MODEL PHOTOAUTOTROPHS ISOLATED FROM A PROTEROZOIC OCEAN ANALOG

Little Salt Spring (Sarasota County, FL, USA) is a sinkhole with groundwater vents at ~77 m depth. The entire water column experiences weakly sulfidic (~ 50 μM) conditions seasonally, resulting in a system poised between oxic and sulfidic conditions. Red pinnacle mats occupy the sediment-water interface in the sunlit upper basin of the sinkhole, and is comprised of Cyanobacteria, Chlorobi, and sulfate-reducing clades of Deltaproteobacteria. The red pinnacle mats bloom in the anoxic basin of the sinkhole and receive low levels of light to support photosynthesis but the mats are capable of light-dependent primary productivity as evidenced by ¹³C-bicarbonate photoassimilation. We also observed ¹³C-bicarbonate photoassimilation in the presence of DCMU, an inhibitor of electron transfer to Photosystem II. Our results indicate that the mats carry out significant light-driven primary production in the absence of oxygen production—a mechanism that may have delayed the oxygenation of the Earth's oceans and atmosphere during the Proterozoic Eon. Furthermore, our observations of the production of 2-methyl hopanoids by cyanobacteria under conditions of low oxygen and low light are consistent with the recovery of these structures from ancient black shales as well as their paucity in modern marine environments.

Characterization of the dominant cyanobacterium and green sulfur bacterium is consistent with observations of oxygenic and anoxygenic photosynthesis in situ—both organisms perform anoxygenic photosynthesis under conditions of very low light. Despite the energetic favorably of oxygenic photosynthesis, this activity in the cyanobacterium isolate is inhibited by the presence of sulfide and under optimal light conditions, rates of anoxygenic photosynthesis by the cyanobacterium are nearly double that of oxygenic photosynthesis. The green sulfur bacterium is tolerant of oxygen and has a very low affinity for sulfide. Collectively, isotopes signatures, biosignatures, in situ data and pure culture studies have the potential to inform our understanding of biogeochemical cycling in the low oxygen Archean and Proterozoic.