Ancestral cyanobacteria are assumed to be prominent primary producers after the Great Oxidation Event [≈2.4 to 2.0 billion years (Ga) ago], but carbon isotope fractionation by extant marine cyanobacteria (α-cyanobacteria) is inconsistent with isotopic records of carbon fixation by primary producers in the mid-Proterozoic eon (1.8 to 1.0 Ga ago). To resolve this disagreement, we quantified carbon isotope fractionation by a wild-type planktic β-cyanobacterium (Synechococcus sp. PCC 7002), an engineered Proterozoic analog lacking a CO2-concentrating mechanism, and cyanobacterial mats. At mid-Proterozoic pH and pCO2 values, carbon isotope fractionation by the wild-type β-cyanobacterium is fully consistent with the Proterozoic carbon isotope record, suggesting that cyanobacteria with CO2-concentrating mechanisms were apparently the major primary producers in the pelagic Proterozoic ocean, despite atmospheric CO2 levels up to 100 times modern. The selectively permeable microcompartments central to cyanobacterial CO2-concentrating mechanisms (“carboxysomes”) likely emerged to shield rubisco from O2 during the Great Oxidation Event.

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