RESUMEN

BACKGROUND: The Andean Altiplano hosts a repertoire of high-altitude lakes with harsh conditions for life. These lakes are undergoing a process of desiccation caused by the current climate, leaving terraces exposed to extreme atmospheric conditions and serving as analogs to Martian paleolake basins. Microbiomes in Altiplano lake terraces have been poorly studied, enclosing uncultured lineages and a great opportunity to understand environmental adaptation and the limits of life on Earth. Here we examine the microbial diversity and function in ancient sediments (10.3-11 kyr BP (before present)) from a terrace profile of Laguna Lejía, a sulfur- and metal/metalloid-rich saline lake in the Chilean Altiplano. We also evaluate the physical and chemical changes of the lake over time by studying the mineralogy and geochemistry of the terrace profile. RESULTS: The mineralogy and geochemistry of the terrace profile revealed large water level fluctuations in the lake, scarcity of organic carbon, and high concentration of SO42--S, Na, Cl and Mg. Lipid biomarker analysis indicated the presence of aquatic/terrestrial plant remnants preserved in the ancient sediments, and genome-resolved metagenomics unveiled a diverse prokaryotic community with still active microorganisms based on in silico growth predictions. We reconstructed 591 bacterial and archaeal metagenome-assembled genomes (MAGs), of which 98.8% belonged to previously unreported species. The most abundant and widespread metabolisms among MAGs were the reduction and oxidation of S, N, As, and halogenated compounds, as well as aerobic CO oxidation, possibly as a key metabolic trait in the organic carbon-depleted sediments. The broad redox and CO2 fixation pathways among phylogenetically distant bacteria and archaea extended the knowledge of metabolic capacities to previously unknown taxa. For instance, we identified genomic potential for dissimilatory sulfate reduction in Bacteroidota and α- and γ-Proteobacteria, predicted an enzyme for ammonia oxidation in a novel Actinobacteriota, and predicted enzymes of the Calvin-Benson-Bassham cycle in Planctomycetota, Gemmatimonadota, and Nanoarchaeota. CONCLUSIONS: The high number of novel bacterial and archaeal MAGs in the Laguna Lejía indicates the wide prokaryotic diversity discovered. In addition, the detection of genes in unexpected taxonomic groups has significant implications for the expansion of microorganisms involved in the biogeochemical cycles of carbon, nitrogen, and sulfur. Video Abstract.

Asunto(s)

Archaea , Bacterias , Variación Genética , Sedimentos Geológicos , Lagos , Lagos/microbiología , Archaea/genética , Archaea/metabolismo , Archaea/clasificación , Sedimentos Geológicos/microbiología , Bacterias/clasificación , Bacterias/genética , Bacterias/metabolismo , Bacterias/aislamiento & purificación , Chile , Filogenia , Microbiota , Extremófilos/metabolismo , Extremófilos/genética , Extremófilos/clasificación , ARN Ribosómico 16S/genética

RESUMEN

Subaerial hydrothermal systems are of great interest for paleobiology and astrobiology as plausible candidate environments to support the origin of life on Earth that offer a unique and interrelated atmosphere-hydrosphere-lithosphere interface. They harbor extensive sinter deposits of high preservation potential that are promising targets in the search for traces of possible extraterrestrial life on Hesperian Mars. However, long-term quality preservation is paramount for recognizing biosignatures in old samples and there are still significant gaps in our understanding of the impact and extent of taphonomy processes on life fingerprints. Here, we propose a study based on lipid biomarkers -highly resistant cell-membrane components- to investigate the effects of silicification on their preservation in hydrothermal opaline sinter. We explore the lipid biomarkers profile in three sinter deposits of up to ~3000 years from El Tatio, one of the best Martian analogs on Earth. The lipid profile in local living biofilms is used as a fresh counterpart of the fossil biomarkers in the centuries-old sinter deposits to qualitatively assess the taphonomy effects of silicification on the lipid's preservation. Despite the geological alteration, the preserved lipids retained a depleted stable-carbon isotopic fingerprint characteristic of biological sources, result highly relevant for astrobiology. The data allowed us to estimate for the first time the degradation rate of lipid biomarkers in sinter deposits from El Tatio, and to assess the time preservation framework of opaline silica. Auxiliary techniques of higher taxonomic resolution (DNA sequencing and metaproteomics) helped in the reconstruction of the paleobiology. The lipids were the best-preserved biomolecules, whereas the detection of DNA and proteins dropped considerably from 5 cm depth. These findings provide new insights into taphonomy processes affecting life fingerprints in hydrothermal deposits and serves as a useful baseline for assessing the time window for recovering unambiguous signs of past life on Earth and beyond.

Asunto(s)

Medio Ambiente Extraterrestre , Marte , Chile , Isótopos , Biomarcadores , Lípidos

RESUMEN

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.