Vladkova Radka
Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., Bl. 21, 1113 Sofia, Bulgaria.
Membranes (Basel). 2025 May 8;15(5):143. doi: 10.3390/membranes15050143.
The rapid regulatory mechanism of light-induced state transitions (STs) in oxygenic photosynthesis is particularly appealing for membrane-based applications. This interest stems from the unique ability of the thylakoid membrane protein cytochrome (cyt) to increase or decrease its hydrophobic thickness (d) in parallel with the reduction or oxidation of the PQ pool induced by changes in light quality. This property appears to be the long-sought biophysical driver behind the reorganizations of membrane proteins during STs. This study decisively advances the hydrophobic mismatch (HMM) model for cyt-driven STs by thoroughly analyzing thirteen X-ray crystal and eight cryo-electron microscopy cyt structures. It uncovers the lipid nanoenvironments that cyt, with different hydrophobic thicknesses, selectively attracts. Under optimal, stationary conditions for photosynthesis in low light, when there is hydrophobic matching between the hydrophobic thicknesses of cyt d and that of the bulk thylakoid lipid phase d, d = d, cyt predominantly binds to anionic lipids-several phosphatidylglycerol (PG) molecules and one sulfoquinovosyldiacylglycerol (SQDG) molecule. Upon the induction of the transition to State 2, when d increases and induces a positive HMM (d > d), the neutral, non-bilayer-forming lipid monogalactosyldiacylglycerol (MGDG) replaces some of the bound PGs. Upon the induction of the transition to State 1, when d decreases and induces a negative HMM (d < d), PGs and SQDG detach from their binding sites, and two neutral, bilayer-forming lipids such as digalactosyldiacylglycerol (DGDG) occupy two sites. Additionally, this research uncovers two lipid-mediated signaling pathways from Chl to the center of flexibility, the Phe/Tyr124 residue-one of which involves β-carotene. This study identifies two novel types of lipid raft-like nanodomains that are devoid of typical components, such as sphingomyelin and cholesterol. These findings firmly validate the HMM model and underscore the STs as the first recognized functional process that fully utilizes the unique and evolutionarily conserved composition of just four thylakoid lipid classes. This research contributes to our understanding of membrane dynamics in general and STs in particular. It introduces a novel and simple approach for reversible protein reorganization driven purely by biophysical mechanisms, with promising implications for various membrane-based applications.
在产氧光合作用中，光诱导状态转换（STs）的快速调节机制对于基于膜的应用特别有吸引力。这种兴趣源于类囊体膜蛋白 Cyt 独特的能力，即随着光质变化诱导的 PQ 池的还原或氧化，其疏水厚度（d）会相应增加或减少。这一特性似乎是 STs 期间膜蛋白重组背后长期寻求的生物物理驱动因素。本研究通过全面分析 13 个 X 射线晶体结构和 8 个冷冻电子显微镜 Cyt 结构，决定性地推进了 Cyt 驱动的 STs 的疏水不匹配（HMM）模型。它揭示了具有不同疏水厚度的 Cyt 选择性吸引的脂质纳米环境。在低光下光合作用的最佳稳定条件下，当 Cyt 的疏水厚度 d 与类囊体脂质主体相的疏水厚度 d 之间存在疏水匹配时，即 d = d，Cyt 主要与阴离子脂质结合——几个磷脂酰甘油（PG）分子和一个磺基喹喔啉二酰基甘油（SQDG）分子。在诱导向状态 2 转变时，当 d 增加并诱导正的 HMM（d > d）时，中性的、非双层形成脂质单半乳糖基二酰基甘油（MGDG）取代了一些结合的 PGs。在诱导向状态 1 转变时，当 d 减小并诱导负的 HMM（d < d）时，PGs 和 SQDG 从它们的结合位点脱离，两种中性的、形成双层的脂质如二半乳糖基二酰基甘油（DGDG）占据两个位点。此外，这项研究还揭示了从叶绿素到灵活性中心（Phe/Tyr124 残基）的两条脂质介导的信号通路——其中一条涉及β-胡萝卜素。本研究确定了两种新型的类脂筏纳米结构域，它们缺乏典型成分，如鞘磷脂和胆固醇。这些发现有力地验证了 HMM 模型，并强调 STs 是第一个被认可的功能过程，它充分利用了仅四种类囊体脂质类别的独特且进化保守的组成。这项研究有助于我们总体上理解膜动力学，特别是 STs。它引入了一种新颖且简单的方法，用于纯粹由生物物理机制驱动的可逆蛋白质重组，对各种基于膜的应用具有潜在的意义。
