The Black Sea is the largest meromictic sea with a reservoir of anoxic water extending from 100 to 1000 m depth. These deeper layers are characterised by a poorly understood fluorescence signal called "deep red fluorescence", a chlorophyll a- (Chl a) like signal found in deep dark oceanic waters. In two cruises, we repeatedly found up to 103 cells ml-1 of picocyanobacteria at 750 m depth in these waters and isolated two phycoerythrin-rich Synechococcus sp. strains (BS55D and BS56D). Tests on BS56D revealed its high adaptability, involving the accumulation of Chl a in anoxic/dark conditions and its capacity to photosynthesise when re-exposed to light. Whole-genome sequencing of the two strains showed the presence of genes that confirms the putative ability of our strains to survive in harsh mesopelagic environments. This discovery provides new evidence to support early speculations associating the "deep red fluorescence" signal to viable picocyanobacteria populations in the deep oxygen-depleted oceans, suggesting a reconsideration of the ecological role of a viable stock of Synechococcus in dark deep waters.

Department of Aquatic Microbial Ecology Institute of Hydrobiology Biology Certer CAS Ceske Budejovice Czech Republic

Evolutionary Genomics Group Departamento de Producción Vegetal y Microbiología Universidad Miguel Hernández San Juan de Alicante Spain

Institute of Oceanology Fridtjof Nansen Bulgarian Academy of Sciences Varna Bulgaria

Limnological Station Institute of Plant and Microbial Biology University of Zurich Kilchberg Switzerland

Museum für Naturkunde Berlin Germany

National Research Council CNR IRSA Microbial Ecology Group Verbania Italy

Sofia University St Kliment Ohridski Faculty of Physics Sofia Bulgaria

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Uncovering the genomic basis of symbiotic interactions and niche adaptations in freshwater picocyanobacteria

Genomic Comparison and Spatial Distribution of Different Synechococcus Phylotypes in the Black Sea