Colors in the dark: Ancestral trade-offs in picocyanobacteria from the Early Ocean analogue

Geochemical evidence combined with application of ecophysiological and molecular tools in an Ancient Ocean analogue can allow us to resolve the mechanism behind the delay in planetary oxygentation, so-called Boring Billion. In the dark, anoxic Black Sea waters, picocyanobacteria maintain photosynthetic capacity during fermentation. This trait, likely had been evolving during rapid switches between oxygenic and anoxygenic metabolism and was implied to support growth. To test the hypothesis that endemic picocyanobacteria generate energy, synthetize photosynthetic pigments and multiply during fermentation under anoxic-dark conditions, we incubated a Black Sea isolate in the presence of 13C-glucose and 15N-ammonium. We used flow cytometry, nanoscale ion mass spectrometry (NanoSims), genomics, transcriptomics, chlorophyll survey and Fourier Transformed Ion Cyclotron Resonance Mass Spectrometry (FT-IRMS) to characterize growth mode, pigmentation, gene expression and molecular composition of exudates under the transition from light-to-dark and oxic-to-anoxic conditions. Chlorophyll biosynthesis genes and lactate dehydrogenases were overexpressed by coloured cells showing 13C enrichment in the dark and under anoxia. Transcriptomics in light/dark and oxic/anoxic conditions revealed the ability to grow in anoxic mesopelagial by carrying out fermentation, hydrogen metabolism and maintaining high levels of photosynthetic pigments. While pico-cyanobacteria multiply slowly in the dark they retain expensive photosynthetic capacity. This metabolic trade-off likely allowed ancestral cyanobacteria to survive in a highly changeable habitat where light was scarce and reductants abundant but could have also slowed their proliferation in the ocean and thus delay planetary oxygenation.