From Cytoplasmic Membrane to Thylakoids: Evolution of Membrane Biogenesis and Photosystem II assembly in early-diverging Cyanobacteria

Thylakoid membranes (TM) in cyanobacteria and chloroplasts host the light-dependent reactions of oxygenic photosynthesis which involve a linear electron transfer (LET) chain composed of multi-subunit complexes, including Photosystem II (PSII). Gloeobacterales, the earliest-diverging cyanobacterial lineage, lack TM and perform photosynthesis within specialized regions of the cytoplasmic membrane (CM), thereby representing an ancestral state with respect to other cyanobacteria, all equipped with TM and termed Phycobacteria. The emergence of TM, which increased the membrane surface available for oxygenic photosynthesis, was a key innovation that likely contributed to the Great Oxidation Event. This evolutionary transition involved the formation of a distinct membrane compartment, followed by the relocation of LET components from the CM to TM. Here, we present a phylogenomic analysis identifying three candidate proteins associated with membrane trafficking that may contribute to TM biogenesis, including the SPFH family member Slr1106, which we show was acquired via lateral gene transfer from Patescibacteria. Moreover, evolutionary analysis of 37 PSII assembly factors reveals key modifications in late-stage PSII assembly, particularly in manganese homeostasis, and highlights structural changes in the YidC translocase, which may have facilitated the relocation of LET components from the CM to TM. Altogether, these results bring new insights into the molecular innovations that led to the emergence of TM.