Microbial diversity and the presence of algae in halite endolithic communities are correlated to atmospheric moisture in the hyper‐arid zone of the Atacama Desert

Abstract

The Atacama Desert is one of the oldest and driest deserts in the world, and its hyper-arid core is described as 'the most barren region imaginable'. We used a combination of high-throughput sequencing and microscopy methods to characterize the endolithic microbial assemblages of halite pinnacles (salt rocks) collected in several hyper-arid areas of the desert. We found communities dominated by archaea that relied on a single phylotype of Halothece cyanobacteria for primary production. A few other phylotypes of salt-adapted bacteria and archaea, including Salinibacter, Halorhabdus, and Halococcus were major components of the halite communities, indicating specific adaptations to the unique halite environments. Multivariate statistical analyses of diversity metrics clearly separated the halite communities from that of the surrounding soil in the Yungay area. These analyses also revealed distribution patterns of halite communities correlated with atmospheric moisture. Microbial endolithic communities from halites exposed to coastal fogs and high relative humidity were more diverse; their archaeal and bacterial assemblages were accompanied by a novel algae related to oceanic picoplankton of the Mamiellales. In contrast, we did not find any algae in the Yungay pinnacles, suggesting that the environmental conditions in this habitat might be too extreme for eukaryotic photosynthetic life.

Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments

“…Habitats as different as the underside of quartz rocks (Azúa-Bustos et al, 2011;Cowan et al, 2011;Chan et al, 2013;de los Ríos et al, 2014;Vikram et al, 2015), sandstones (Friedmann, 1982;de la Torre et al, 2003;Pointing et al, 2009), granite boulders (Wei et al, 2015), the inside of gypsum (Dong et al, 2007;Wierzchos et al, 2011Wierzchos et al, , 2015 and halite evaporites (Wierzchos et al, 2006;Robinson et al, 2015), carbonaceous (DiRuggiero et al, 2013) and volcanic rocks Cámara et al, 2014) among others, have shown that life has found innovative ways to adapt to the extreme conditions of hyper-arid deserts.…”

“…In the Yungay area of the hyper-arid zone of the Atacama Desert, with decades between rainfall events and extremely low air relative humidity (RH; mean yr −1 values <35%), ancient halite crusts of evaporitic origin have been shown to provide sufficient moisture to sustain cryptoendolithic (within pores) microbial communities (Wierzchos et al, 2006;de los Ríos et al, 2010;Robinson et al, 2015). Another strategy for survival in this hyper-arid desert is the colonization of cracks and fissures of rock substrates, also called chasmoendolithic colonization (Dong et al, 2007;DiRuggiero et al, 2013).…”

Fluorescent Fingerprints of Endolithic Phototrophic Cyanobacteria Living within Halite Rocks in the Atacama Desert

“…This remarkable discovery was made inside the halite deposits that form part of the Neogene salt-encrusted playas of Atacama, also known as salares (7). Chroococcidiopsis-like cells were the only cyanobacteria found inside halite pinnacles, and phylogenetic studies revealed their close genetic affinity to the genus Halothece (5,6). The presence of this endolithic community indicates that life has found a survival strategy in the hyperarid zone of Atacama, where all other colonization strategies have failed.…”

“…Indeed, only extremely low concentrations of microorganisms had been detected in the soils of this zone (3). However, despite the major constraint for microbial life in the desert being the scarcity of liquid water, an abundance of photosynthetic life, mainly cyanobacteria associated with heterotrophic bacteria and archaea, has recently been detected in the Atacama's hyperarid zone (4)(5)(6). This remarkable discovery was made inside the halite deposits that form part of the Neogene salt-encrusted playas of Atacama, also known as salares (7).…”

“…These stresses lead to damage that cannot be repaired until metabolism restarts (10,11). Besides desiccation, microbial communities inside halite crusts have to deal with conditions of extreme salinity (5,6) and excess light, which have a direct effect on their physiology. In response to varying light conditions, photosynthetic microorganisms undergo structural, behavioral, physiological, and chemical modifications (12,13), such as changing the quality and concentration of their light-harvesting pigments (12,14,15) and pigment degradation (11,16,17).…”