Mirroring the effect of geological evolution: Protist divergence in the Atacama Desert

Abstract

Unicellular eukaryotes, also called protists, are potentially fast evolving organisms. The small size of protists, their fast reproduction rate and ability to form cysts as well as their adaptability to extreme conditions allow them to associate to endemic animals, plants, saline lakes and soil even in extremely arid systems. These properties make unicellular eukaryotes ideal model organisms to combine studies on evolutionary processes of very different groups of organisms and across very different time scales comprising even geological ones. The hyperarid Atacama Desert offers a study area unique on Earth, where a predominantly arid climate was present for millions of years. A comprehensive analysis of the diversity of unicellular eukaryotes in different habitats (endemic desert plant phyllosphere, the gut of endemic darkling beetles, isolated hypersaline waters) revealed a dataset distinct and divergent from other regions on Earth. We used standard isolation and cultivation protocols to elucidate divergence patterns for a variety of very different and independent taxonomic groups of protists such as gregarines and ciliates among alveolates, placidids among stramenopiles and choanoflagellates among opisthokonts. The ability to rapidly adapt to extreme environments, which enhance a fast divergence rate at high UV radiation, has only been reported for prokaryotes up to now. The establishment of arid to hyperarid conditions in the Atacama Desert about 20 Ma ago has obviously led to an isolation of protist populations followed by a radiation of species. There are only a few regions on Earth with similar extreme salinity conditions reducing the chance of an exchange between protist populations. Divergence patterns in unicellular eukaryotes in very different phylogenetic groups independently mirror the effect of geological evolution and climate variability during the Neogene. • Protist diversity in different habitats of the Atacama Desert is distinct and divergent from other regions on Earth • Due to the isolation of habitable microenvironments the Atacama region forms a center of radiation of protists • Time scales of the evolution of protists can be related to geological/tectonic events