An early diverging SQR enzyme in Antarctic Gloeobacterales indicates sulfide tolerance in thylakoid-lacking cyanobacteria

Oxygenic photosynthesis first appeared in cyanobacteria approximately 3.3 Ga and ultimately drove the Great Oxidation Event around 2.4 Ga. However, early cyanobacteria likely evolved in euxinic oceans enriched in sulfide, a compound that both inhibits PSII and can serve as an electron donor through anoxygenic photosynthesis pathways. Sulfur is also integrated into cyanobacterial photosynthetic membranes through sulfoquinovosyldiacylglycerol (SQDG), a sulfur-containing lipid associated with thylakoid function. Yet SQDG appears to be absent from Gloeobacterales, the earliest-branching cyanobacterial lineage, which also lacks thylakoids.
Here, we report the presence of sulfide-quinone reductase (SQR), an enzyme involved in sulfide oxidation, in Antarctic representatives of Gloeobacterales (Hambücken et al., 2026a). Phylogenetic analyses consistently place these Gloeobacterales SQR sequences at the base of the cyanobacterial SQR clade, suggesting that they may represent an ancient acquisition predating the multiple lateral transfers previously reported for this gene within Cyanobacteria. Searches in metagenomic datasets further indicate that closely related SQR sequences are restricted to cold environments, pointing to Antarctic lakes as possible refugia for ancient cyanobacterial traits. In parallel, we investigated the taxonomic distribution and synteny of three genes linked to SQDG biosynthesis: sqdB, sqdX, and sll1499, the gene encoding FdGOGAT. Our results suggest that FdGOGAT was vertically transmitted across Cyanobacteria, whereas sqdB and sqdX were likely horizontally transferred to an ancestor of thylakoid-bearing cyanobacteria after the divergence of Gloeobacterales but before the divergence of Thermostichales. Together, these findings suggest that some early-diverging cyanobacteria may have retained the capacity for sulfide-dependent anoxygenic photosynthesis, while SQDG biosynthesis was acquired only after the divergence of Gloeobacterales.