The Thermal-Stable LH1-RC Complex of a Hot Spring Purple Bacterium Powers Photosynthesis with Extremely Low-Energy Near-Infrared Light.

Abstract

Blastochloris (Blc.) tepida is a hot spring purple nonsulfur phototrophic bacterium that contains bacteriochlorophyll (BChl) b. Here, we present a 2.21 Å cryo-EM structure of the thermostable light-harvesting 1-reaction center (LH1-RC) complex from Blc. tepida. The LH1 ring comprises 16 circularly arranged αβγ-subunits plus one αβ-subunit that surround the RC complex composed of C-, H-, L-, and M-subunits. In a comparative study, the Blc. tepida LH1-RC showed numerous electrostatic and hydrophobic interactions both within the LH1 complex itself and between the LH1 and the RC complexes that are absent from the LH1-RC complex of its mesophilic counterpart, Blc. viridis. These additional interactions result in a tightly packed LH1-RC architecture with a reduced accessible surface area per volume that enhances the thermal stability of the Blc. tepida complex and allows the light reactions of photosynthesis to proceed at hot spring temperatures. Moreover, based on high-resolution structural information combined with spectroscopic evidence, the unique photosynthetic property of the Blc. tepida LH1-RC─absorption of energy-poor near-infrared light beyond 1000 nm─can be attributed to strong hydrogen-bonding interactions between the C3-acetyl C═O of the LH1 BChl b and two LH1 α-Trp residues, structural rigidity of the LH1, and the enhanced exciton coupling of the LH1 BChls of this thermophile.