Niche expansion for phototrophic sulfur bacteria at the Proterozoic-Phanerozoic transition

Fossilized carotenoid hydrocarbons provide a window into the physiology and biochemistry of ancient microbial phototrophic communities for which only a sparse and incomplete fossil record exists. However, accurate interpretation of carotenoid-derived biomarkers requires detailed knowledge of the carotenoid inven-tories of contemporary phototrophs and their physiologies. Here we report two distinct patterns of fossilized C-40 diaromatic carot-enoids. Phanerozoic marine settings show distributions of diaro-matic hydrocarbons dominated by isorenieratane, a biomarker derived from low-light-adapted phototrophic green sulfur bacte-ria. In contrast, isorenieratane is only a minor constituent within Neoproterozoic marine sediments and Phanerozoic lacustrine pale-oenvironments, for which the major compounds detected are renierapurpurane and renieratane, together with some novel C-39 and C-38 carotenoid degradation products. This latter pattern can be traced to cyanobacteria as shown by analyses of cultured taxa and laboratory simulations of sedimentary diagenesis. The cyano-bacterial carotenoid synechoxanthin, and its immediate biosyn-thetic precursors, contain thermally labile, aromatic carboxylic-acid functional groups, which upon hydrogenation and mild heating yield mixtures of products that closely resemble those found in the Proterozoic fossil record. The Neoproterozoic-Phanerozoic transition in fossil carotenoid patterns likely reflects a step change in the surface sulfur inventory that afforded opportunities for the expansion of phototropic sulfur bacteria in marine ecosystems. Furthermore, this expansion might have also coincided with a major change in physiology. One possibility is that the green sulfur bacteria developed the capacity to oxidize sulfide fully to sulfate, an in-novation which would have significantly increased their capacity for photosynthetic carbon fixation.