Molecular Basis for the Photosynthetic Primary Process

Abstract

In this paper, the molecular details for the primary reaction in photosynthesis are deduced from several recent critical experimental observations. A symmetrical structure is proposed for the basic unit of the reaction center in plant photosynthesis. A mathematical consequence of the symmetrical arrangement is the creation of an anomalously long-lived trap state, which makes possible the summation of a reaction-center triplet excitation and an antenna chlorophyll singlet excitation to bring the photoactive chlorophylls to a charge-transfer state prior to entering into a primary photochemical reaction.It has long been recognized that certain chlorophyll (Chl)-a molecules in plants and photosynthetic bacteria are capable of performing highly efficient photochemical work under the illumination of relatively low-energy photons in the near infrared. No parallel situation exists in chemistry. Chlorophyll-a molecules by themselves are not photochemically activated by visible or infrared photons.In existing theories (1-3), the possible involvement of the excited singlet and triplet eigenstates of the Chl-a molecule in the primary photochemical reactions has been considered.In a recent paper (4), I suggested a basic mechanism for the primary reaction in photosynthesis. Through interactions between the lowest-lying triplet state of the reaction-center chlorophylls and the first excited singlet state of the antenna chlorophylls, absorbed light quanta are upconverted to a higher-lying charge-transfer state. In this paper, the molecular details of the energy-upconversion reaction are described in terms of experimental observations and first principles. Nature of the photoactive charge-transfer stateIn seeking the most probable configuration for the reactioncenter chlorophylls, we take into cognizance: (i) the recent finding (5-10) that the primary photooxidation product of in vivo photosynthesis contains a special pair of Chl molecules over which the spin density is equivalently distributed and (ii) in vitro mixtures of Chl and H20 give rise to photoactive 1: 1 Chl-H20 adducts (10). We propose an interesting symmetrical (C2) structure (see Fig; 1) in which the two parallel porphyrin rings of the Chl molecules are complementarily held in position by two H20 molecules, each being involved in a hydrogen bond to the carbonyl of the ring V carbomethoxy group of one Chl molecule and an oxygen coordination bond to the magnesium atom of the second Chl molecule. This structure is a modification of the original Katz model (10) in which the two chlorophyll molecules are asymmetrically Abbreviation: Chl, chlorophyll. linked by a single H20 molecule with one chlorophyll acting as an electron donor and the second an acceptor. The symmetry of the present model, which appears to be consistent with the observation of the equivalent spin distribution in the photooxidized special pair, suggests a number of theoretical possibilities. Upon light excitation, for example, two equivalent tautomeric forms of the postulated charge-transfer...

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