Cryo-EM structure of a Ca2+-bound photosynthetic LH1-RC complex containing multiple \u03b1\u03b2-polypeptides

Kazutoshi Tani,Zheng-Yu Wang-Otomo,Ryo Kanno,Yukihiro Kimura,Akira Mizoguchi,Bruno M Humbel,Long-Jiang Yu,Malgorzata Hall,Jörg Overmann,Yuki Makino,Mizuki Takenouchi,Michie Imanishi,Michael T Madigan

doi:10.1038/s41467-020-18748-3

Abstract

The light-harvesting-reaction center complex (LH1-RC) from the purple phototrophic bacterium Thiorhodovibrio strain 970 exhibits an LH1 absorption maximum at 960 nm, the most red-shifted absorption for any bacteriochlorophyll (BChl) a-containing species. Here we present a cryo-EM structure of the strain 970 LH1-RC complex at 2.82 Å resolution. The LH1 forms a closed ring structure composed of sixteen pairs of the αβ-polypeptides. Sixteen Ca ions are present in the LH1 C-terminal domain and are coordinated by residues from the αβ-polypeptides that are hydrogen-bonded to BChl a. The Ca2+-facilitated hydrogen-bonding network forms the structural basis of the unusual LH1 redshift. The structure also revealed the arrangement of multiple forms of α- and β-polypeptides in an individual LH1 ring. Such organization indicates a mechanism of interplay between the expression and assembly of the LH1 complex that is regulated through interactions with the RC subunits inside.

Highlights

The light-harvesting-reaction center complex (LH1-RC) from the purple phototrophic bacterium Thiorhodovibrio strain 970 exhibits an LH1 absorption maximum at 960 nm, the most red-shifted absorption for any bacteriochlorophyll (BChl) a-containing species
The LH1 subunits of strain 970 are uniformly distributed around the RC forming a closed, slightly elliptical double cylinder composed of 16 pairs of helical α(inner)β(outer)-polypeptides, 32 BChls a, 16 carotenoids (3,4,3′,4′-tetrahydrospirilloxanthin)[16], and 16 Ca ions (Fig. 1 and Supplementary Figs. 5 and 6)
The RC is accommodated in the LH1 ellipsoid and fits the shape of the inner LH1 α-ring with the L- and M-subunits in close proximity to the LH1 α2- and α4-polypeptides, respectively, in the transmembrane region (Fig. 1b, Supplementary Table 2, and Supplementary Fig. 5)

Summary

Introduction

The light-harvesting-reaction center complex (LH1-RC) from the purple phototrophic bacterium Thiorhodovibrio strain 970 exhibits an LH1 absorption maximum at 960 nm, the most red-shifted absorption for any bacteriochlorophyll (BChl) a-containing species. The LH1-α (inner) and β(outer) rings form a tight network connected by Ca2+ This leads to a more rigid structure for the entire LH1 complex and highly restricts molecular motions around the BChl a-binding domain causing inhomogeneous narrowing in the spectroscopy[14,15]. As for the thermophilic Tch. tepidum, calcium ions were responsible for this ultra-redshift; removal of Ca2+ resulted in a blue-shift of the LH1-Qy to 875 nm, whereas the subsequent addition of Ca2+ restored 960-nm absorbance[16] This process required Ca2+ and was freely reversible, the structural basis behind these Ca2+-induced spectral changes remained unsolved. Elucidating the structural basis for this ultra-redshift of the special pair would reveal how RCs have evolved to coordinate absorbance with their LH1 partner in order to maintain an appropriate energy gap for energy transfer

Methods

Results

Conclusion