Lithobiontic life: “Atacama rocks are well and alive”

Our knowledge on the Microbiology of the Atacama Desert has increased steadily and substantially during the last two decades. This information now supports a paradigmatic change on the Atacama Desert from a sterile, uninhabitable territory to a hyperarid region colonized by a rich microbiota that includes extremophiles and extreme-tolerant microorganisms. Also, extensive reports are available on the prevalent physical and chemical environmental conditions, ecological niches and, the abundance, diversity and organization of the microbial life in the Atacama Desert. This territory is a highly desiccated environment due to the absence of regular rain events. Liquid water scarcity is the most serious environmental factor affecting the Atacama Desert microorganisms. The intense solar irradiation in this region contributes, in a synergistic fashion with desiccation, to limit the survival and growth of the microbial life. In order to overcome these two extreme conditions, successful microorganisms, organized as microbial consortia, take advantage of (a) the physical characteristics of lithic habitats, which provide sites for colonization on, within or below the rock substrate, the attenuation and filtration of the intense solar irradiation and, the collection of liquid water from incoming fog formations and by water vapour condensation and deliquescence on or within their surfaces, and (b) the biological adaptations of members of the microbial communities that allow them to synthesize hydrophilic macromolecules, antioxidants and UV-light absorbents. Lithic habitats have been considered specialized shelters where life forms can reach protection at environments subjected to extremes of desiccation and solar irradiation, here on Earth or elsewhere. This review is an overview of part of the scientific information collected on lithobionts from the Atacama Desert, their rock substrates and their strategies to cope with extremes of desiccation and intense photosynthetic active radiation and UV irradiations.     

Microbiology of hyper-arid environments: recent insights from the Atacama Desert, Chile

Interests in the Atacama Desert of northern Chile until very recently were founded on its mineral resources, notably nitrate, copper, lithium and boron. Now this vast desert, the oldest and most arid on Earth, is revealing a microbial diversity that was unimagined even a decade or so ago; indeed the extreme hyper-arid core of the Desert was considered previously to be completely devoid of life. In this Perspective article we highlight pioneering research that, to the contrary, establishes the Atacama as a combination of rich microbial habitats including bacteria that influence biogeochemical transformations in the desert and others that are propitious sources of novel natural products. Many of the Atacama’s habitats are especially rich in actinobacteria, not necessarily as dense populations but extensive in taxonomic diversity and capacities to synthesize novel secondary metabolites. Among the latter, compounds have been characterized that express a range of antibiotic, anti-cancer and anti- inflammatory properties to which a variety of bioinformatics and metabolic engineering tools are being applied in order to enhance potencies and productivities. Unquestionably the Atacama Desert is a living desert with regard to which future microbiology and biotechnology research presents exciting opportunities.     

Historical and ecological divergence among populations of Monttea chilensis (Plantaginaceae), an endemic endangered shrub bordering the Atacama Desert,Chile

The coastal deserts of northern Chile show an important latitudinal gradient of aridity with more arid areas to the north of the Atacama Desert than to the south. Several plant species have disjunct distributions that correspond with the extremes of this latitudinal gradient. In this study, using genetic (chloroplast and nuclear DNA), morphological (vegetative and floral traits of various kinds) and climatic and topographic information, we explored ecological and historical events that have putatively shaped patterns of variation among Monttea chilensis populations—a species that shows this disjunct distribution. Through phylogeographic and phylogenetic analyses, two divergent lineages were identified located at the latitudinal extremes. The lineage located northern lineage (NG) of the Atacama Desert showed more genetic diversity and better-resolved phylogeographic structure than the southern lineage (SG). Considerable morphological variation across the geographical range corresponds with these genetic groups. We observed contrasting relationships between floral and vegetative traits: populations from the most arid region NG possessed larger flowers, but smaller vegetative values, and vice versa. Niche modelling and multivariate analyses, including environmental data, revealed different environmental requirements for each lineage. NG plants occur in regions with warmer and drier climatic conditions and at higher altitudes, while SG populations inhabit colder and more humid environments and lower altitudes. The evolutionary history of M. chilensis exhibits a phylogeographical footprint consistent with past fragmentation and allopatric differentiation, where the hyper-arid zone formed by the Atacama Desert clearly acted as an important gene flow barrier. This barrier has led to considerable differentiation in morphology and ecology, resulting in two ecotypes or geographical races, suggesting incipient speciation promoted by local adaptation and geographical isolation.     

Natural product diversity of actinobacteria in the Atacama Desert

The Atacama Desert of northern Chile is considered one of the most arid and extreme environment on Earth. Its core region was described as featuring “Mars-like” soils that were at one point deemed too extreme for life to exist. However, recent investigations confirmed the presence of diverse culturable actinobacteria. In the current review, we discuss a total of 46 natural products isolated to date representing diverse chemical classes characterized from different actinobacteria isolated from various locations in the Atacama Desert. Their reported biological activities are also discussed.     

Determination of low bacterial concentrations in hyperarid Atacama soils: comparison of biochemical and microscopy methods with real-time quantitative PCR

Hyperarid Atacama soils are reported to contain significantly reduced numbers of microbes per gram of soil relative to soils from other environments. Molecular methods have been used to evaluate microbial populations in hyperarid Atacama soils; however, conflicting results across the various studies, possibly caused by this low number of microorganisms and consequent biomass, suggest that knowledge of expected DNA concentrations in these soils becomes important to interpreting data from any method regarding microbial concentrations and diversity. In this paper we compare the number of bacteria per gram of Atacama Desert soils determined by real-time quantitative polymerase chain reaction with the number of bacteria estimated by the standard methods of phospholipids fatty acid analysis, adenine composition (determined by liquid chromatography - time-of-flight mass spectrometry), and SYBR-green microscopy. The number determined by real-time quantitative polymerase chain reaction as implemented in this study was several orders of magnitude lower than that determined by the other three methods and probably underestimates the concentrations of soil bacteria, most likely because of soil binding during the DNA extraction methods. However, the other methods very possibly overestimate the bacteria concentrations owing to desiccated, intact organisms, which would stain positive in microscopy and preserve both adenine and phospholipid fatty acid for the other methods.     

Ancient Photosynthetic Eukaryote Biofilms in an Atacama Desert Coastal Cave

Caves offer a stable and protected environment from harsh and changing outside prevailing conditions. Hence, they represent an interesting habitat for studying life in extreme environments. Here, we report the presence of a member of the ancient eukaryote red algae Cyanidium group in a coastal cave of the hyperarid Atacama Desert. This microorganism was found to form a seemingly monospecific biofilm growing under extremely low photon flux levels. Our work suggests that this species, Cyanidium sp. Atacama, is a new member of a recently proposed novel monophyletic lineage of mesophilic “cave” Cyanidium sp., distinct from the remaining three other lineages which are all thermo-acidophilic. The cave described in this work may represent an evolutionary island for life in the midst of the Atacama Desert.     

Geology and geochemistry of the Atacama Desert

The Atacama Desert, the driest of its kind on Earth, hosts a number of unique geological and geochemical features that make it unlike any other environment on the planet. Considering its location on the western border of South America, between 17 and 28 °S, its climate has been characterized as arid to hyperarid for at least the past 10 million years. Notably dry climatic conditions of the Atacama Desert have been related to uplift of the Andes and are believed to have played an important role in the development of the most distinctive features of this desert, including: (i) nitrates and iodine deposits in the Central Depression, (ii) secondary enrichment in porphyry copper deposits in the Precordillera, (iii) Li enrichment in salt flats of the Altiplano, and (iv) life in extreme habitats. The geology and physiography of the Atacama Desert have been largely shaped by the convergent margin present since the Mesozoic era. The geochemistry of surface materials is related to rock geochemistry (Co, Cr, Fe, Mn, V, and Zn), salt flats, and evaporite compositions in endorheic basins (As, B, and Li), in addition to anthropogenic activities (Cu, Mo, and Pb). The composition of surface water is highly variable, nonetheless in general it presents a circumneutral pH with higher conductivity and total dissolved solids in brines. Major water constituents, with the exception of HCO₃^?, are generally related to the increase of salinity, and despite the fact that trace elements are not well-documented, surface waters of the Atacama Desert are enriched in As, B, and Li when compared to the average respective concentrations in rivers worldwide.     

Ultraviolet radiation in the Atacama Desert

The world’s highest levels of surface ultraviolet (UV) irradiance have been measured in the Atacama Desert. This area is characterized by its high altitude, prevalent cloudless conditions, and a relatively low total ozone column. In this paper, we provide estimates of the surface UV (monthly UV index at noon and annual doses of UV-B and UV-A) for all sky conditions in the Atacama Desert. We found that the UV index at noon during the austral summer is expected to be greater than 11 in the whole desert. The annual UV-B (UV-A) doses were found to range from about 3.5 kWh/m² (130 kWh/m²) in coastal areas to 5 kWh/m² (160 kWh/m²) on the Andean plateau. Our results confirm significant interhemispherical differences. Typical annual UV-B doses in the Atacama Desert are about 40% greater than typical annual UV-B doses in northern Africa. Mostly due to seasonal changes in the ozone, the differences between the Atacama Desert and northern Africa are expected to be about 60% in the case of peak UV-B levels (i.e. the UV-B irradiances at noon close to the summer solstice in each hemisphere). Interhemispherical differences in the UV-A are significantly lower since the effect of the ozone in this part of the spectrum is minor.     

Fungal diversity in the Atacama Desert

Fungi are generally easily dispersed, able to colonise a wide variety of substrata and can tolerate diverse environmental conditions. However, despite these abilities, the diversity of fungi in the Atacama Desert is practically unknown. Most of the resident fungi in desert regions are ubiquitous. Some of them, however, seem to display specific adaptations that enable them to survive under the variety of extreme conditions of these regions, such as high temperature, low availability of water, osmotic stress, desiccation, low availability of nutrients, and exposure to high levels of UV radiation. For these reasons, fungal communities living in the Atacama Desert represent an unknown part of global fungal diversity and, consequently, may be source of new species that could be potential sources for new biotechnological products. In this review, we focus on the current knowledge of the diversity, ecology, adaptive strategies, and biotechnological potential of the fungi reported in the different ecosystems of the Atacama Desert.     

Validation of a Clostridium endospore viability assay and analysis of Greenland ices and Atacama Desert soils

A microscopy-based endospore viability assay (micro-EVA) capable of enumerating germinable Clostridium endospores (GCEs) in less than 30 min has been validated and employed to determine GCE concentrations in Greenland ices and Atacama Desert soils. Inoculation onto agarose doped with Tb(3+) and d-alanine triggers Clostridium spore germination and the concomitant release of ～10(8) molecules of dipicolinic acid (DPA) per endospore, which, under pulsed UV excitation, enables enumeration of resultant green Tb(3+)-DPA luminescent spots as GCEs with time-gated luminescence microscopy. The intensity time courses of the luminescent spots were characteristic of stage I Clostridium spore germination dynamics. Micro-EVA was validated against traditional CFU cultivation from 0 to 1,000 total endospores/ml (i.e., phase-bright bodies/ml), yielding 56.4% ± 1.5% GCEs and 43.0% ± 1.0% CFU. We also show that d-alanine serves as a Clostridium-specific germinant (three species tested) that inhibits Bacillus germination of spores (five species tested) in that endospore concentration regime. Finally, GCE concentrations in Greenland ice cores and Atacama Desert soils were determined with micro-EVA, yielding 1 to 2 GCEs/ml of Greenland ice (versus <1 CFU/ml after 6 months of incubation) and 66 to 157 GCEs/g of Atacama Desert soil (versus 40 CFU/g soil).     

Microbial colonization of the salt deposits in the driest place of the Atacama Desert (Chile)

The Atacama Desert (Chile), one of the most arid places on Earth, shows hostile conditions for the development of epilithic microbial communities. In this study, we report the association of cyanobacteria (Chroococcidiopsis sp.) and bacteria belonging to Actinobacteria and Beta-Gammaproteobacteria and Firmicutes phyla inhabiting the near surface of salt (halite) deposits of the Salar Grande Basin, Atacama Desert (Chile). The halite deposits were investigated by using optical, confocal and field emission scanning electron microscopes, whereas culture-independent molecular techniques, 16S rDNA clone library, alongside RFLP analysis and 16S rRNA gene sequencing were applied to investigate the bacterial diversity. These microbial communities are an example of life that has adapted to extreme environmental conditions caused by dryness, high irradiation, and metal concentrations. Their adaptation is, therefore, important in the investigation of the environmental conditions that might be expected for life outside of Earth.     

A forest‐specialist carnivore in the middle of the desert?Comments on Anabalon et al. 2019

We present comments on an article recently published in Ecology and Evolution (“High‐resolution melting of the cytochrome B gene in fecal DNA: A powerful approach for fox species identification of the Lycalopex genus in Chile”) by Anabalon et al. that reported the presence of Darwin's fox (Lycalopex fulvipes), a temperate forest specialist, in the hyperarid Atacama Desert of northern Chile. We argue that this putative record lacks ecological support in light of ongoing research on this endangered species, and contains numerous methodological flaws and omissions related to the molecular identification of the species. Based on these issues, we suggest the scientific community and conservation decision‐makers disregard the alleged presence of the Darwin's fox in the Atacama Desert.     

A comparative analysis of gaseous phase hydration properties of two lichenized fungi: Niebla tigrina (Follman) Rundel & Bowler from Atacama Desert and Umbilicaria antarctica Frey & I. M. Lamb from Robert Island,Southern Shetlands Archipelago,maritime Antarctica

Extremophiles - Gaseous phase hydration properties for thalli of Niebla tigrina from Atacama Desert, and for Umbilicaria antarctica from Isla Robert, maritime Antarctica, were analyzed using 1H-NMR...     

Phylogenetic Profiling and Diversity of Bacterial Communities in the Death Valley,an Extreme Habitat in the Atacama Desert

The Atacama Desert, one of the driest deserts in the world, represents a unique extreme environmental ecosystem to explore the bacterial diversity as it is considered to be at the dry limit for life. A 16S rRNA gene (spanning the hyper variable V3 region) library was constructed from an alkaline sample of unvegetated soil at the hyperarid margin in the Atacama Desert. A total of 244 clone sequences were used for MOTHUR analysis, which revealed 20 unique phylotypes or operational taxonomic units (OTUs). V3 region amplicons of the 16S rRNA were suitable for distinguishing the bacterial community to the genus and specie level. We found that all OTUs were affiliated with taxa representative of the Firmicutes phylum. The extremely high abundance of Firmicutes indicated that most bacteria in the soil were spore-forming survivors. In this study we detected a narrower diversity as compared to other ecological studies performed in other areas of the Atacama Desert. The reported genera were Oceanobacillus (representing the 69.5 % of the clones sequenced), Bacillus, Thalassobacillus and Virgibacillus. The present work shows physical and chemical parameters have a prominent impact on the microbial community structure. It constitutes an example of the communities adapted to live in extreme conditions caused by dryness and metal concentrations .

Electronic supplementary material

The online version of this article (doi:10.1007/s12088-015-0539-3) contains supplementary material, which is available to authorized users.     

Life at the dry edge: Microorganisms of the Atacama Desert

The Atacama Desert, located in northern Chile, is the driest and oldest Desert on Earth. Research aimed at the understanding of this unique habitat and its diverse microbial ecosystems begun only a few decades ago, mainly driven by NASA's astrobiology program. A milestone in these efforts was a paper published in 2003, when the Atacama was shown to be a proper model of Mars. From then on, studies have been focused to examine every possible niche suitable for microbial life in this extreme environment. Habitats as different as the underside of quartz rocks, fumaroles at the Andes Mountains, the inside of halite evaporates and caves of the Coastal Range, among others, have shown that life has found ingenious ways to adapt to extreme conditions such as low water availability, high salt concentration and intense UV radiation.     

Desert breath—How fog promotes a novel type of soil biocenosis,forming the coastal Atacama Desert’s living skin

The Atacama Desert is the driest non‐polar desert on Earth, presenting precarious conditions for biological activity. In the arid coastal belt, life is restricted to areas with fog events that cause almost daily wet–dry cycles. In such an area, we discovered a hitherto unknown and unique ground covering biocenosis dominated by lichens, fungi, and algae attached to grit‐sized (~6 mm) quartz and granitoid stones. Comparable biocenosis forming a kind of a layer on top of soil and rock surfaces in general is summarized as cryptogamic ground covers (CGC) in literature. In contrast to known CGC from arid environments to which frequent cyclic wetting events are lethal, in the Atacama Desert every fog event is answered by photosynthetic activity of the soil community and thus considered as the desert's breath. Photosynthesis of the new CGC type is activated by the lowest amount of water known for such a community worldwide thus enabling the unique biocenosis to fulfill a variety of ecosystem services. In a considerable portion of the coastal Atacama Desert, it protects the soil from sporadically occurring splash erosion and contributes to the accumulation of soil carbon and nitrogen as well as soil formation through bio‐weathering. The structure and function of the new CGC type are discussed, and we suggest the name grit–crust. We conclude that this type of CGC can be expected in all non‐polar fog deserts of the world and may resemble the cryptogam communities that shaped ancient Earth. It may thus represent a relevant player in current and ancient biogeochemical cycling.     

Disrupted phylogeographical microsatellite and chloroplast DNA patterns indicate a vicariance rather than long‐distance dispersal origin for the disjunct distribution of the Chilean endemic Dioscorea biloba (Dioscoreaceae) around the Atacama Desert

Aim The Chilean endemic Dioscorea biloba (Dioscoreaceae) is a dioecious geophyte that shows a remarkable 600 km north–south disjunction in the peripheral arid area of the Atacama Desert. Its restricted present‐day distribution and probable Neogene origin indicate that its populations have a history linked to that of the Atacama Desert, making this an ideal model species with which to investigate the biogeography of the region. Location Chile, Atacama Desert and peripheral arid area. Methods Two hundred and seventy‐five individuals from nine populations were genotyped for seven nuclear microsatellite loci, and plastid trnL–F and trnT–L sequences were obtained for a representative subset of these. Analyses included the estimation of genetic diversity and population structure through clustering, Bayesian and analysis of molecular variance analyses, and statistical parsimony networks of chloroplast haplotypes. Isolation by distance was tested against alternative dispersal hypotheses. Results Microsatellite markers revealed moderate to high levels of genetic diversity within populations, with those from the southern Limarí Valley showing the highest values and northern populations showing less exclusive alleles. Bayesian analysis of microsatellite data identified three genetic groups that corresponded to geographical ranges. Chloroplast phylogeography revealed no haplotypes shared between northern and southern ranges, and little haplotype sharing between the two neighbouring southern valleys. Dispersal models suggested the presence of extinct hypothetical populations between the southern and northern ranges. Main conclusions Our results are consistent with prolonged isolation of the northern and southern groups, mediated by the life‐history traits of the species. Significant isolation was revealed at both large and moderate distances as gene flow was not evident even between neighbouring valleys. Bayesian analyses of microsatellite and chloroplast haplotype diversity identified the southern area of Limarí as the probable area of origin of the species. Our data do not support recent dispersal of D. biloba from the southern range into Antofagasta, but indicate the fragmentation of an earlier wider range, concomitant with the Pliocene–Pleistocene climatic oscillations, with subsequent extinctions of the Atacama Desert populations and the divergence of the peripheral ones as a consequence of genetic drift.     

Phylogenetic and biogeographic relationships of the mouse opossum Thylamys (Didelphimorphia,Didelphidae) in southern South America

Nucleotide sequence data from the mitochondrial cytochrome b gene were used to evaluate the phylogenetic relationships among mouse opossum species of the genus Thylamys. Based on approximately 1000 bp in five of the six species of the genus and including different localities for some of the species, we concluded that T. macrura from the subtropical forests of eastern Paraguay is the most primitive taxon. Subsequent radiation of the genus is explained mainly via founder effect speciation. This evolutionary scenario would account for the speciation of T. pusilla, T. venusta, T. pallidior, and T. elegans in the Chaco, southern Bolivia and northern Argentina, the Andean Altiplano, the Coastal Desert of Chile, and coastal Perú, respectively. Calibration of a molecular clock set the Pleistocene as the period for the differentiation of Thylamys species. The molecular results confirm the strong genetic connection between populations that inhabit the "pre-cordillera" of northern Chile (T. pallidior) and the canyons that run through the Atacama Desert to the lowlands in northern Chile. Our results confirm the occurrence of two Thylamys species in Chile, T. pallidior and T. elegans, within and south to the Atacama Desert, respectively.