Crystallographic models of photosystem I (PS I) highlight a symmetrical arrangement of the electron transfer cofactors which are organized in two parallel branches (A, B) relative to a pseudo-C-2 symmetry axis that is perpendicular to the membrane plane. Here, we explore the electron transfer pathways of PS I in whole cells of the deuterated green alga Chlamydomonas reinhardtii using high-time-resolution electron paramagnetic resonance (EPR) at cryogenic temperatures. Particular emphasis is given to quantum oscillations detectable in the tertiary radical pairs P(700)(+)A(1A)(-) and P(700)(+)A(1B)(-) of the electron transfer chain. Results are presented first for the deuterated site-directed mutant PsaA-M684H in which electron transfer beyond the primary electron acceptor A(0A) on the PsaA branch of electron transfer is impaired. Analysis of the quantum oscillations, observed in a two-dimensional Q-band (34 GHz) EPR experiment, provides the geometry of the B-side radical pair. The orientation of the g tensor of P-700(+) in an external reference system is adapted from a time-resolved multifrequency EPR study of deuterated and N-15-substituted cyanobacteria (Link, G.; Berthold, T.; Bechtold, M.; Weidner, J.-U.; Ohmes, E.; Tang, J.; Poluektov, O.; Utschig, L.; Schlesselman, S. L.; Thurnauer, M. C.; Kothe, G. J. Am. Chem, Soc. 2001, 123, 4211-4222). Thus, we obtain the three-dimensional structure of the B-side radical pair following photoexcitation of PS I in its native membrane. The new structure describes the position and orientation of the reduced B-side quinone A(1B)(-) on a nanosecond time scale after light-induced charge separation. Furthermore, we present results for deuterated wild-type cells of C. reinhardtii demonstrating that both radical Pairs P(700)(+)A(1A)(-) and P(700)(+)A(1B)(-) participate in the electron transfer process according to a mole ratio of 0.71/0.29 in favor of P(700)(+)A(1A)(-). A detailed comparison reveals different orientations of A(1A)(-) and A(1B)(-) in their respective binding sites such that formation of a strong hydrogen bond from A(1)(-) to the protein backbone is possible only in the case of A(1A)(-). We suggest that this is relevant to the rates of forward electron transfer from A(1A)(-) or A(1B)(-) to the iron-sulfur center F-x, which differ by a factor of 10. Thus, the present study sheds new light on the orientation of the phylloquinone acceptors in their binding pockets in PS I and the effect this has on function.