Endolithic microbial habitats as refuges for life in polyextreme environment of the Atacama Desert
Graphical abstract
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
References (49)
- et al.
Life at the dry edge: microorganisms of the Atacama Desert
FEBS Lett
(2012) - et al.
Moisture activation and carbon use efficiency of soil microbial communities along an aridity gradient in the Atacama Desert
Soil Biol Biochem
(2018) - et al.
Microbial colonisation of chasmoendolithic habitats in the hyper-arid zone of the Atacama Desert
Biogeosciences
(2013) - et al.
Discovery of carotenoid red-shift in endolithic cyanobacteria from the Atacama Desert
Sci Rep
(2017) - et al.
Cyanobacterial photoprotection by the orange carotenoid protein
Nat Plants
(2016) Some comments on the evolution of extremophiles
Biosystems
(1974)- et al.
Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life
Science
(2003) - et al.
Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert
Microb Ecol
(2006) - et al.
Discovery and microbial content of the driest site of the hyperarid Atacama Desert, Chile
Environ Microbiol Rep
(2015) - et al.
Temperature and moisture conditions for life in the of observations including the El Niño of 1997–1998
Astrobiology
(2003)
Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the Atacama Desert
Front Microbiol
The Atacama surface solar maximum
Bull Am Meteorol Soc
The world's highest levels of surface UV
Photochem Photobiol Sci
Record solar UV irradiance in the tropical Andes
Front Environ Sci
Microbial colonization and controls in dryland systems
Nat Rev Microbiol
Microorganisms in desert rocks: the edge of life on Earth
Int Microbiol
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
Environ Microbiol
Comparative analysis of the microbial communities inhabiting halite evaporites of the Atacama Desert
Int Microbiol
Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert
Astrobiology
Microbial colonization of the salt deposits in the driest place of the Atacama Desert (Chile)
Orig Life Evol Biosph
Endolithnic cyanobacteria in soil gypsum: occurences in Atacama (Chile), Mojave (United States), and Al-Jafr Basin (Jordan) Deserts
J Geophys Res G Biogeosci
Microbial colonization of Ca-sulfate crusts in the hyperarid core of the Atacama Desert: implications for the search for life on Mars
Geobiology
Ignimbrite as a substrate for endolithic life in the hyper-arid Atacama Desert: implications for the search for life on Mars
Icarus
A preliminary survey of non-lichenized fungi cultured from the hyperarid Atacama Desert of Chile
Astrobiology
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