Molecular and Isotopic impact of desiccation in high-altitude wetlands analogous to Martian paleolakes

High-altitude Andean wetlands hold extremophilic communities adapted to live in harsh conditions (i.e. high radiation, low rates of precipitation, high rates of evaporation, high salinity, high arsenic concentration, low oxygen pressure, strong winds, or wide daily range in temperatures). They are ecologically interesting settings for understanding the limits of life upon extreme UV radiation and provide natural scenarios to advance knowledge in the evolution of early life on Earth, which emerged upon intense UV radiation due to the lack of an ozone layer in the primitive Earth’s atmosphere. In addition, the unique environmental conditions of the high-altitude Andean lakes show some analogy to Martian paleolakes of the Noachian period (i.e. about 3.5 billion years ago). Therefore, the study of the Andean microbial ecosystem could provide information about life on other planets and we may learn from the microbial survival strategies in the highest perennial lakes and ponds on Earth what happened in the past.

Here, we investigated the microbial ecology of three high-altitude hypersaline ponds from La Puna region (Argentina) showing an increasing extent of desiccation by analyzing their lipid sedimentary record. The aim was to characterize the microbial community structure and metabolic functioning of three hypersaline ponds through the molecular and isotopic (stable carbon and hydrogen) analysis of lipid compounds in their sediments. This work is the first to describe the molecular and isotopic lipid fingerprints in the sediments of astrobiologically interesting wetlands from the Andean Puna region.

We detected lipid biomarkers of cyanobacteria, sulfate-reducing bacteria, purple sulfur bacteria, and archaea in the three alpine ponds, as well as diatoms in the intermediate salinity system. We observed that the relative abundance of biomarkers related to purple sulfur and sulfate-reducing bacteria decreased with salinity, whereas those associated to cyanobacteria and archaea decreased their relative abundance in the mid-saline pond to increase it again and became both prevailing at the highest salinity. Compound-specific isotopic analysis of sedimentary lipid biomarkers revealed that carbon assimilation in the three high-altitude ponds occurred via a combination of the reductive tricarboxylic acid cycle, the reductive pentose phosphate cycle, and the reductive acetyl-CoA pathway. The use of a number of lipid compound ratios as geochemical/environmental proxies allowed the ecological reconstruction of the three lacustrine systems, where a transition along the salinity gradient illustrated the potential impact of desiccation on the microbial community structure. The molecular and compound-specific isotopic analysis of highly resistant lipid biomarkers represents a powerful tool to record those changes over time, which has great value for interpreting the paleobiology of ancient sediment deposits on Earth and beyond.