Limited Response of Indigenous Microbes to Water and Nutrient Pulses in High-Elevation Atacama Soils: Implications for the Cold–Dry Limits of Life on Earth

Soils on the world’s highest volcanoes in the Atacama region represent some of the harshest ecosystems yet discovered on Earth. Life in these environments must cope with high UV flux, extreme diurnal freeze–thaw cycles, low atmospheric pressure and extremely low nutrient and water availability. Only a limited spectrum of bacterial and fungal lineages seems to have overcome the harshness of this environment and may have evolved the ability to function in situ. However, these communities may lay dormant for most of the time and spring to life only when enough water and nutrients become available during occasional snowfalls and aeolian depositions. We applied water and nutrients to high-elevation soils (5100 meters above sea level) from Volcán Llullaillaco, both in lab microcosms and in the field, to investigate how microbial communities respond when resource limitations are alleviated. The dominant taxon in these soils, the extremophilic yeast Naganishia sp., increased in relative sequence abundance and colony-forming unit counts after water + nutrient additions in microcosms, and marginally in the field after only 6 days. Among bacteria, only a Noviherbaspirillum sp. (Oxalobacteraceae) significantly increased in relative abundance both in the lab and field in response to water addition but not in response to water and nutrients together, indicating that it might be an oligotroph uniquely suited to this extreme environment. The community structure of both bacteria and eukaryotes changed significantly with water and water + nutrient additions in the microcosms and taxonomic richness declined with amendments to water and nutrients. These results indicate that only a fraction of the detected community is able to become active when water and nutrients limitations are alleviated in lab microcosms, and that water alone can dramatically change community structure. Our study sheds light on which extremophilic organisms are likely to respond when favorable conditions occur in extreme earthly environments and perhaps in extraterrestrial environments as well.