Abstract
Geothermal springs support microbial communities at elevated temperatures in an ecosystem with high preservation potential that makes them interesting analogs for early evolution of the biogeosphere. The El Tatio geysers field in the Atacama Desert has astrobiological relevance due to the unique occurrence of geothermal features with steep hydrothermal gradients in an otherwise high altitude, hyper-arid environment. We present here results of our multidisciplinary field and molecular study of biogeochemical evidence for habitability and preservation in silica sinter at El Tatio. We sampled three morphologically similar geyser mounds characterized by differences in water activity (i.e., episodic liquid water, steam, and inactive geyser lacking hydrothermal activity). Multiple approaches were employed to determine (past and present) biological signatures and dominant metabolism. Lipid biomarkers indicated relative abundance of thermophiles (dicarboxylic acids) and sulfate reducing bacteria (branched carboxylic acids) in the sinter collected from the liquid water mound; photosynthetic microorganisms such as cyanobacteria (alkanes and isoprenoids) in the steam sinter mound; and archaea (squalane and crocetane) as well as purple sulfur bacteria (cyclopropyl acids) in the dry sinter from the inactive geyser. The three sinter structures preserved biosignatures representative of primary (thermophilic) and secondary (including endoliths and environmental contaminants) microbial communities. Sequencing of environmental 16S rRNA genes and immuno-assays generally corroborated the lipid-based microbial identification. The multiplex immunoassays and the compound-specific isotopic analysis of carboxylic acids, alkanols, and alkanes indicated that the principal microbial pathway for carbon fixation in the three sinter mounds was through the Calvin cycle, with a relative larger contribution of the reductive acetyl-CoA pathway in the dry system. Other inferred metabolic traits varied from the liquid mound (iron and sulfur chemistry), to the steam mound (nitrogen cycle), to the dry mound (perchlorate reduction). The combined results revealed different stages of colonization that reflect differences in the lifetime of the mounds, where primary communities dominated the biosignatures preserved in sinters from the still active geysers (liquid and steam mounds), in contrast to the surviving metabolisms and microbial communities at the end of lifetime of the inactive geothermal mound.
Highlights
Geothermal springs are natural environments of scientific interest because of their significance in the early evolution of the biogeosphere (Walter and Des Marais, 1993; Konhauser et al, 2003; Cady et al, 2018)
Sedimentary microtextures in the sinter deposits suggested that the microbial community at El Tatio is moderately diverse, with a variety of extreme biological communities of thermophilic bacteria (Chloroflexuslike), cyanobacteria, and diatoms (Fernandez-Turiel et al, 2005)
scanning electron microscope (SEM) images from the inside of this sample illustrated entombment of microbial remnants in opalA nanocolloids (Supplementary Figure S1D) and the remnants of exopolysaccharides (EPS) that are often preserved with a honeycomb-like structure on surfaces where microorganisms attached reversibly and irreversibly on exposed sinter surfaces (Supplementary Figure S1E)
Summary
Geothermal springs are natural environments of scientific interest because of their significance in the early evolution of the biogeosphere (Walter and Des Marais, 1993; Konhauser et al, 2003; Cady et al, 2018) Despite their apparent in hospitability, terrestrial geothermal springs are recognized habitats for microbial life on Earth (Brock, 1978). They are considered some of the candidate sites where life began (Van Kranendonk et al, 2017), in contrast to the classical sub-marine hydrothermal-vents theory including the alkaline hydrothermal vent model (Russell, 2018). Not consensus exists on whether wet-dry cycling played a role during abiogenesis (Russell, 2018), the possibility of a landbased origin of life strengthens the relevance of such settings for astrobiological exploration (Van Kranendonk et al, 2017)
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