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Lipid Profiles From Fresh Biofilms Along a Temperature Gradient on a Hydrothermal Stream at El Tatio (Chilean Andes), as a Proxy for the Interpretation of Past and Present Biomarkers Beyond Earth

ABSTRACT: Hydrothermal systems and their deposits are primary targets in the search for fossil evidence of life beyond Earth. However, to learn how to decode fossil biomarker records in ancient hydrothermal deposits, we must first be able to interpret unambiguously modern biosignatures, their distribution patterns, and their association with physicochemical factors. Here, we investigated the molecular and isotopic profile of microbial biomarkers along a thermal gradient (from 29 to 72°C) in a hot spring (labeled Cacao) from El Tatio, a geyser field in the Chilean Andes with abundant opaline silica deposits resembling the nodular and digitate structures discovered on Mars. As a molecular forensic approach, we focused on the analysis of lipid compounds bearing recognized resistance to degradation and the potential to reconstruct the paleobiology of an environment on a broader temporal scale than other, more labile, biomolecules. By exploiting the lipid biomarkers’ potential to diagnose biological sources and carbon fixation pathways, we reconstructed the microbial community structure and its ecology along the Cacao hydrothermal transect. The taxonomic adscription of the lipid biomarkers was qualitatively corroborated with DNA sequencing analysis. The forensic capacity of the lipid biomarkers to identify biosources in fresh biofilms was validated down to the genus level for Roseiflexus, Chloroflexus, and Fischerella. We identified lipid biomarkers and DNA of several new cyanobacterial species in El Tatio and reported the first detection of Fischerella biomarkers at a temperature as high as 72°C. This, together with ecological peculiarities and the proportion of clades being characterized as unclassified, illustrates the ecological singularity of El Tatio and strengthens its astrobiological relevance. The Cacao hydrothermal ecosystem was defined by a succession of microbial communities and metabolic traits associated with a high- (72°C) to low-(29°C) temperature gradient that resembled the inferred metabolic sequence events from the 16S rRNA gene universal phylogenetic tree from thermophilic to anoxygenic photosynthetic species and oxygenic phototrophs. The locally calibrated DNA-validated lipidic profile in the Cacao biofilms provided a modern (molecular and isotopic) end member to facilitate the recognition of past biosources and metabolisms from altered biomarkers records in ancient silica deposits at El Tatio analogous to Martian opaline silica structures.

SUBMITTER: Megevand V

PROVIDER: S-EPMC9271869 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:Microbial mats floating within multiple hydrothermally sourced streams in El Tatio, Chile, frequently exhibit brittle siliceous crusts (~1 mm thick) above the air-water interface. The partially silicified mats contain a diverse assemblage of microbial clades and metabolisms, including cyanobacteria performing oxygenic photosynthesis. Surficial crusts are composed of several amorphous silica layers containing well-preserved filaments (most likely cyanobacteria) and other cellular textures overlying EPS-rich unsilicified mats. Environmental logs, silica crust distribution, and microbial preservation patterns provide evidence for crust formation via repeated cycles of evaporation and silica precipitation. Within the mats, in situ microelectrode profiling reveals that daytime oxygen concentrations and pH values are diminished beneath silica crusts compared with adjacent unencrusted communities, indicating localized inhibition of oxygenic photosynthesis due to light attenuation. As a result, aqueous conditions under encrusted mats have a higher saturation state with regard to amorphous silica compared with adjacent, more active mats where high pH increases silica solubility, likely forming a modest feedback loop between diminished photosynthesis and crust precipitation. However, no fully lithified sinters are associated with floating encrusted mats in El Tatio streams, as both subaqueous and subaerial silica precipitation are limited by undersaturated, low-SiO2 (<150 ppm) stream waters. By contrast, well-cemented sinters can form by evaporation in silica-undersaturated solutions above 200 ppm SiO2 . Floating mats in El Tatio therefore represent a specific sinter preservation window, where evaporation in silica-undersaturated microbial mats produces crusts, which preserve cells and affect mat chemistry, but low-silica concentrations prevent the formation of lasting sinter deposits. Patterns of silica precipitation in El Tatio microbial communities show that the preservation potential of silicifying mats in the rock record is strongly dependent on aqueous silica concentrations.

Dataset Information

Lipid Profiles From Fresh Biofilms Along a Temperature Gradient on a Hydrothermal Stream at El Tatio (Chilean Andes), as a Proxy for the Interpretation of Past and Present Biomarkers Beyond Earth

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