Thylakoid membrane lipid sulfoquinovosyl-diacylglycerol (SQDG) is required for full functioning of photosystem II in Thermosynechococcus elongatus

Abstract

Sulfoquinovosyl-diacylglycerol (SQDG) is one of the four lipids present in the thylakoid membranes. Depletion of SQDG causes different degrees of effects on photosynthetic growth and activities in different organisms. Four SQDG molecules bind to each monomer of photosystem II (PSII), but their role in PSII function has not been characterized in detail, and no PSII structure without SQDG has been reported. We analyzed the activities of PSII from an SQDG-deficient mutant of the cyanobacterium by various spectroscopic methods, which showed that depletion of SQDG partially impaired the PSII activity by impairing secondary quinone (Q) exchange at the acceptor site. We further solved the crystal structure of the PSII dimer from the SQDG deletion mutant at 2.1 Å resolution and found that all of the four SQDG-binding sites were occupied by other lipids, most likely PG molecules. Replacement of SQDG at a site near the head of Q provides a possible explanation for the Q impairment. The replacement of two SQDGs located at the monomer-monomer interface by other lipids decreased the stability of the PSII dimer, resulting in an increase in the amount of PSII monomer in the mutant. The present results thus suggest that although SQDG binding in all of the PSII-binding sites is necessary to fully maintain the activity and stability of PSII, replacement of SQDG by other lipids can partially compensate for their functions.

Structural insights into NDH-1 mediated cyclic electron transfer

“…5). Mass spectrometric analysis showed that the observed molecular weights of the co-purified lipids are identical to the calculated values of these thylakoid membrane-specific lipids 30 , unequivocally confirming their chemical identities ( Supplementary Fig. 8c).…”

“…8c). Given that we purified the endogenous NDH-1LΔV complex from T. elongatus thylakoid membranes with a mild detergent (digitonin), the lipids we found in the NDH-1L structure are very likely physiologically relevant and reflect their actual binding positions in NDH-1L in vivo, suggesting that lipids in NDH-1L may play important roles as lipids found in other photosynthesis complexes of cyanobacteria 30 .…”

Structure of plant photosystem I−light harvesting complex I supercomplex at 2.4 Å resolution

“…The other important difference is the lipid molecules found in the present structure and those of the previous structures. Lipids play important roles in the assembly and functions of membrane‐protein complexes (Hasan et al, 2011; Mizusawa and Wada, 2012; Kansy et al, 2014; Nakajima et al, 2018), but are difficult to identify in the X‐ray crystallography due to the weak electron density of their acyl chains. We identified five new lipids in the present structure compared with the previous 2.8 Å structure (4XK8) (Qin et al, 2015); among them, four are located in the Lhca 1‐4 dimer.…”

In situ cryo-ET structure of phycobilisome–photosystem II supercomplex from red alga

“…PSII is a multi-pigment transmembrane protein complex involved in converting light energy into electrochemical potential energy ( Adachi et al, 2008 ). The X-ray crystal structures of PSII from red alga Cyanidium caldarium ( Ago et al, 2016 ), cyanobacterium Thermosynechococcus elongatus ( Nakajima et al, 2018 ), and the cryo-EM structure of PSII from green alga Chlamydomonas reihardtii ( Sheng et al, 2019 ), the marine diatom Chaetoceros gracilis ( Pi et al, 2019 ), and the higher plants Arabidopsis thaliana ( van Bezouwen et al, 2017 ), Spinacia oleracea ( Wei et al, 2016 ), and Pisum sativum ( Su et al, 2017 ) have revealed the structural basis of energy transfer, electron transfer, and photoprotection within the photosystem. The main subunits of PSII include the reaction center D1, D2 protein, and chlorophyll-a binding proteins, CP43 and CP47.…”