An 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 a sulfide-quinone reductase (SQR) enzyme in Antarctic representatives of Gloeobacterales, the earliest-branching cyanobacterial lineage. Phylogenetic analyses consistently position these SQR sequences at the base of the cyanobacterial clade, likely predating the multiple lateral transfers reported for this gene in the phylum. Additional searches in metagenomic data sets 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.IMPORTANCEThe 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 early diverging cyanobacterium lacking thylakoids, isolated from Antarctica, suggests that oxygenic and anoxygenic photosynthesis coexisted early on in cyanobacterial evolution. 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.