Hyperdiverse archaea near life limits at the polyextreme geothermal Dallol area

Abstract

M Microbial life has adapted to various individual extreme conditions; yet, organisms simultaneously adapted to very low pH, high salt and high temperature are unknown. We combined environmental 16S/18S rRNAgene metabarcoding, cultural approaches, fluorescence-activated cell sorting, scanning electron microscopy and chemical analyses to study samples along such unique polyextreme gradients in the Dallol-Danakil area (Ethiopia). We identify two physicochemical barriers to life in the presence of surface liquid water defined by: i) high chaotropicity-low water activity in Mg 2+ /Ca 2+-dominated brines and ii) hyperacidity-salt combinations (pH~0/ NaCl-dominated salt-saturation). When detected, life was dominated by highly diverse ultrasmall archaea widely distributed across phyla with and without previously known halophilic members. We hypothesize that high cytoplasmic K +-level was an original archaeal adaptation to hyperthermophily, subsequently exapted during multiple transitions to extreme halophily. W We detect active silica encrustment/fossilization of cells but also abiotic biomorphs of varied chemistry. Our work helps circumscribing habitability and calls for cautionary interpretations of morphological biosignatures on Earth and beyond. Belilla et al. 3 Microbial life has adapted to so-called extreme values of temperature, pH or salinity, but also to several polyextreme, e.g. hot acidic or salty alkaline, ecosystems 1,2. Various microbial lineages have been identified in acidic brines in the pH range 1.5-4.5, e.g. in Western Australia 3,4 and Chile 3. However, although some acidophilic archaea thrive at pH~0 (Picrophilus oshimae grows at an optimal pH of 0.7) 5 and many halophilic archaea live in hypersaline systems (>30%; NaCl-saturation conditions), organisms adapted simultaneously to very low pH (<1) and high salt, and eventually also high temperature, are not known among cultured prokaryotic species 1. Are molecular adaptations to these combinations incompatible or (hot) hyperacidic hypersaline environments simply rare and unexplored? The Dallol geothermal dome and its surroundings (Danakil Depression, Afar, Ethiopia) allow to address this question by offering unique polyextreme gradients combining high salt content (33 to >50%; either Mg 2+ /Ca 2+ or Na + (/Fe 2+/3+)-rich), high temperature (25-110°C) and low pH (≤-1.5 to 6). Dallol is an uplifted (~40 m) dome structure located in the North of the Danakil depression (~120 m below-sea-level), a 200 km-long basin within the Afar rift, at the triple junction between the Nubian, Somalian and Arabian Plates 6. Lying only 30 km north of the hypersaline, hydrothermally-influenced, Lake Assale (Karum) and the Erta Ale volcanic range, Dallol does not display volcanic outcrops but intense degassing and hydrothermalism. These activities are observed on the salt dome and the adjacent Black Mountain and Yellow Lake (Gaet'Ale) areas 6,7 (Fig. 1a-b). Gas and fluid isotopic measurements indicate that meteoritic waters, notably infiltrating from the high Ethiopian plat...

Origin and Evolution of the Halo-Volcanic Complex of Dallol: Proto-Volcanism in Northern Afar (Ethiopia)

“…We identified similar bubbling pools aligned following an E-W direction north of the Round Mountain, 3.5 km west of the Dallol crater ( Figures 3J, 5). The Black Lake is also an active small geothermal pond (∼15 m diameter, ∼10 m depth) located close to the north limit of the Black Mountain and containing an acidic (pH ∼3) hot (∼70 • C) extremely hypersaline (>70%) brine, mainly composed of bischofite (magnesium chloride) (Belilla et al, 2019). The Black Mountain area exhibits frequent massive bischofite flows, which we witnessed in January 2016 and 2019 (no.…”

“…30 km south to Dallol, on the northern side of the Erta Ale volcanic chain. In addition to geological observations, field and laboratory analyses were performed to characterize the local physicochemistry of the different local polyextreme environments, determine whether life can thrive under those conditions (Belilla et al, 2019) and study brine chemical evolution and the dynamics of mineral precipitation (Kotopoulou et al, 2019). During the third field trip (12-26 January 2019), we revisited the previously sampled areas and we extended our exploration to the Round Mountain and to different lakes around the Erta Ale volcanic range: Lake Assale (Karum), Lake Bakili and several unnamed small lakes ( Figures 1A,B).…”

“…One of the most spectacular morphologies are the salt terraced ponds (Figures 8E,F). When they are full of water, they exhibit very low pH values (pH ≤ 0) and high amounts of iron, manganese, and sulfur (Belilla et al, 2019) at different oxidation states that color these pools with an impressive green, orange and yellow palette detailed in Kotopoulou et al (2019). Most of the different delicate salt crystallization processes take place in these areas, some of them being very common, as the mushroom-like salt deposits (Figure 8G), while others are very rare, e.g., salt balls ( Figure 8H).…”

“…An intense geothermal activity, which occasionally includes phreatic explosions and is mainly controlled by poorly understood interactions between magma, deep hydrated salts and groundwater, results in the world-renowned colorful acidic brine ponds, fumaroles, small geysers, salt deposits, and other hydro-geothermal manifestations (Holwerda and Hutchinson, 1968;Hovland et al, 2006;Talbot, 2008;Franzson et al, 2015;Warren, 2015a;Varet, 2018). The result of such interactions is a particularly extreme environment with brines exhibiting low pH (≤0), high salt contents (>30%) and high temperatures (up to ∼110 • C) (Belilla et al, 2019), undergoing a hyper-arid climate (<200 mm/year rainfall) with the official world record of the highest annual mean temperature (34.5 • C; Pedgley, 1967). Other minor geothermal-related structures are located around the Dallol dome.…”

“…Dallol has also attracted attention as a potential analog of some Mars regions (Cavalazzi et al, 2019). The brines of the geothermal field of Dallol combine unique polyextreme conditions that are limiting for life (Belilla et al, 2019). However, although some general models to explain the genesis of the dome have been proposed (Talbot, 2008;Carniel et al, 2010;Franzson et al, 2015;Warren, 2015c), a comprehensive model about the origin and temporal evolution of both, the dome and its geothermal activity resulting in hyperacidic and saltoversaturated brines is still lacking.…”