Nickel toxicity inhibits abundance and activity of cyanobacteria and Fe(III)-reducers in low-phosphate Archean oceans

Banded iron formations (BIFs) are iron (Fe)- and silica (SiO2)-rich marine chemical sediments that formed between 3.8 and 1.85 Ga, recording early ocean geochemistry and the rise of oxygen during the Great Oxidation Event (GOE, ∼2.45 Ga). Cyanobacterial oxygen (O2) production led to iron mineral precipitation, with subsequent Fe(III) reduction by dissimilatory Fe(III)-reducing bacteria (DIRB). However, the remobilization and roles of essential dissolved nutrients (phosphate, PO43−) and micronutrients that also function as potential toxins (nickel, Ni), remain unclear. We conducted batch experiments with two consecutive Fe(II) oxidation and Fe(III) reduction cycles with the marine cyanobacterium Synechococcus sp. PCC7002 and the DIRB Shewanella colwelliana under simulated Archean ocean conditions (0.5 mM Fe2+ aq, 0.67 mM SiO2 aq) with varying concentrations of PO43− (3.67 and 367 μM) and Ni (0.4, 4 and 40 μM). High Ni (4, 40 μM) inhibited growth, except at high PO43− (365 μM) with 4 μM Ni, whereas total cell counts temporarily increased from 2 × 107 cells/mL at day 60 to 6 × 107 cells/mL at day 135, followed by a decline to 4 × 107 cells/mL by day 195. Low PO43− concentrations (3.67 μM) limited growth except at low Ni (0.4 μM), rising from 2 × 107 cells/mL on day 60 to 8 × 107 cells/mL by day 82. These results suggest that first, the combined stress of high Ni toxicity and low PO43− availability likely constrained cyanobacterial proliferation, possibly delaying the onset of the GOE. Second, DIRB could remobilize PO43− during Fe(III) reduction, thereby sustaining microbial activity and maintaining iron cycling in the early ocean.