Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

Abstract BackgroundCyanobacteria are photosynthetic ancient bacteria ubiquitous in terrestrial and aquatic environments. Even though they carry a photosynthesis apparatus they are known to survive in dark environments. Cyanophages are viruses that infect and lyse cyanobacterial cells, adding bioavailable carbon and nutrients into the environment. Here we present the first study that investigate the metabolic spectrum of cyanobacteria in dark and anoxic environments, as well as their associated cyanophages. We sampled surface sediments during April 2018 located along a water depth gradient of 60–210 m—representing oxic, hypoxic and anoxic conditions—in the largest dead zone in the world (Baltic Sea). We combined metagenomic and RNA-seq to investigate cyanobacterial taxonomy, activity and their associated cyanophages.ResultsCyanobacteria were detected at all four stations (n = 3 per station) along the sampled gradient, including the anoxic sediment. Top genera in the anoxic sediment included Anabaena (19% RNA data), Synechococcus (16%), and Cyanobium (5%). The mRNA data showed that cyanobacteria were surviving through i) anaerobic carbon metabolism indicated by glycolysis plus fatty acid biosynthesis, and ii) nitrogen (N2) fixation (likely by heterocystous Anabaena). Interestingly, in the mRNA data cyanobacteria were also transcribing photosynthesis, phytochromes, and gas vesicle genes. Cyanophages were detected at all stations, and compared to the oxic sediment had a different beta diversity in the hypoxic-anoxic sediment. Moreover, our results show that these cyanophages can infect cyanobacteria affecting the photosystem and phosphate regulation.ConclusionsCyanobacteria were found to transcribe genes for photosynthesis, phytochromes, and gas vesicles and this suggests that cyanobacteria try to ascend to the surface waters. The difference in cyanophage beta diversity between oxic and hypoxic-anoxic sediment suggests that anaerobic cyanobacteria select for specific cyanophages. Cyanobacteria are known to fuel oxygen depleted benthic ecosystems with phosphorous (so called internal loading), and our study suggests that cyanophage-controlled lysis of cyanobacteria likely provides a source of nitrogen. Our results suggest that cyanobacteria might also provide nutrients via N2 fixation and viral lysis in dark and anoxic environments.