tained by fit ting the data to oneexponential (3 ps) de cay ki net ics and sub tract ing this ki net ics from ex per i men tal data (Fig. 2B). For com par i son the same was done for the ki net ics at 935 nm (the P* stim u lated emis sion band) as shown in Fig. 2C. The fre quency com po nents of the os cil la tory parts were an a lyzed by Fou rier trans for ma tions (Fig. 3). Os cil la tions seen at 120 and 380 fs (Fig. 2B) make a fre quency around 130 cm 1 (Fig. 3). Fine struc ture in side these os cil la tions pro duces a broad fre quency band in the cm 1 range. The os cil la tion near 120fs de lay is com pletely re vers ible (Fig. 2A and Ref. 24). This is in con trast to fur ther os cil la tions that are de vel oped on a back ground of ex po nen tial growth with the 3ps time con stant. Next os cil la tions ob served at 1 ps, 2 ps and 3 ps (Fig. 2A and B) can be con sid ered as mainly ir re vers ible (~85%) for ma tion of the state P + B A mon i tored by the 1020 nm band mea sure ments. These os cil la tions give a fre quency of 33 cm 1 in Fou rier anal y sis (Fig. 3). Com par i son with the ki net ics of the bleach ing at 800 nm 23 shows that os cil la tions at 120 fs, 380 fs, 1 ps, 2 ps and 3 ps for ap pear ance of the 1020 nm band are in phase with cor re spond ing os cil la tions ob served for bleach ing of the B A band at 800 nm. This shows that these os cil la tions are re lated to the for ma tion of the B A when a ground state ab sorp tion at 800 nm is bleached and a new rad i cal an ion band at 1020 nm ap pears. The Fou rier spec tra for the 1020nm (Fig. 3B) and 800nm (Fig. 3C) bands are es sen tially the same for pheophytinmodified RC. The os cil la tions with fre quen cies around 130 and 33 cm 1 for the 1020 nm band have the same ini tial phases show ing that both modes are cre ated within the first one hun dred fs af ter the ex ci ta tion (Fig. 2B). Time widths of the os cil la tions for the ap pear ance of the 1020 nm band are ~100 fs and ~600 fs around 120 fs and 1 ps de lay, re spec tively. A 9 cm 1 mode seen in the Fou rier spec trum (Fig. 3) should Fig. 2. (A) Ki net ics of at 1020 nm (max i mum of ab sorp tion band of B A ). (B) The os cil la tory part of that ki net ics af ter sub trac tion of a 3ps ex po nen tial growth. (C) Os cil la tory part of ki net ics of A at 935 nm (longwavelength max i mum of stim u lated emis sion from P*). All ki net ics are based on the mea sured spec tra of A at dif fer ent de lays (see M&M and Fig. 1). Fig. 3. The Fou rier trans form spec tra of the os cil la tory parts of the ki net ics of A (taken from Fig. 2) at 935 nm (A), at 1020 nm (B). (C) The Fou rier trans form spec trum of the os cil la tory parts of the ki net ics of A at 805 nm for pheophytinmodified Rhodobacter sphaeroides R26 RCs ex cited by 30fs pulses at 870 nm (data are taken from Ref. 23 and from A.M. Streltsov, S.I.E. Vulto, A.Ya. Shkuropatov, A.J. Hoff, T.J. Aartsma, V.A. Shuvalov, un pub lished re sults).

4 712 J. Chin. Chem. Soc., Vol. 47, No. 4A, 2000 Yakovlev and Shuvalov cor re spond to os cil la tions sep a rated by ~3.7 ps. The os cil la tions at 120 and 380 fs (130 cm 1 mode) for the 1020 nm band are in phase with those for the stim u lated emis sion of P* at 935 nm (Fig. 2B and C and in Ref. 24). The Fou rier anal y sis of the 935 nm and 1020 nm ki net ics dem on strated in Fig 3 shows that the 9 and 130 cm 1 modes are pres ent in both spec tra. The 33 cm 1 mode clearly seen in the spec trum for the 1020 nm band and for 800 nm band (Fig. 3B and C) is al most ab sent in the 930 nm band spec trum (Fig. 3A) in agree ment with pre vi ous mea sure ments. 1721,23 DIS CUS SION The data pre sented here agree in many re spects with fs data de scribed ear lier for the P* stim u lated emis sion, 1721 for the absorbance changes within the B A ab sorp tion band at 800 nm 23 and for the 1020 nm band mea sured at ear lier de lay 24 in R. sphaeroides R26 RCs. The os cil la tions of the bleach ing around 800 nm were ob served in na tive R26 RCs 23 as well as in pheophytinmodified RCs (Ref. 23 and A.M. Streltsov, S.I.E. Vulto, A.Ya. Shkuropatov, A.J. Hoff, T.J. Aartsma, V.A. Shuvalov, un pub lished re sults). It was dem on strated that these two kinds of RCs show es sen tially the same os cil lat ing ki net ics at 890 nm and 805 nm and the same Fou rier trans form spec tra (see also Fig. 3). The com plete anal y sis of fs ki net ics for the 1020 nm band (mon i tor ing the for ma tion of the bacte rio chlorophyll rad i cal an ion B A and the state P + B A ) in com par i son with other data al lows mak ing some con clu sions about a cou pling of the nu clear wavepacket mo tion with a pri mary charge sep a ra tion. The com par i son of the data men tioned above shows that the 130 cm 1 mode seen in the stim u lated emis sion from P* at 930 nm, is in phase with the same mode ob served for the bleach ing at 800 nm 23 and for the for ma tion of the B A band at 1020 nm (Figs. 2 and 3). This proves a con clu sion that when the wavepacket cre ated on the P* po ten tial sur face ap proaches an in ter sec tion with the P + B A sur face, the re vers ible ET be tween P* and B A is ob served for this mode. This in ter sec tion is close to the longwavelength side of the emis sion from P* and is above a bot tom of the P* sur face by ~30 cm 1. This value was found by re fine ment of cal cu la tions pre sented in Ref. 24. They are based on the ra tio of the in ter sec tion time (~100 fs) around 120 fs de lay and a pe riod of the os cil la tion (260 fs) when the en ergy of the wavepacket above the sur face bot tom is known (about 150 cm 1 ). The rea sons for the re vers ible ET ob served for the 130 cm 1 mode is sug gested to be con nected to: i) large dif fer ence be tween broad width (~300 cm 1 ) of the wavepacket and small slit (~30 cm 1 ) be tween two sur faces; ii) long elec tron trans fer time be tween P* and B A (~700 fs) and short in ter sec tion time (~100 fs) ob served near 120 fs de lay. In fact the am pli tude of re vers ible ap pear ance of the band at 1020 nm at 120 fs de lay is con sid ered as a prod uct of a FranckCondon fac tor close to 1 24 and of the elec tron den sity shift from P* to B A for 100 fs at the in ter sec tion. The av er aged elec tron cou pling en ergy (V) of 15 cm cor re sponds to the elec tron trans fer time of 700 fs at the in ter sec tion (cal cu la tions will be pub lished else where) and is larger than the in ter sec tion time by a fac tor of 7. This value is in good agree ment with the am pli tude of A at 1020 nm at 118 fs as com pared with that at 53 ps (1:6.3, see Fig. 1). In con trast to that, the in ter sec tion time for the 33 cm 1 mode (1 ps de lay) is about 600 fs which is close to the ex change in ter ac tion time. It means that al most all elec tron den sity can be trans ferred from P* to B A for this time pe riod. This cor re sponds to the mostly ir re vers ible ET ob served for this mode (Fig. 2). FranckCondon fac tor for this case is prob a bly less than 1 at 293K but can be close to 1 at 5K. It would ac cel er ate ET ex cited by the fspulses at low tem per a ture as ob served ex per i men tally. The 30 3 cm 1 mode ob served in the bleach ing of the B A band at 800 nm 23 is in phase with the 33cm 1 mode ob served for the for ma tion of the 1020 nm band (Fig. 2) since the same phases for the bleach ing at 800 nm and the de vel op ment at 1020 nm are ob served at 1 ps, 2 ps and 3 ps de lays. It means that the lat ter band be longs to the B A and is a re sult of mainly (~85%) ir re vers ible for ma tion of the state P + B A. The 130 and 33 cm 1 modes for the 1020 nm band have the same ini tial phases (Fig. 2B) show ing that both modes are cre ated within the first hun dred fs af ter ex ci ta tion. Both lat ter modes are cou pled dif fer ently (more strong ly for the 130 cm 1 mode) to the ground elec tron tran si tion in P in near in frared as re vealed by hole burn ing at 1.7K. 30 Zerophonon line width is about 2545 cm 1 in open RCs 30,31 (in con trast to find ing of nar row holes by Small group 32 which seem to be re lated to dis torted RCs 33 ). This width cor re sponds to ~150 fs re lax ation time that is much faster than ET at 5K (1.6 ps 14 ). How ever this short re lax ation time (~150 fs) might be re lated to the dephasing pro cess con nected to elec tron ex change in ter ac tion be tween P* and B A that was sug gested ear lier 30 and ob served clearly in the fs os cil la tions of the 1020 nm band (Figs. 13). Fig. 4 shows a sim pli fied scheme of dif fer ent po ten tial en ergy sur faces. The ab sence of the 33cm 1 mode in the stim u lated emis sion of P* at 930 nm (Fig. 2) might be re lated to a rel a tively small dis place ment of the P* po ten tial sur face with re spect to that of the ground state for this mode. Hole burn ing mea sure ments show 30 that Sfactor value for this mode is about 0.2 in agree ment with this sug ges tion and is in con trast to an Sfactor value of about 2 for the 140 cm 1 mode (for Rb.

5 Co her ence in Re ac tion Cen ters J. Chin. Chem. Soc., Vol. 47, No. 4A, sphaeroides). 34 There fore two P* sur faces for the 130 and 33 cm 1 modes have some dis place ment shown in Fig. 4. In spite of that, both sur faces have the in ter sec tions with the P + B A sur face (that might have some dif fer ent modes as well). Since the po si tion of the in ter sec tion for the 130 cm 1 mode with the P + B A sur face is above the bot tom of its sur face by 30 cm 1 (see above) the in ter sec tion is close to zero vi bra tion level (130:2 = 65 cm 1 ). As all modes in the ex cited state have the same po si tion for zero vi bra tion level, the 33 cm 1 mode might have the in ter sec tion with the P + B A sur face close to zero level as well (not shown in Fig. 4). If both 130 and 33 cm 1 sur faces of P* have the in ter sec tions with the same P + B A sur face at points that are close to each other, there is a pos si bil ity to trans fer the vi bra tion from the 130 cm 1 sur face to the 33 cm 1 sur face. This can be fa cil i tated by splittings of the sur faces due to elec tron ex change in ter ac tions at the in ter sec tions. This sug ges tion is con sis tent with the inphase for ma tion of two modes (Fig. 2B). Such a pos si bil ity might have an im por tant role for pri mary ET since the main ab sorp tion band of P is formed by a pro gres sion of the 140 cm 1 mode with Sfactor value close to 2. 30,34 There fore the max i mum of the P ab sorp tion at 870 nm is shifted to the blue with re spect to 00 tran si tion (~905 nm) and cor re sponds to the 02 and 03 tran si tions of the 140 cm 1 mode 34 (which cor re sponds to the 130 cm 1 mode in the fs os cil la tions since the cen ter of the lat ter mode is at 140 cm 1 ). There fore the ex ci ta tion of RCs at 870 nm leads to pop u la tion of the 130 cm 1 mode rather than the 30 cm 1 one. The pop u la tion of the lat ter mode might hap pen via the for mer one. The 17 and 28 cm 1 modes are ob served in mo lec u lar dy nam ics cal cu la tions 35 in volve pro tein move ments that mod u late the po si tion or ori en ta tion of P and B A with re spect to each other. These two modes are close to the 33 cm 1 mode ob served ex per i men tally. These mo lec u lar mo tions can be im por tant for the ef fi ciency of the charge sep a ra tion and of light en ergy con ver sion at pho to syn the sis. AC KNOWL EDG MENTS We thank Dr. A.V. Sharkov for help in con struc tion of fs spec trom e ter and Dr. A. Ya. Shkuropatov and V. A. Shkuropatova for pre par ing the sam ples. Sup port by the Rus sian Fun da men tal Re search Foun da tion (grant N ), «Uni ver sities of Rus sia Fun da men tal Re searches» and NWO ( Hol land) grants is grate fully ac knowl edged. Re ceived De cem ber 31, Key Words Re ac tion cen ter; Elec tron trans fer; Wavepacket; Pri mary elec tron do nor; Pri mary elec tron ac cep tor. Fig. 4. Ten ta tive en ergy level scheme for states PB, P*B (for 33 cm 1 and 130 cm 1 modes) and P + B A. The po ten tial en ergy curves for these states are shown as a onedimensional crosssection of the po ten tial en ergy sur faces. The wavepacket is cre ated on the P*B po ten tial en ergy sur face for the 130cm 1 mode un der ex ci ta tion by 30fs pulses at 870 nm. Then this wavepacket moves on the P* po ten tial en ergy sur face and ap proaches the in ter sec tion with the P + B A sur face. At this point the re vers ible ET be tween P* and B A takes place. At the in ter sec tion of the 130 and 33 cm 1 modes near the in ter sec tion with the P + B A sur face the trans fer of the wavepacket from the 130 to 33 cm 1 mode prob a bly oc curs. Mostly ir re vers ible ET is ob served when wavepacket moves on the 33 cm 1 sur face and ap proaches the in ter sec tion with the P + B A sur face. See text for other de tails. REF ER ENCES 1. Shuvalov, V. A. Pri mary Light En ergy Con ver sion at Pho to syn the sis, Nauka (in Rus sian), Mos cow, Hoff, A. J.; Deisenhofer, J. Phys. Rep. 1997, 287, Shuvalov, V. A.; Klevanik, A. V.; Sharkov, A. V.; Matveetz, Yu. A.; Krukov, P. G. FEBS Lett. 1978, 91, Shuvalov, V. A.; Duysens, L. N. M. Proc. Natl. Acad. Sci. USA 1986, 83, Chekalin, S. N.; Matveetz, Yu. A.; Shkuropatov, A. Ya.; Shuvalov, V. A.; Yartzev, A. FEBS Lett. 1987, 216, Shkuropatov, A. Ya.; Shuvalov, V. A. FEBS Lett. 1993, 322, Arlt, T.; Schmidt, S.; Lauterwasser, C.; Meyer, M.; Scheer,

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