Hambucken, L. | bioRxiv Science

bioRxiv2025

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

O_LIThylakoid membranes (TM) in cyanobacteria and chloroplasts host the light-dependent reactions of oxygenic photosynthesis. Gloeobacterales, the earliest-diverging cyanobacterial lineage, lack TM and perform photosynthesis in the cytoplasmic membrane, representing an ancestral state relative to other cyanobacteria (Phycobacteria). This study investigates the evolutionary origin of TM. C_LIO_LIPhylogenomic analyses were performed across a phylogenetically diverse set of cyanobacteria, including extensive representation of basal lineages (Gloeobacterales, Thermostichales, Gloeomargaritales and Pseudanabaenales), as well as micro- and macrocyanobacteria, using orthologous proteins involved in membrane dynamics and Photosystem II (PSII) assembly, together with structural modelling using AlphaFold3. C_LIO_LIWe identified two candidate proteins associated with membrane trafficking that may contribute to TM biogenesis, including the SPFH family member Slr1106, proposed to have been acquired by lateral gene transfer. Analysis of 36 PSII assembly factors revealed modifications in late-stage assembly, notably in manganese homeostasis. Structural changes in the YidC translocase may have facilitated relocation of linear electron transfer components from the cytoplasmic membrane to TM. C_LIO_LIAltogether, these phylogenetic and functional prediction analyses provide new insight into the molecular innovations that led to TM emergence, including membrane trafficking systems, PSII assembly changes, and protein targeting adaptations. C_LI

evolutionary biology↗

bioRxiv2025

Early-Diverging SQR Enzyme in Antarctic Gloeobacterales Indicates Sulfide Tolerance in Thylakoid-Lacking Cyanobacteria

Oxygenic photosynthesis, which converts solar energy into carbohydrates via a linear electron transport chain and two photosystems (PSII and PSI), first appeared in cyanobacteria approximately 3.3 Ga and drove the Great Oxidation Event around 2.4 Ga. During this period, euxinic conditions--characterized by sulfidic, anoxic oceans--posed a metabolic challenge to cyanobacteria, as sulfide inhibits PSII, the reaction center responsible for water splitting. Here, we report the presence of an early-diverging form of the sulfide quinone reductase (SQR) enzyme in Antarctic representatives of Gloeobacterales, the earliest-branching cyanobacterial lineage lacking thylakoids. Phylogenetic analyses reveal that these SQR sequences are the earliest-diverging cyanobacterial SQR known to date, predating the multiple lateral gene transfer events previously observed in the phylum. Additional searches in metagenomic datasets indicate that such sequences are restricted to cold environments. Our findings unveil possible adaptive strategies of early cyanobacteria to cope with sulfidic stress and point to Antarctic lakes as preserved natural laboratories for investigating cyanobacterial diversification and the evolution of oxygenic photosynthesis under euxinic conditions. Impact StatementThe diversification of cyanobacteria during and after the Great Oxidation Event occurred in early Proterozoic oceans that were partially euxinic (anoxic and sulfidic) a condition generally considered incompatible with oxygenic photosynthesis due to photosystem II inhibition. The presence of a sulfide quinone reductase in an Antarctic early diverging cyanobacterium lacking thylakoids gives credit on an ancestral evolutionary stage where oxygenic and anoxygenic traits coexisted within cyanobacteria. The occurrence of these organisms in Antarctic lakes under euxinic conditions offers a natural laboratory for studying the physiology and adaptation of the first oxygenic photosynthetic organisms.

evolutionary biology↗