Exploring Thylakoid Emergence: 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, notably Photosystem II (PSII), the D1-containing water-splitting complex. Gloeobacterales, the earliest-diverging cyanobacterial lineage, lack TM and perform photosynthesis within specialized regions of the cytoplasmic membrane (CM). This organization likely reflects an ancestral state that predates the emergence of TM, in contrast to all other cyanobacteria—collectively known as Phycobacteria—which possess TM. The emergence of TM conceptually involves two processes, the formation of a distinct membrane compartment and the relocation of LET components from the CM to TM, a transition that likely increased photosynthetic capacity and oxygen production, potentially contributing to the rise of atmospheric oxygen during the Great Oxidation Event.
Here, we present a phylogenomic analysis identifying two candidate proteins associated with membrane trafficking that may contribute to TM biogenesis and emergence, including the SPFH family member Slr1106, which we show was acquired via lateral gene transfer. Moreover, evolutionary analysis of 36 PSII assembly factors indicates key modifications in late-stage PSII assembly, notably in manganese homeostasis. We further highlight structural changes in the early-acting YidC translocase that may have facilitated the relocation of LET components from the CM to TM.