A Dual Role for Ca2+ in Expanding the Spectral Diversity and Stability of Light-Harvesting 1 Reaction Center Photocomplexes of Purple Phototrophic Bacteria

Abstract

The light-harvesting 1 reaction center (LH1-RC) complex in the purple sulfur bacterium Thiorhodovibrio ( Trv.) strain 970 cells exhibits its LH1 Q _y transition at 973 nm, the lowest-energy Q _y absorption among purple bacteria containing bacteriochlorophyll a (BChl a). Here we characterize the origin of this extremely red-shifted Q _y transition. Growth of Trv. strain 970 did not occur in cultures free of Ca²⁺, and elemental analysis of Ca²⁺-grown cells confirmed that purified Trv. strain 970 LH1-RC complexes contained Ca²⁺. The LH1 Q _y band of Trv. strain 970 was blue-shifted from 959 to 875 nm upon Ca²⁺ depletion, but the original spectral properties were restored upon Ca²⁺ reconstitution, which also occurs with the thermophilic purple bacterium Thermochromatium ( Tch.) tepidum. The amino acid sequences of the LH1 α- and β-polypeptides from Trv. strain 970 closely resemble those of Tch. tepidum; however, Ca²⁺ binding in the Trv. strain 970 LH1-RC occurred more selectively than in Tch. tepidum LH1-RC and with a reduced affinity. Ultraviolet resonance Raman analysis indicated that the number of hydrogen-bonding interactions between BChl a and LH1 proteins of Trv. strain 970 was significantly greater than for Tch. tepidum and that Ca²⁺ was indispensable for maintaining these bonds. Furthermore, perfusion-induced Fourier transform infrared analyses detected Ca²⁺-induced conformational changes in the binding site closely related to the unique spectral properties of Trv. strain 970. Collectively, our results reveal an ecological strategy employed by Trv. strain 970 of integrating Ca²⁺ into its LH1-RC complex to extend its light-harvesting capacity to regions of the near-infrared spectrum unused by other purple bacteria.