Jérémie Beghin

1.1-billion-year-old porphyrins establish a marine ecosystem dominated by bacterial primary producers

Significance The oceans of Earth’s middle age, 1.8–0.8 billion years ago, were devoid of animal-like life. According to one hypothesis, the emergence of large, active organisms was restrained by the limited supply of large food particles such as algae. Through the discovery of molecular fossils of the photopigment chlorophyll in 1.1-billion-year-old marine sedimentary rocks, we were able to quantify the abundance of different phototrophs. The nitrogen isotopic values of the fossil pigments showed that the oceans were dominated by cyanobacteria, while larger planktonic algae were scarce. This supports the hypothesis that small cells at the base of the food chain limited the flow of energy to higher trophic levels, potentially retarding the emergence of large and complex life. The average cell size of marine phytoplankton is critical for the flow of energy and nutrients from the base of the food web to higher trophic levels. Thus, the evolutionary succession of primary producers through Earth’s history is important for our understanding of the radiation of modern protists ∼800 million years ago and the emergence of eumetazoan animals ∼200 million years later. Currently, it is difficult to establish connections between primary production and the proliferation of large and complex organisms because the mid-Proterozoic (∼1,800–800 million years ago) rock record is nearly devoid of recognizable phytoplankton fossils. We report the discovery of intact porphyrins, the molecular fossils of chlorophylls, from 1,100-million-year-old marine black shales of the Taoudeni Basin (Mauritania), 600 million years older than previous findings. The porphyrin nitrogen isotopes (δ15Npor = 5.6–10.2‰) are heavier than in younger sedimentary sequences, and the isotopic offset between sedimentary bulk nitrogen and porphyrins (εpor = −5.1 to −0.5‰) points to cyanobacteria as dominant primary producers. Based on fossil carotenoids, anoxygenic green (Chlorobiacea) and purple sulfur bacteria (Chromatiaceae) also contributed to photosynthate. The low εpor values, in combination with a lack of diagnostic eukaryotic steranes in the time interval of 1,600–1,000 million years ago, demonstrate that algae played an insignificant role in mid-Proterozoic oceans. The paucity of algae and the small cell size of bacterial phytoplankton may have curtailed the flow of energy to higher trophic levels, potentially contributing to a diminished evolutionary pace toward complex eukaryotic ecosystems and large and active organisms.