Nickel limited methanogens shaped Precambrian climate

High nickel (Ni) availability during the Archean enabled the proliferation of Ni-dependent methanogens1,2, whose methane (CH4) emissions sustained a strong greenhouse effect that offset the reduced luminosity of the young Sun3. By the end of the Archean eon, a severe decline in Ni availability—a phenomenon known as the Nickel Famine (~2.7-2.5 Ga)—triggered a drop in methane production, contributing to global cooling, and a subsequent rise in atmospheric oxygen (O2)4,5. Intriguingly, despite Earth’s permanent decline in bioavailable Ni6,7, methanogens utilizing organic energy source such as acetate and methyl compounds remain pivotal agents in modern methane emissions and global carbon cycling8,9. Here, we demonstrated that organotrophic methanogens are inherently more tolerant to Ni scarcity, with less inhibitory impact on growth rates and methane production under Ni limitation. We attribute this resilience to a systematic metabolism retooling—replacement of ancestral [NiFe]-hydrogenase-based energy system with an electron transport chain (ETC), which underpins the advent of organotrophic methanogens. Divergence time estimations reveal that the emergence of organotrophic methanogenesis aligned with the Nickel Famine. This temporal correlation suggests that the profound metabolic innovation was triggered by the protracted decline in environmental Ni bioavailability. It marks a key evolutionary adaptation to a major geochemical shift, revealing how microbial metabolic flexibility regulates planetary processes, enabled methanogens to endure sustained Ni limitation, and explains the ~1.5 Gyr delay in further global glaciations.