The Lipidome of a Mars Analog Poly-Extreme Community in Atacama Halite Endolith: Chemotaxonomy,Lipid Adaptation,and Implications for the Search for Extraplanetary Biosignatures

Abstract

We analyzed the lipidome of the endolithic community in halite nodules from Salar Grande in the hyperarid Atacama Desert, which is considered an analog for martian subsurface environments. We tested the utility of complex functionalized lipids to trace possible extraterrestrial biosignatures under poly-extreme conditions (high osmolarity, desiccation, and irradiance) and evaluated their chemotaxonomic potential for space applications. We identified a total of 269 compounds in the Mars analog community. The complex functionalized lipid pool includes 150 bacterial bilayer-forming intact ester and ether lipids, 15 membrane-regulating bacteriohopanepolyols, and 9 heterocyte glycolipids, as well as 34 archaeal diether membrane lipids and 8 eukaryotic sterols. Thirteen pigments and quinones were also detected. The complex functionalized lipid pool carries the diagnostic fingerprints of cyanobacteria (including N₂-fixing cyanobacteria), Salinibacter, Planctomycetes, and archaeal Halobacteria; each showed core lipid and headgroup adaptation to the multistress environment. We also compared the complex functionalized lipid fingerprints with the lipid fingerprint obtained following base hydrolysis. Our results show that lipid assemblages differ at the compound class level (e.g., absence of hopanoids) as well as core lipid structure level (e.g., degree of unsaturation). Much of the diagnostic information contained in the complex functionalized lipid pool is lost when analyzing gas chromatography–amenable biomarkers only. These results should guide future analysis of Mars return samples as well as ongoing technological developments for in situ detection of mineral-associated lipids.