Active Microbial Airborne Dispersal and Biomorphs as Confounding Factors for Life Detection in the Cell-Degrading Brines of the Polyextreme Dallol Geothermal Field.

Determining the precise limits of life in polyextreme environments is challenging. Studies along gradients of polyextreme conditions in the Dallol proto-volcano area (Danakil salt desert, Ethiopia) showed the occurrence of archaea-dominated communities (up to 99%) in several hypersaline systems but strongly suggested that life did not thrive in the hyperacidic (pH ∼0), hypersaline (∼35% [wt/vol],) and sometimes hot (up to 108°C) ponds of the Dallol dome. However, it was recently claimed that archaea flourish in these brines based on the detection of one Nanohaloarchaeotas 16S rRNA gene and fluorescent in situ hybridization (FISH) experiments with archaea-specific probes. Here, we characterized the diversity of microorganisms in aerosols over Dallol, and we show that, in addition to typical bacteria from soil/dust, they transport halophilic archaea likely originating from neighboring hypersaline ecosystems. We also show that cells and DNA from cultures and natural local halophilic communities are rapidly destroyed upon contact with Dallol brine. Furthermore, we confirm the widespread occurrence of mineral particles, including silica-based biomorphs, in Dallol brines. FISH experiments using appropriate controls show that DNA fluorescent probes and dyes unspecifically bind to mineral precipitates in Dallol brines; cellular morphologies were unambiguously observed only in nearby hypersaline ecosystems. Our results show that airborne cell dispersal and unspecific binding of fluorescent probes are confounding factors likely affecting previous inferences of archaea thriving in Dallol. They highlight the need for controls and the consideration of alternative abiotic explanations before safely drawing conclusions about the presence of life in polyextreme terrestrial or extraterrestrial systems. IMPORTANCE Determining the precise limits of life in polyextreme environments is challenging. Confounding factors such as exogenous contamination and the abiotic formation of structures resembling cells need to be considered before concluding on the unambiguous development of microbial life in low-biomass environments. Here, we explored how these factors can affect contrasting reports about microbial life thriving in the hypersaline and hyperacidic brines of the Dallol geothermal field (Danakil Depression, Ethiopia). We show not only that aerosols actively transport a wide diversity of prokaryotic and eukaryotic cells over Dallol but also that, upon contact with the chaotropic hyperacidic brine, cells and DNA are rapidly degraded. We also show the extant occurrence of mineral (mostly silica-based) biomorphs that unspecifically bind fluorescent probes and dyes. Our study highlights the need for controls and the consideration of alternative abiotic explanations before safely drawing conclusions on the presence of life in polyextreme terrestrial or extraterrestrial systems.

Nanoscale Anatomy of Iron-Silica Self-Organized Membranes: Implications for Prebiotic Chemistry.

Iron-silica self-organized membranes, so-called chemical gardens, behave as fuel cells and catalyze the formation of amino/carboxylic acids and RNA nucleobases from organics that were available on early Earth. Despite their relevance for prebiotic chemistry, little is known about their structure and mineralogy at the nanoscale. Studied here are focused ion beam milled sections of iron-silica membranes, grown from synthetic and natural, alkaline, serpentinization-derived fluids thought to be widespread on early Earth. Electron microscopy shows they comprise amorphous silica and iron nanoparticles of large surface areas and inter/intraparticle porosities. Their construction resembles that of a heterogeneous catalyst, but they can also exhibit a bilayer structure. Surface-area measurements suggest that membranes grown from natural waters have even higher catalytic potential. Considering their geochemically plausible precipitation in the early hydrothermal systems where abiotic organics were produced, iron-silica membranes might have assisted the generation and organization of the first biologically relevant organics.

A Polyextreme Hydrothermal System Controlled by Iron: The Case of Dallol at the Afar Triangle.

One of the latest volcanic features of the Erta Ale range at the Afar Triangle (NE Ethiopia) has created a polyextreme hydrothermal system located at the Danakil depression on top of a protovolcano known as the dome of Dallol. The interaction of the underlying basaltic magma with the evaporitic salts of the Danakil depression has generated a unique, high-temperature (108 °C), hypersaline (NaCl supersaturated), hyperacidic (pH values from 0.1 to -1.7), oxygen-free hydrothermal site containing up to 150 g/L of iron. We find that the colorful brine pools and mineral patterns of Dallol derive from the slow oxygen diffusion and progressive oxidation of the dissolved ferrous iron, the iron-chlorine/-sulfate complexation, and the evaporation. These inorganic processes induce the precipitation of nanoscale jarosite-group minerals and iron(III)-oxyhydroxides over a vast deposition of halite displaying complex architectures. Our results suggest that life, if present under such conditions, does not play a dominant role in the geochemical cycling and mineral precipitation at Dallol as opposed to other hydrothermal sites. Dallol, a hydrothermal system controlled by iron, is a present-day laboratory for studying the precipitation and progressive oxidation of iron minerals, relevant for geochemical processes occurring at early Earth and Martian environments.

Biomimetic mineral self-organization from silica-rich spring waters.

Purely inorganic reactions of silica, metal carbonates, and metal hydroxides can produce self-organized complex structures that mimic the texture of biominerals, the morphology of primitive organisms, and that catalyze prebiotic reactions. To date, these fascinating structures have only been synthesized using model solutions. We report that mineral self-assembly can be also obtained from natural alkaline silica-rich water deriving from serpentinization. Specifically, we demonstrate three main types of mineral self-assembly: (i) nanocrystalline biomorphs of barium carbonate and silica, (ii) mesocrystals and crystal aggregates of calcium carbonate with complex biomimetic textures, and (iii) osmosis-driven metal silicate hydrate membranes that form compartmentalized, hollow structures. Our results suggest that silica-induced mineral self-assembly could have been a common phenomenon in alkaline environments of early Earth and Earth-like planets.