The drilling of the Rio Tinto basement has provided evidence of an underground microbial community primarily sustained by the Fe and S metabolism through the biooxidation of pyrite orebodies. Although the gossan is the microbial activity product, which dates back to the Oligocene (25 Ma), no molecular evidence of such activity in the past has been reported yet. A Time of Flight Secondary Ion Mass Spectrometry (ToF-SIMS) molecular analysis of a subsurface sample in the Peña de Hierro basement has provided novel data of the ancient underground microbial community. It shows that the microbial remains are preserved in a mineral matrix composed of laminated Fe-oxysulfates and K- and Na-bearing sulfates alternating with secondary silica. In such a mineral substrate, the biomolecule traces are found in five different microstructure associations, (1) <15 micron-sized nodular microstructures composed of PO_n(2≤n≤4)⁻, (2) <30 micron-size micronodules containing fatty acids, acylglycerides, and alkanol chains, (3) 200-micron thick layer with N-bearing adducts, and sphingolipid and/or peptide traces. It suggests the mineralization of at least five microbial preserved entities with different metabolic capabilities, including: (1) Acidiphilium/Tessaracoccus-like phosphate mineralizers, (2) microbial patches preserving phosphate-free acylglycerides bacteria, (3) nitrogen oxidizing bacteria (e.g., Acidovorax sp.), (4) traces of heterotrophic ammonifying bacteria, and (5) sphingolipid bearing bacteria (e.g., Sphingomonadales, and δ-Proteobacteria) and/or mineralized biofilms. The primary biooxidation process acted as a preservation mechanism to release the inorganic ions that ultimately mineralized the microbial structures.

Microbial mats represented the earliest complex ecosystems on Earth, since fossil mineralized examples (i.e., microbialites) date back to the Archean Eon. Some microbialites contain putative remains of organic matter (OM), however the processes and pathways that lead to the preservation of OM within microbialite minerals are still poorly understood. Here, a multidisciplinary study is presented (including petrographic, mineralogical and organic geochemical analyses), focusing on a modern calcifying mat from a hypersaline lake in the Kiritimati atoll (Central Pacific). The results show that this mat has a complex history, with two main growth phases under hypersaline conditions, separated by an interruption caused by desiccation and/or freshening of the lake. The mineral precipitates of the mat are predominantly aragonitic and two contrasting precipitation modes are observed: the main growth phases of the mat were characterized by the slow formation of irregular micritic particles with micropeloidal textures and subspherical particles, linked to the degradation of the exopolymer (EPS) matrix of the mat; whereas the interruption period was characterized by the rapid development of a thin but laterally continuous crust composed of superposed fibrous aragonite botryoids that entombed their contemporaneous benthic microbial community. These two precipitation modes triggered different preservation pathways for the OM of the mat as the thin crust shows a particular lipid biomarker signature, different from that of other layers and the relatively rapid precipitation of the crust protecting the underlying lipids from degradation, causing them to show a preservation equivalent to that of a modern active microbial community, despite them being >1100 years old. Equivalent thin mineral crusts occur in other microbialite examples and, thus, this study highlights them as excellent targets for the search of well-preserved biomarker signatures in fossil microbialites. Nevertheless, the results of this work warn for extreme caution when interpreting complex microbialite biomarker signatures, advising combined petrographic, mineralogical and geochemical investigations for the different microbialite layers and mineral microfabrics.