Optimization and evolution of light harvesting in photosynthesis: the role of antenna chlorophyll conserved between photosystem II and photosystem I

Abstract

The efficiency of oxygenic photosynthesis depends on the presence of core antenna chlorophyll closely associated with the photochemical reaction centers of both photosystem II (PSII) and photosystem I (PSI). Although the number and overall arrangement of these chlorophylls in PSII and PSI differ, structural comparison reveals a cluster of 26 conserved chlorophylls in nearly identical positions and orientations. To explore the role of these conserved chlorophylls within PSII and PSI we studied the influence of their orientation on the efficiency of photochemistry in computer simulations. We found that the native orientations of the conserved chlorophylls were not optimal for light harvesting in either photosystem. However, PSII and PSI each contain two highly orientationally optimized antenna chlorophylls, located close to their respective reaction centers, in positions unique to each photosystem. In both photosystems the orientation of these optimized bridging chlorophylls had a much larger impact on photochemical efficiency than the orientation of any of the conserved chlorophylls. The differential optimization of antenna chlorophyll is discussed in the context of competing selection pressures for the evolution of light harvesting in photosynthesis.

Figure 1.

Comparison of PSI and PSII Structures. The top panel is a side-on view from within the plane of the thylakoid membrane. The bottom panel is a view from the lumenal side. The individual domains of PSII (CP43, CP47, and D1/D2) are overlapped with the PSI structure as described in the text. Chlorophylls of the RC core domains of PSII (PSI) are shown in red (pink). Antenna chlorophylls of PSII (PSI) are shown in green (gray). Antenna chlorophylls that are conserved in both photosystems are shown with bold lines. Chlorophylls unique to one photosystem are shown with thin lines. The most important optimized connecting chlorophylls of PSII (PSI) are shown in yellow (orange).

Figure 2.

Histograms of the Quantum Yield Distributions Computed for Model Antenna Systems of PSII and PSI. Inserts show the structure of the respective models. Arrows indicate the location of the quantum yield calculated with native chlorophyll orientations as found in the x-ray structures. Areas under the shadowed/black parts of the histograms represent the number of alternative pigment orientations with yields higher/lower than the native x-ray structure, respectively. Orientations of all antenna chlorophylls except Chl_Z/D in the case of PSII and chlorophylls A39 and B40 in the case of PSI were varied. (A) PSI including only the 26 chlorophylls conserved between PSI and PSII. (B) PSII including 26 chlorophylls conserved between PSI and PSII. (C) PSII including all antenna chlorophylls. (D) PSI including all antenna chlorophylls.

Figure 3.

Histograms of the Quantum Yield Distributions Computed for Models of the Antenna Systems. (A) Green sulfur bacteria C. lumicola. (B) Heliobacteria H. mobilis. The orientations of all antenna chlorophyll included in each model were varied. Inserts show the structure of the respective models. Arrows indicate the location of the quantum yield calculated with native chlorophyll orientations as found in the x-ray structures. Areas under the shadowed/black parts of the histograms represent the number of alternative pigment orientations with yields higher/lower than the native x-ray structure, respectively.

Figure 4.

Dependence of the Difference (ΔΦ) between the Best and the Worst Quantum Yield Achieved by Reorientation of Individual Chlorophylls on Their Distance to the Closest Pigment in the RC Core. (A) PSII. (B) PSI.

Figure 5.

Plots of a Measure of Orientational Optimality (P) versus a Measure of the Potential of the Orientation of Each Individual Chlorophyll to Affect Quantum Yield (ΔΦ) in PSII and PSI. P is the probability of occurrence of orientations that result in a higher quantum yield than that calculated for the native orientation. Thus, the smaller the value of P the more highly optimized the native orientation. In both (A) and (B), solid upright triangles represent the 26 chlorophylls conserved between PSII and PSI and open circles the chlorophylls unique to each photosystem.

Figure 6.

Histograms of the Quantum Yield Distributions Computed for the Complete Antenna Systems. (A) PSII. (B) PSI. In the PSII model the orientations of all antenna chlorophylls except the two highly optimized chlorophylls (C14 and C31) and the two Chl_Z/D were varied. In the PSI model the orientations of all antenna chlorophylls except the two highly optimized chlorophylls (B24 and A26) and chlorophylls A39 and B40 were varied. Inserts show the structure of the respective models. Arrows indicate the location of the quantum yield calculated with native chlorophyll orientations as found in the x-ray structures. Areas under the shadowed/black parts of the histograms represent the number of alternative pigment orientations with yields higher/lower than the native x-ray structure, respectively.