Hyperdiverse archaea near life limits at the polyextreme geothermal Dallol area

• Published in: Nature ecology & evolution Vol. 3; no. 11; pp. 1552 - 1561
• Main Authors: Belilla, Jodie, Moreira, David, Jardillier, Ludwig, Reboul, Guillaume, Benzerara, Karim, López-García, José M., Bertolino, Paola, López-Archilla, Ana I., López-García, Purificación
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01-11-2019; Nature Publishing Group; Nature
• Subjects: 631/326/171; 631/326/26/2524; Archaea; Bacteria; Biodiversity; Biological and Physical Anthropology; Biomedical and Life Sciences; Brines; Calcium; Calcium ions; Ecology; Evolutionary Biology; Flow cytometry; Fluorescence; Habitability; High temperature; Life Sciences; Magnesium; Microorganisms; Paleontology; pH effects; Phylogeny; Populations and Evolution; RNA, Ribosomal, 16S; rRNA 16S; rRNA 18S; Salts; Scanning electron microscopy; Silica; Silicon dioxide; Sodium chloride; Systematics, Phylogenetics and taxonomy; Water; Water activity; Zoology
• ISSN: 2397-334X; 2397-334X
• DOI: 10.1038/s41559-019-1005-0

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 ribosomal RNA gene 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 in Ethiopia. We identified two physicochemical barriers to life in the presence of surface liquid water defined by (1) high chaotropicity–low water activity in Mg
2+
/Ca
2+
-dominated brines and (2) hyperacidity–salt combinations (pH ~0/NaCl-dominated salt saturation). When detected, life was dominated by highly diverse ultrasmall archaea that were widely distributed across phyla with and without previously known halophilic members. We hypothesize that a high cytoplasmic K
+
-level was an original archaeal adaptation to hyperthermophily, subsequently exapted during several transitions to extreme halophily. 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.
An interdisciplinary investigation of the Dallol polyextreme environment reveals two physicochemical barriers to life in the presence of surface liquid water: high chaotropicity–low water activity and hyperacidity–salt combinations.