Endolithic microbial habitats as refuges for life in polyextreme environment of the Atacama Desert

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Highlights

  • The hyperarid core of the Atacama Desert is one of the most abiotic places on Earth.

  • The Atacama Desert's core is a polyextreme environment for all forms of life.

  • Atacama's endoliths are low-complexity communities adapted to polyextreme conditions.

  • Microbial habitability of rocks depends on their architecture and water availability.

The extremely harsh conditions of hyperarid deserts are a true challenge for microbial life. Microorganisms thriving in such polyextreme environments are fascinating as they can tell us more about life, its strategies and its boundaries than other groups of organisms. The Atacama Desert (North Chile) holds two world records of extreme environmental characteristics: the lowest rainfall and greatest surface ultraviolet radiation and total solar irradiance ever measured on Earth. Despite these limiting conditions for life, we recently identified several remarkable examples of endolithic habitats colonized by phototrophic and heterotrophic microorganisms in the hyperarid core of the Atacama Desert.

Introduction

The combined extreme environmental conditions of the hyperarid desert give rise to perhaps the harshest setting faced by microbial life. As such, desert microbial ecosystems are excellent models to address the environmental selection of a terrestrial biome and the limits of life on our planet. The aridity of the desert environment implies a scarcity of water. Water is the single most important requirement for life on Earth, and theoretically, there is a threshold in the natural environment  the dry limit  where liquid water is too scarce for the full range of necessary functions required to sustain viable populations of organisms. Thus, some known environments exist with multiple and/or simultaneous forms of stress that will determine the limits of life. These environments can be considered as polyextreme as they could be inhabited by polyextremophilic and/or polyextremotolerant (sensu McElroy [1]) microorganisms. Polyextreme environments could thus be optimal models for the study of the multiple biochemical survival mechanisms and resistance strategies of their inhabitants.

This report reviews the endolithic microbial communities discovered in the past decade within the hyperarid core of the Atacama Desert. We excluded the microbial communities of the Pacific Coastal Cordillera, as this zone receives significant fog and humid air, along with the soil biome, because of its abiotic nature [2, 3, 4]. After an initial description of the polyextreme environment of this desert, we focus on its endolithic microbial habitats and the structure, diversity and adaptation strategies of their colonizing endoliths.

Section snippets

The Atacama Desert as Earth's most polyextreme environment

Among others deserts, the Atacama Desert (North Chile) is perhaps the most challenging polyextreme environment on Earth and the most barren region imaginable. Until 2006 it was thought that the hyperarid core of this desert was devoid of photosynthetic life [5]. This hyperarid core lies between 20°S and 24°S, between the Pacific Coastal Range and the Andean Altiplano, and is known as the driest places on our planet [6], its rainfall being 3–27 mm y−1 [7, 8•]. Further, this desert holds another

Endolithic habitats in the hyperarid zone

The first evidence of an endolithic microbial community in the hyperarid core of the Atacama Desert was the discovery of exceptional cryptoendolithic colonization within the halite (NaCl) rocks of the Yungay area [16], considered one of the most hyperarid zones of this desert. This colonization takes place just a few millimeters beneath the rock surface, occupying spaces among salt crystals (Figure 2a–c). Liquid water, in the form of NaCl saturated brine appears within these rocks due to

Diversity and functioning of endolithic microbial communities

Different endolithic associations in the hyperarid core of the Atacama Desert have been reported from several substrates where distinct communities occur. Halite nodules in details described by Artieda et al. [32] harbor a unique community that reflects the adaptation of its members to high-salt conditions. Metagenomic analysis revealed the composition of this association: archaea (80%), bacteria (20%) and eukarya (1%) barely represented in Salar Grande [14, 33••], Salar de Llamara [27], Salar

Adaptation strategies of Atacama's endoliths to the polyextreme environment

It is well known that phototrophic microorganisms engage in self-protection via the synthesis and build-up of secondary metabolites. This likely produces a shielding effect that prevents photoinhibition and lethal photooxidative damage. Works by Wierzchos et al. [8] and Vítek et al. [41] based on spectrometry and Raman spectroscopy have shown distinctly enhanced carotenoid pigments (xanthophylls) and abundant lipid production within endolithic microalgae cells lying close to the gypcrete

Concluding remarks

Atacama's endoliths are low-complexity microbial communities dominated by primary producers, such as Cyanobacteria, mostly of the Chroococcidiopsis genus, and the phyla Actinobacteria, Proteobacteria, Chloroflexi, Bacterioidetes, and Euryarchaeota as well as other heterotrophic microorganisms, and specifically adapted to this polyextreme environment. Their composition is influenced by substrate architecture, which is a key factor in water availability and light intensity. However, these issues

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors wish to thank J. DiRuggiero, P. Vítek, V. B. Gomez-Silva, V. Meslier and A. F. Davila for contribution in previous common articles and valuable conversations and scientific debates also during common expeditions to the Atacama Desert. We also thank the MNCN  CSIC Microscopy Service staff and V. Souza-Egipsy (Inst. Estructura de la Materia  CSIC, Madrid), I. Sanchez Almagro (CIC  Univ. Granada) and M. Roldán (Univ. Autonoma, Barcelona) for technical assistance and Ana Burton for

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