105

ORIGIN AND EVOLUTION OF PHOTOSYNTHETIC REACTION CENTERS

John M. Olson* and Beverly K. Pierson** *Inst. of Biochemistry, Odense University,

DK-5230 Odense M, Denmark

**Biology Dept., University of Puget Sound, Tacoma, WA 984]6, USA

The prototype reaction center (RC) may have used protoporphyrin-IX associated with small peptides to create and maintain one or more ion gradients across the primitive cell membrane. This process was both primitive and ancient and may have been significant in driving the uptake of essential nutrients.

Protoporphyrin-IX in ether has a strong absorption band at 408 nm. When similar porphyrins (uroporphyrin, coproporphyrin, and hemato- porphyrin) are illuminated with white or blue (410 nm) light in the presence of ethylene diamine tetraacetic acid (EDTA), H_ and oxidized

EDTA are produced in the presence of a platinum catalys~ (Mercer- Smith and Mauzerall, 1984). In this type of photochemistry the primary charge separation leaves the originally excited porphyrin molecule in the reduced state, whereas in contemporary RCs the primary charge separation leaves the originally excited chlorophyll molecule in the oxidized state. In ancient RCs containing porphyrins but no chlorophyll, the primary electron transfer would have required a donor molecule to react with the excited porphyrin. The reduced porphyrin might then have donated an electron to a quinone-like acceptor and/or a low potential Fe-S center. A phototrophic organism using protoporphyrin would probably have contained a large number of RCs with no accessory light- harvesting molecules, because energy transfer between pigment molecules would have been very poor due to the weak absorption band at 633 nm

(in ether). The introduction of Mg into protoporphyrin presumably would have

changed the character of the primary charge separation to the "chlorophyll" type. With the introduction of ring V in protochlorophyll ~, the red absorption band (622 nm in ether) was doubled or tripled in oscillator strength, and the rate of energy transfer was also doubled or tripled compared to the cases of protoporphyrin-IX or Mg-proto- porphyrin-IX. With the advent of chlorophyll (Chl) ~ the red absorption band (662 nm in ether) was about quadrupled in strength, and the rate of energy transfer was also quadrupled in comparison to the situation in protochlorophyll ~. Furthermore Chl ~ could effectively use both red

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PHOTOSYNTHETIC REACTION CENTERS

and blue light for photochemistry. The precursor of all contemporary RCs is thought to have continued

Chl a molecules as both primary electron donor and initial electron acceptor, and a very low potential quinone-like molecule and an Fe-S center as secondary acceptors as in the RC of Heliobacterium chlorum (Brok et al; 1986). This RC is thought to have been part of a membrane- bound electron transport chain containing ferredoxin, a quinone pool, and cytochromes. This cyclic electron transport system probably functioned initially in photoassimilation, but was easily adapted to CO fixation using H 2 and H2S about 3.5 Ga ago (Olson and Pierson, 1926).

A second reaction center (RC-2) evolved from the first type (RC-I) between 3.5 and 2.5 Ga ago in response to the competition for reductants

for CO 2 fixation. Organisms containing RC-2 in series with RC-I would have been able to use poor reducing agents such as the abundant aqueous ferrous ion in place of H and H S

Between 3.0 and 2.5 ~ 2 " a ago organisms containing Chl a in both RC-I and RC-2 added a water-splitting enzyme to RC-2 in order to use H20 in place of hydrated ferrous ion as alectron donor for autotrophic photosynthesis.

Mercer-Smith, J. A. and Mauzerall, D. C.: 1984, Photochem. Photobiol. 3_9_9, 397.

Brok, M., Vasmel, H., Horikx, J. T. G. and Hoff, A. J.: 1986, FEBS Lett. 194, 322.

Olson, J. M. and Pierson, B. K.: 1986, Photosyn. Res. (I April).

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