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

Abstract 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 Statement The 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. Competing Interest Statement The authors have declared no competing interest.