Impact of biomineralization on the preservation of microorganisms during fossilization: An experimental perspective

The biogenicity of fossil microbial biomorphs is often debated because their morphologies are poorly informative and the chemical, structural and isotopic signatures of putative biogenic organic molecules have been altered during their incorporation into the sediments and the geological history of the host rock. Here, we investigated the effect of encrustation by biominerals on the morphological and chemical degradation of Escherichia coli cells during experimental thermal treatments. Non-calcified E. coli cells and E. coli cells encrusted by calcium phosphates were exposed to heating under an Argon atmosphere at two different temperatures (300 °C, 600 °C) for 20 h. Two additional experiments were performed on non-calcified E. coli cells at 300 °C for 2 h and 100 h to discuss the influence of experiment duration. Organic residues of all experiments were characterized at a multiple length scale using a combination of scanning electron microscopy, transmission electron microscopy, Raman microspectroscopy, electron paramagnetic resonance (EPR) spectroscopy, Fourier transform infrared (FT-IR) spectroscopy and X-ray absorption near edge structure spectroscopy (XANES) at the carbon K edge. In the absence of encrusting biominerals, the morphological structure of the organic residues of E. coli cells was completely lost after heating at 300 or 600 °C, even after short (2 h long) heating experiments. The content of aromatic functional groups of the organic residues of non-calcified E. coli cells increased during heat-treatment at 600 °C for 20 h while the amide functional groups were lost, as indicated by FT-IR spectroscopy. Consistently, the EPR spectrum of these organic residues indicated important transformation. As a comparison, this spectrum appeared similar to EPR spectra of ancient organic carbons such as carbons from the Apex chert (ca. 3460 Myr), indicating a similar concentration of aromatic moieties. In contrast, calcified E. coli exposed to the same conditions showed only limited morphological alteration as observed by electron microscopy as well as lower chemical transformation as detected by FT-IR and EPR spectroscopies. Despite the difficulties to relate experimental conditions directly to geological conditions, these experiments evidence the influence of cell encrustation by minerals on their chemical and morphological preservation potential during fossilization processes.