Metabolic versatility in a modern lineage of cyanobacteria from terrestrial hot springs

Abstract

The extent of oxygenated environments on the early Earth was much lower than today, and cyanobacteria were critical players in Earth's shift from widespread anoxia to oxygenated surface environments. Extant cyanobacteria that aggregate into cones, tufts and ridges are used to understand the long record of photosynthesis and microbe-mineral interactions during times when oxygen was much lower, i.e., the Archean and the Proterozoic. To better understand the metabolic versatility and physiological properties of these organisms, we examined publicly available genomes of cyanobacteria from modern terrestrial hydrothermal systems and a newly sequenced genome of a cyanobacterium isolated from conical and ridged microbialites that grow in occasionally sulfidic hydrothermal springs in Yellowstone National Park, USA. Phylogenomic analyses reveal that cyanobacteria from globally distributed terrestrial and shallow marine hydrothermal systems form a monophyletic clade within the Cyanobacteria phylum. Comparative genomics of this clade reveals the genetic capacity for oxygenic photosynthesis that uses photosystems I and II, and anoxygenic photosynthesis that uses a putative sulfide quinone reductase to oxidize sulfide and bypass photosystem II. Surprisingly large proportions of the newly sequenced genome from Yellowstone National Park are also dedicated to secondary metabolite production (15.1–15.6%), of which ∼6% can be attributed to antibiotic production and resistance genes. All this may be advantageous to benthic, mat-forming photosynthesizers that have to compete for light and nutrients in sporadically or permanently sulfidic environments, and may have also improved the tolerance of ancient counterparts of these cyanobacteria to sulfidic conditions in benthic communities that colonized the coastal margins in the Archean and the Proterozoic.