Metallomics in deep time and the influence of ocean chemistry on the metabolic landscapes of Earth’s earliest ecosystems

Modern biological dependency on trace elements is proposed to be a consequence of their enrichment in the habitats of early life together with Earth’s evolving physicochemical conditions; the resulting metallic biological complement is termed the metallome. Herein, we detail a protocol for describing metallomes in deep time, with applications to the earliest fossil record. Our approach extends the metallome record by more than 3 Ga and provides a novel, non-destructive method of estimating biogenicity in the absence of cellular preservation. Using microbeam particle-induced X-ray emission (µPIXE), we spatially quantify transition metals and metalloids within organic material from 3.33 billion-year-old cherts of the Barberton greenstone belt, and demonstrate that elements key to anaerobic prokaryotic molecular nanomachines, including Fe, V, Ni, As and Co, are enriched within carbonaceous material. Moreover, Mo and Zn, incorporated into enzymes only after the Great Oxygenation Event, are absent. Transmission electron microscopy demonstrates that metal enrichments do not arise from accumulation in nanomineral phases and thus unambiguously reflect the primary composition of the carbonaceous material. This carbonaceous material also has δ13C between 0.03‰ and –41.3‰, dominantly –11.5‰ to –21.0‰, consistent with biological fractionation and mostly within a restricted range inconsistent with abiotic processes. Considering spatially quantified trace metal enrichments and negative δ13C fractionations together, we propose that, although lacking cellular preservation, this organic material has biological origins, and its precursor metabolism may be estimated from its fossilised “palaeo-metallome”. Enriched Fe, V, Ni and Co suggests that this kerogen reflects the remnants of a lithotrophic or organotrophic consortium cycling methane or nitrogen. Palaeo-metallome compositions could be used to deduce the metabolic networks of Earth’s earliest ecosystems and, potentially, as a biosignature for the evaluation of the origin of preserved organic materials found on Mars.