Exploring the microbial biotransformation of extraterrestrial material on nanometer scale

Abstract

Exploration of microbial-meteorite redox interactions highlights the possibility of bioprocessing of extraterrestrial metal resources and reveals specific microbial fingerprints left on extraterrestrial material. In the present study, we provide our observations on a microbial-meteorite nanoscale interface of the metal respiring thermoacidophile Metallosphaera sedula. M. sedula colonizes the stony meteorite Northwest Africa 1172 (NWA 1172; an H5 ordinary chondrite) and releases free soluble metals, with Ni ions as the most solubilized. We show the redox route of Ni ions, originating from the metallic Ni° of the meteorite grains and leading to released soluble Ni²⁺. Nanoscale resolution ultrastructural studies of meteorite grown M. sedula coupled to electron energy loss spectroscopy (EELS) points to the redox processing of Fe-bearing meteorite material. Our investigations validate the ability of M. sedula to perform the biotransformation of meteorite minerals, unravel microbial fingerprints left on meteorite material, and provide the next step towards an understanding of meteorite biogeochemistry. Our findings will serve in defining mineralogical and morphological criteria for the identification of metal-containing microfossils.

Figure 1

Biotransformation of the chondrite meteorite NWA 1172 by M. sedula. (a) Scanning electron microscopy (SEM) image of fragments of the chondrite meteorite NWA 1172 bioprocessed by M. sedula. (b) SEM image showing M. sedula cells colonizing the surface of the meteorite particles. (c–e) Multi-Labeled-Fluorescence in situ Hybridization (MiL-FISH) of M. sedula cells grown on NWA 1172 as the sole energy sources: (c) MiL-FISH images of cells (green) after hybridization with the specific oligonucleotide probe targeting M. sedula; (d) DAPI staining of the same field (blue); (e) Overlaid epifluorescence image, showing overlap of the specific oligonucleotide probe targeting M. sedula with DAPI signals. Arrows indicate cells of M. sedula. Scale bar, 2 µm. (f) Growth curves of autotrophic cultures of M. sedula cultivated at 73 °C on NWA 1172 (red) and chalcopyrite (blue). Legends represent the corresponding type of energy source. (g) Inductively coupled plasma-optical emission spectrometry (ICP-OES) analysis of released metal ions in the supernatant of M. sedula cultures grown on NWA 1172 as the sole energy source. Samples were taken at “0” time point (red), from late exponentially growing cultures of M. sedula (purple), and from corresponding abiotic controls (blue and grey, respectively). (h) Single crystals of nickel sulfate hexahydrate and magnesium sulfate heptahydrate were obtained after recrystallization of the crystalline material (α) shown in Supplementary Fig. 4. (i) Atomic structures of NiSO₄ × 6 H₂O and MgSO₄ × 7 H₂O from crystals in (h) as investigated with single crystal X-ray diffraction, with the unit cell for each structure represented. Crystal water has been removed for clarity. Legend: Ni(H₂O)₆, red octahedra; Mg(H₂O)₆, blue octahedra; SO₄²⁻, yellow tetrahedra. Points and error bars show the mean and error-represented standard deviation, respectively, of n = 3 biological replicates. If not visible, error bars are smaller than symbols.

Figure 2

Elemental ultrastructural analysis of M. sedula grown on NWA 1172. The annular dark field (ADF) scanning transmission electron microscopy (STEM) image of a cell of M. sedula used for the EDS spectrum image acquisition and corresponding extracted carbon (C), oxygen (O), nitrogen (N), copper (Cu), sulfur (S), potassium (K), chlorine (Cl), iron (Fe), aluminum (Al), phosphorus (P), cobalt (Co), silicon (Si), and uranium (U) elemental maps. Scale bar, 0.5 µm.

Figure 3

Elemental ultrastructural analysis of M. sedula empty envelopes encrusted during growth on NWA 1172 and corresponding Fe L_2,3-edge core electron energy loss (EEL) spectra. The high angular annular dark field (HAADF) scanning transmission electron microscopy (STEM) image of a heavily encrusted cell remnants of M. sedula used for the EDS spectrum image acquisition and corresponding carbon (C), copper (Cu), phosphorus (P), iron (Fe) oxygen (O), nickel (Ni), sulfur (S), and nitrogen (N) elemental maps. Corresponding Fe L_2,3-edge core electron energy loss (EEL) spectra acquired from the S-layer of M. sedula cells depicted in Supplementary Fig. 8a (shown as dotted line) and from the crust in Supplementary Fig. 8c (shown as solid line) are provided at the bottom panel.

Figure 4

Alteration of the surface of the chondrite meteorite NWA 1172 slabs mediated by M. sedula. (a) Secondary electron (SE) image of a NWA 1172 slab cultivated with M. sedula at 73 °C. (b) Magnified SE image of a NWA 1172 slab cultivated with M. sedula at 73 °C. (c) SE image of abiotically exposed slab of NWA 1172 to the cultivation medium at 73 °C. (d) Magnified area of SE image of NWA 1172 slab cultivated with M. sedula at 73 °C. (e) EDS spectra of globular structures (marked with red A) that form iron oxides aggregates, containing mainly Fe and P. (f) EDS spectra of branched network of crystalline iron oxides (marked with red b). Arrows indicate the areas where crystalline iron oxides occur.

Figure 5

Electron Paramagnetic Resonance (EPR) spectra of raw NWA 1172 (gray line), NWA 1172 bioprocessed by M. sedula (red line) and NWA 1172 after the treatment with cultivation medium, but without M. sedula (abiotic control, blue line). (a) Spectra recorded at 90 K with assigned linewidth (deltaH) and g-values. (b) Spectra recorded at 273 K.