Black Sea picocyanobacteria exploit ancestral traits for energy and chlorophyll production in dark anoxia

Abstract Picocyanobacteria, typically associated with oxygenated waters, thrive also in oxygen minimum zones (OMZs) and anoxic environments. The extent to which retention of diverse ancestral anaerobic traits facilitate their metabolic flexibility with regards to transitioning between oxic and anoxic habitats is poorly understood. Here, using Black Sea Cyanobium (BSA11S), we performed 13C-glucose and 15N-ammonium incubations coupled with nanoscale ion mass spectrometry (NanoSIMS) and transcriptomics to characterize the growth mode and gene expression during transition from light-to-dark and oxic-to-anoxic conditions. Incubated picocyanobacteria assimilate 13C-glucose and ammonium under anoxic-dark conditions, grow slowly without light, and retain the capability to synthesize photosynthetic pigments. They moderately upregulate genes responsible for chlorophyll-a/bilin biosynthesis, uptake of C sources, debranching of glycogen storage, and the pentose phosphate pathway for ATP, NADH, and NADPH production, as well as genes involved in NAD+ regeneration, including proton-reduction hydrogen-metabolism coupled with lactic acid fermentation. Our results support the remarkable versatility, plasticity, and potential for mixotrophy in photoautotrophs that allow them to dominate diverse aquatic systems worldwide.