Experimental maturation of Archaea encrusted by Fe-phosphates

Abstract

Burial is generally detrimental to the preservation of biological signals. It has often been assumed that (bio)mineral-encrusted microorganisms are more resistant to burial-induced degradation than non-encrusted ones over geological timescales. For the present study, we submitted Sulfolobus acidocaldarius experimentally encrusted by amorphous Fe phosphates to constrained temperature conditions (150 °C) under pressure for 1 to 5 days, thereby simulating burial-induced processes. We document the molecular and mineralogical evolution of these assemblages down to the sub-micrometer scale using X-ray diffraction, scanning and transmission electron microscopies and synchrotron-based X-ray absorption near edge structure spectroscopy at the carbon K-edge. The present results demonstrate that the presence of Fe-phosphates enhances the chemical degradation of microbial organic matter. While Fe-phosphates remained amorphous in abiotic controls, crystalline lipscombite (Fe^II_xFe^III_3-x(PO₄)₂(OH)_3-x) entrapping organic matter formed in the presence of S. acidocaldarius cells. Lipscombite textures (framboidal vs. bipyramidal) appeared only controlled by the initial level of encrustation of the cells, suggesting that the initial organic matter to mineral ratio influences the competition between nucleation and crystal growth. Altogether these results highlight the important interplay between minerals and organic matter during fossilization, which should be taken into account when interpreting the fossil record.

Figure 1

Evolution of non-encrusted and encrusted S. acidocaldarius cells upon heating at 150 °C for 1 to 5 days. TEM images of thin sections of the starting materials (before heating, first row) and SEM images of the heated samples. Thin arrows point out non mineralized vesicles (G) and patches of organic matter (K). Thick arrows point out pores at the surface of the framboids (G,H). Inset in panel H shows a detail of a partly filled hole.

Figure 2

SEM images of abiotic controls (Fe phosphate precipitates) before heating (A) and after heating at 150 °C for 5 days (B).

Figure 3

XRD analyses of abiotic controls and S. acidocaldarius samples (mineralized for 6 h or 24 h) and heated for 1 day or 5 days in close system. Non labeled (hkl) planes are those of lipscombite. The (200) plane of lipscombite overlaps with the (104) plane of siderite.

Figure 4

Normalized C K-edge XANES spectra of non mineralized S. acidolcadarius cells and cells mineralized for 6 or 24 h and heated for 1 or 5 days at 150 °C.

Figure 5

TEM analysis of a FIB section through a framboidal mineral from S. acidocaldarius mineralized for 6 h and heated for 1 day at 150 °C in close system. STEM (A) and TEM (B–E) images of the section. (E) close up of the carbon-rich area / mineral interface in (D), with corresponding FFT, showing that the carbon-rich region is amorphous, whereas the mineral part corresponds to lipscombite <−211> zone axis. (F) EDX map of the cell-like structure in (C) and corresponding EDX spectra (G,H). (H) overlay of the EDX spectra shown in (G), normalized to the Fe L ray. Colours of the spectra correspond to regions of interest of the same colour in (F). Arrowheads point out cell-like structures.

Figure 6

TEM analysis of a FIB section through a framboidal mineral from S. acidocaldarius mineralized for 6 h and heated for 5 days at 150 °C in close system. STEM (A) and TEM (B,C) images of the section. FFT corresponding to different domains are consistent with aggregates of lipscombite nanocrystals with different crystallographical orientations. (D–F) EDX analysis of the central part of the FIB section (STEM image, EDX map and EDX spectra). Colours of the spectra correspond to regions of interest of the same colour in (E).

Figure 7

TEM analysis of a FIB section through a bipyramidal mineral from S. acidocaldarius mineralized for 24 h and heated for 1 day at 150 °C in close system. STEM (A) and TEM (B) images of the section and corresponding SAED pattern consistent with lipscombite. (C,D) EDX map and spectra of the area in (B). Colours of the spectra correspond to regions of interest of the same colour in (C). Arrowhead in panel A shows a large ovoid possibly resulting from the coalescence of individual cellular residues.

Figure 8

TEM analysis of a FIB section through a bipyramidal mineral from S. acidocaldarius mineralized for 24 h and heated for 5 days at 150 °C in close system. STEM (A,C) and TEM (B) images of the section and corresponding SAED pattern consistent with lipscombite (<−110> zone axis). The same SAED pattern is obtained on either sides of the overgrowth boundary, pointed out by arrowheads. (D,E) EDX map and spectra of the area in (C). Colours of the spectra correspond to regions of interest of the same colour in (D).