Native architecture and acclimation of photosynthetic membranes in a fast-growing cyanobacterium

Abstract

Efficient solar energy conversion is ensured by the organization, physical association, and physiological coordination of various protein complexes in photosynthetic membranes. Here, we visualize the native architecture and interactions of photosynthetic complexes within the thylakoid membranes from a fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 (Syn2973) using high-resolution atomic force microscopy (AFM). In the Syn2973 thylakoid membranes, both photosystem I (PSI)-enriched domains and crystalline photosystem II (PSII) dimer arrays were observed, providing favorable membrane environments for photosynthetic electron transport. The high light (HL)-adapted thylakoid membranes accommodated a large amount of PSI complexes, without the incorporation of iron-stress-induced protein A (IsiA) assemblies and formation of IsiA−PSI supercomplexes. In the iron deficiency (Fe−)-treated thylakoid membranes, in contrast, IsiA proteins densely associated with PSI, forming the IsiA−PSI supercomplexes with varying assembly structures. Moreover, type-I NADH dehydrogenase-like complexes (NDH-1) were upregulated under the HL and Fe− conditions and established close association with PSI complexes to facilitate cyclic electron transport. Our study provides insight into the structural heterogeneity and plasticity of the photosynthetic apparatus in the context of their native membranes in Syn2973 under environmental stress. Advanced understanding of the photosynthetic membrane organization and adaptation will provide a framework for uncovering the molecular mechanisms of efficient light harvesting and energy conversion.

In situstructural determination of cyanobacterial phycobilisome-PSII supercomplex by STAgSPA strategy

“…This situation is significantly different from that of red algae, where two PSI subcomplexes are connected to two ends of PSII array 20 , suggesting the interaction fashion of PSII with PSI is distinguished between cyanobacteria and red algae. This is likely reasonable because AFM observation for thylakoid membranes of cyanobacterium Synechococcus elongatus UTEX 2973 corroborated that PSII arrays are interspersed with PSI, which exhibits diverse interaction patterns and inhomogeneous arrangement in native thylakoid membranes 26,27 . We also identified 180 phycocyanobilin (PCB) for each PBS, and 70 chlorophylls, 4 heme molecules, 18 carotenoids and 56 lipids for each PSII dimer.…”

“…The copyright holder for this this version posted December 18, 2023. ; https://doi.org/10.1101/2023.12.17.572042 doi: bioRxiv preprint are interspersed with PSI, which exhibits diverse interaction patterns and inhomogeneous arrangement in native thylakoid membranes 26,27 . We also identified 180 phycocyanobilin (PCB) for each PBS, and 70 chlorophylls, 4 heme molecules, 18 carotenoids and 56 lipids for each PSII dimer.…”

The Ycf48 accessory factor occupies the site of the oxygen-evolving manganese cluster during photosystem II biogenesis

“…The RCII/PSI complex therefore appears to be artefactual, although we cannot totally exclude the possibility that the complex might reflect interactions at an early stage of PSII assembly within specialised but still ill-defined biogenesis regions of the membrane 22 . Recent work has also suggested that trimeric PSI complexes might exist in opposite orientations in the thylakoid membrane 23 .

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The Ycf48 accessory factor occupies the site of the oxygen-evolving manganese cluster during photosystem II biogenesis

“…The RCII/PSI complex therefore appears to be artefactual, although we cannot totally exclude the possibility that the complex might reflect interactions at an early stage of PSII assembly within specialised but still ill-defined biogenesis regions of the membrane 22 . Recent work has also suggested that trimeric PSI complexes might exist in opposite orientations in the thylakoid membrane 23 .…”