The entanglement of microorganisms and mineral matrices in a hyperarid environment – observations by SEM imaging and biomarker analysis from the Atacama Desert

Abstract

In hyperarid deserts like the Atacama Desert, biota face additional aggravations beside the dryness, e.g. high UV radiation and often high surface temperatures. However, even under these extreme conditions, diverse microbial communities thrive on and within the sediment and interact strongly with their mineral substrate. Common habitats for microbial communities in this environment are fog-receiving surfaces and endolithic zones within evaporite crusts. Endolithic microorganisms are highly adapted to both the substrate and severe water limitations and colonize protected cracks, niches, and caverns within translucent rocks and crusts. They have the potential to alter mineral components and stimulate the formation of secondary minerals as they redistribute moisture and potentially extract crystal water. Processes like these are the starting point of pedogenesis and, even if proceeding extremely slowly, affect the shape of the surface. To elucidate the relationship of microbial communities with the mineral matrix, we investigated the biogeochemical traces of microbial communities and their spatial distribution on and within gypsum and halite crusts from different regions within the Atacama Desert in Northern Chile. We combined imaging techniques (scanning electron microscopy, SEM) and biomolecular methods (gas chromatography-mass spectrometry, GC-MS/MS and nuclear magnetic resonance, NMR) to obtain a deeper insight into the entanglement of microorganisms and evaporitic crusts. Tight interactions of bacteria and fungi with the mineral matrix were revealed by SEM. Short-chain membrane fatty acids (C14-C18) indicated recent bacterial activity in all samples analyzed. Extracellular short-chain acids (C6-C12) and carbohydrates of the extracellular polymeric substances (EPS) make up to 75% of the total biomass within evaporites which point to efficient desiccation buffers and protection mechanisms against UV radiation. Furthermore, the sticky EPS leads to the biochemical stabilization of mineral aggregates by agglutination, which was also visible with SEM.