Abstract
Cyanobacterial mats were hotspots of biogeochemical cycling during the Precambrian. However, mechanisms that controlled O2 release by these ecosystems are poorly understood. In an analog to Proterozoic coastal ecosystems, the Frasassi sulfidic springs mats, we studied the regulation of oxygenic and sulfide-driven anoxygenic photosynthesis (OP and AP) in versatile cyanobacteria, and interactions with sulfur reducing bacteria (SRB). Using microsensors and stable isotope probing we found that dissolved organic carbon (DOC) released by OP fuels sulfide production, likely by a specialized SRB population. Increased sulfide fluxes were only stimulated after the cyanobacteria switched from AP to OP. O2 production triggered migration of large sulfur-oxidizing bacteria from the surface to underneath the cyanobacterial layer. The resultant sulfide shield tempered AP and allowed OP to occur for a longer duration over a diel cycle. The lack of cyanobacterial DOC supply to SRB during AP therefore maximized O2 export. This mechanism is unique to benthic ecosystems because transitions between metabolisms occur on the same time scale as solute transport to functionally distinct layers, with the rearrangement of the system by migration of microorganisms exaggerating the effect. Overall, cyanobacterial versatility disrupts the synergistic relationship between sulfide production and AP, and thus enhances diel O2 production.
Highlights
The evolution of oxygenic photosynthesis (OP) by cyanobacteria was one of the major transformative events in the history of life and is responsible for the bounty of life on Supplementary information The online version of this article contains supplementary material, which is available to authorized users.Earth as we know it today
Cyanobacterial and gammaproteobacterial 16S rRNA sequences dominated throughout all samples taken directly in the spring and during the incubations, which was consistent with highly abundant filamentous cyanobacteria and large sulfur bacteria observed by microscopy (Fig. 1)
Transitions between anoxygenic and oxygenic photosynthesis depend on irradiance In the dark and after adjustment of pH and O2 and total sulfide (Stot) concentration in the water column approximately to in situ conditions (Table S3), the mat surface was covered with sulfur-oxidizing bacteria (SOB) as deduced from the whitish appearance of the mat
Summary
O2 is the most favorable electron acceptor used for respiration by myriads of organisms, and its accumulation in the atmosphere considerably changed the surface chemistry of the Earth. There are, many open questions concerning the history of O2 on Earth. The long lag in the rise of atmospheric O2 levels after the first appearance of free oxygen signals in the geological record still defy holistic mechanistic explanation [1]. One of the most mysterious episodes in Earth’s history
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