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Exploring the Microbial Biotransformation of Extraterrestrial www.nature.com/scientificreports OPEN Exploring the microbial biotransformation of extraterrestrial material on nanometer scale Tetyana Milojevic1*, Denise Kölbl1, Ludovic Ferrière 2, Mihaela Albu 3, Adrienne Kish4, Roberta L. Flemming5, Christian Koeberl2,9, Amir Blazevic1, Ziga Zebec 1,6, Simon K.-M. R. Rittmann 6, Christa Schleper 6, Marc Pignitter7, Veronika Somoza7, Mario P. Schimak8 & Alexandra N. Rupert 5 Exploration of microbial-meteorite redox interactions highlights the possibility of bioprocessing of extraterrestrial metal resources and reveals specifc microbial fngerprints 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 fngerprints left on meteorite material, and provide the next step towards an understanding of meteorite biogeochemistry. Our fndings will serve in defning mineralogical and morphological criteria for the identifcation of metal-containing microfossils. Te ability of chemolithotrophic microorganisms to catalyze redox transformations of metals is an exquisite tool for energy transduction between a mineral body and a living entity. Te diferent types of meteorites from diverse parental bodies (asteroids, Moon, or Mars) represent exceptional metal-bearing substrates that have experienced an exposure to multiple extreme conditions during their interstellar or interplanetary travel. During their journey in space, these meteoroids are constantly exposed to vacuum, radiation, and extreme temperature fuctuations. While microbial-mineral interfaces have been extensively investigated and microbial-mediated processing of metal-bearing terrestrial minerals has been abundantly harnessed, exploitation of meteorite resources requires detailed investigations of microbe-extraterrestrial mineral interactions. Te study of meteorite-associated phys- iology of chemolithotrophic microbes is of a special focus due to implications for assessing the potential of extraterrestrial materials as a source of accessible nutrients and energy on the early Earth. Meteorites may have delivered a variety of essential compounds facilitating the evolution of life, as we know it on Earth1–3. Moreover, assessing the biogenicity based on extraterrestrial materials provides a valuable source of information for explor- ing the putative extraterrestrial bioinorganic chemistry that potentially might have occurred in the Solar System. 1Extremophiles/Space Biochemistry Group, Department of Biophysical Chemistry, University of Vienna, Althanstrasse 14, A-1090, Vienna, Austria. 2Natural History Museum, Burgring 7, A-1010, Vienna, Austria. 3Graz Centre for Electron Microscopy, Graz, Austria. 4Unité Molécules de Communication et Adaptation des Microorganismes (MCAM), Muséum National d’Histoire Naturelle, CNRS, 57 rue Cuvier, 75005, Paris, France. 5Department of Earth Sciences, Western University, London, UK. 6Archaea Biology and Ecogenomics Division, Department of Ecogenomics and Systems Biology, University of Vienna, Althanstraße 14, A-1090, Vienna, Austria. 7Department of Physiological Chemistry, Faculty of Chemistry, University of Vienna, Althanstraße 14, 1090, Vienna, Austria. 8Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359, Bremen, Germany. 9Department of Lithospheric Research, University of Vienna, Althanstrasse 14, A-1090, Vienna, Austria. *email: tetyana. [email protected] SCIENTIFIC REPORTS | (2019) 9:18028 | https://doi.org/10.1038/s41598-019-54482-7 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Given that returned extraterrestrial mineralogical samples are to date inaccessible, meteorites are “space probes” available on Earth. Te compositional variety of meteorites is very broad; over 400 minerals have been found in meteorites, predominantly troilite, olivine, pyroxene, feldspar, phyllosilicates, magnetite, kamacite, and taenite. Te primitive (chondritic) classes of meteorites are the most abundant, with iron and nickel as the dominant ferrous metals4. Troilite [FeS] and FeNi alloys [Fe1-xNix] as meteoritic components can be potentially used as electron donors by iron and sulfur oxidizing organisms. Several laboratory experiments on meteorites have been performed, demonstrating that some iron-oxidizing bacteria (e.g., Leptospirillum ferrooxidans, Acidithiobacillus ferrooxidans) could propagate on metal-bearing meteorite materials and use them as energy sources5,6. Recently, an in situ assessment of the microbial communities, which colonize stony meteorites, has been published, aim- ing to reveal metal-cycling microorganisms naturally contaminating astromaterials rich in FeNi-alloys and FeS7. Te extreme thermoacidophile Metallosphaera sedula is a metallophilic archaeon that lives in hot acidic condi- tions (73 °C and pH 2) and uses various metal-containing ores to run its respiratory electron transport chain8–10. Previously, we have shown that this metal mobilizing archaeon can grow on Martian regolith simulants, actively colonizing these artifcial extraterrestrial materials, releasing free soluble metals into the leachate solution and leaving specifc spectral fngerprints11. In the present work, we explore the physiology and metal-microbial inter- face of M. sedula, living on and interacting with a real extraterrestrial material, H5 ordinary chondrite Northwest Africa 1172 ((NWA 1172), Supplementary Fig. 1)12. Specifc chemical analysis of the meteorite-microbial inter- face at nm-scale spatial resolution allowed us to trace the trafcking of meteorite inorganic constituents into a microbial cell and to investigate iron redox behavior. Combining several analytical spectroscopy techniques with transmission electron microscopy (TEM) analysis, we provide a set of biogeochemical fngerprints lef upon M. sedula growth on the NWA 1172 meteorite. Results and Discussion Chemolithotrophic growth of M. sedula on NWA 1172. M. sedula was capable of autotrophic growth on stony meteorite NWA 1172, utilizing metals trapped within it as the sole energy source. Scanning electron microscopy (SEM) investigations (Fig. 1a,b and Supplementary Fig. 2) and multi-labeled fuorescence in situ hybridization (MiL-FISH) with an M. sedula-specifc ribosomal RNA-targeted probe (Fig. 1c–e, Supplementary Fig. 3, and Supplementary Table 1) indicate an active colonization of the meteorite material by M. sedula. As reported earlier, the round to slightly irregular coccoid cells of M. sedula possess pilus-like structures and can be motile when grown on the metal ore9. When grown in the presence of NWA 1172, cells of M. sedula were characterized by intensive vivid motility (Supplementary Movie 1). In comparison to chalcopyrite, M. sedula had a superior growth rate on the stony meteorite (Fig. 1f). Grown in the presence of chalcopyrite, cells of M. sedula displayed motility as well (Supplementary Movie 2). Meteorite-grown M. sedula reached stationary phase at 163 h (maximum density 18.5 ± 2 × 108 cells/mL, a mean generation time of 8 h), while chalcopyrite-grown cells were still in exponential phase at that time point, and reached the stationary phase afer 300 h (maximum density 15.1 ± 5 × 108 cells/mL, a mean generation time of 21.4 h) (Fig. 1f). Tis diference refects the benefcial contribution of NWA 1172 as the sole electron donor suggesting its preferential nature as energy source for M. sedula. NWA 1172 is a chondrite meteorite with relatively high iron abundance12 and a wide range of other metal elements (Supplementary Fig. 1). Tose might be used by M. sedula as an energy source to satisfy its bioener- getic needs and as specifc metabolic/enzymatic cofactors, providing more optimal constitutive and/or structural elements for enzymatic machinery. In addition, copper sulfdes, such as chalcopyrite, dictate certain inevitable issues in respect with metal mobilizing due to their refractory characteristics. Hence, the porosity of NWA 1172 (typically of a few percent13) might also refect the superior growth rate of M. sedula over refractory and densely packed chalcopyrite. As a result of tight biogeochemical interactions, by means of its metal oxidizing machinery14–16, M. sedula released free soluble metals (Ni, Si, Co, Mn, and K) into the cultivation medium (Fig. 1g). Ni and Si were pre- dominantly released, reaching 0.55 and 0.17 g/L, respectively, with lesser contributions from Co, Mn, and K ions (Fig. 1g). Dehydration-crystallization and X-ray difraction experiments (Supplementary Fig. 4) revealed 17 the chemical speciation of the released Ni: nickel sulfate hexahydrate in the tetragonal space group P 41212 (a = 6.8 Å, b = 6.8 Å, c = 18.29999, α = β = γ = 90°) and magnesium sulfate heptahydrate18 in the orthorhombic space group P 212121 (a = 11.868 Å, b = 11.996 Å, c = 6.857 Å, α = β = γ = 90°), suggesting +2 oxidation state of extracted Ni ions and the occurrence of nickel
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