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.     

Isolation of UVC-Tolerant Bacteria from the Hyperarid Atacama Desert, Chile

Martian surface microbial inhabitants would be challenged by a constant and unimpeded flux of UV radiation, and the study of analog model terrestrial environments may be of help to understand how such life forms could survive under this stressful condition. One of these environments is the Atacama Desert (Chile), a well-known Mars analog due to its extreme dryness and intense solar UV radiation. Here, we report the microbial diversity at five locations across this desert and the isolation of UVC-tolerant microbial strains found in these sites. Denaturing gradient gel electrophoresis (DGGE) of 16S rDNA sequences obtained from these sites showed banding patterns that suggest distinct and complex microbial communities. Analysis of 16S rDNA sequences obtained from UV-tolerant strains isolated from these sites revealed species related to the Bacillus and Pseudomonas genera. Vegetative cells of one of these isolates, Bacillus S3.300-2, showed the highest UV tolerance profile (LD₁₀?=?318 J?m²), tenfold higher than a wild-type strain of Escherichia coli. Thus, our results show that the Atacama Desert harbors a noteworthy microbial community that may be considered for future astrobiological-related research in terms of UV tolerance.     

Rare taxa and dark microbial matter: novel bioactive actinobacteria abound in Atacama Desert soils

An “in house” taxonomic approach to drug discovery led to the isolation of diverse actinobacteria from hyper-arid, extreme hyper-arid and very high altitude Atacama Desert soils. A high proportion of the isolates were assigned to novel taxa, with many showing activity in standard antimicrobial plug assays. The application of more advanced taxonomic and screening strategies showed that strains classified as novel species of Lentzea and Streptomyces synthesised new specialised metabolites thereby underpinning the premise that the extreme abiotic conditions in the Atacama Desert favour the development of a unique actinobacterial diversity which is the basis of novel chemistry. Complementary metagenomic analyses showed that the soils encompassed an astonishing degree of actinobacterial ‘dark matter’, while rank-abundance analyses showed them to be highly diverse habitats mainly composed of rare taxa that have not been recovered using culture-dependent methods. The implications of these pioneering studies on future bioprospecting campaigns are discussed.     

Introducing the Atacama Desert

This brief introduction is intended to orientate the reader with respect to the principal environmental and historical features of the Atacama Desert, the oldest and continuously driest non-polar temperate desert on Earth. Exploration of its microbiology is relatively recent but both fundamental and applied research activities have grown dramatically in recent years reflecting the substantial interest in its microbial diversity, ecology, biogeochemistry, natural product potential and Mars-analogue properties of this unique and invigorating environment.     

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.     

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.     

Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert,Chile

The Atacama Desert presents one of the most extreme environments on Earth and we report here the first extensive isolations of actinomycetes from soils at various locations within the Desert. The use of selective isolation procedures enabled actinomycetes to be recovered from arid, hyper-arid and even extreme hyper-arid environments in significant numbers and diversity. In some cases actinomycetes were the only culturable bacteria to be isolated under the conditions of this study. Phylogenetic analysis and some phenotypic characterisation revealed that the majority of isolates belonged to members of the genera Amycolatopsis, Lechevalieria and Streptomyces, a high proportion of which represent novel centres of taxonomic variation. The results of this study support the view that arid desert soils constitute a largely unexplored repository of novel bacteria, while the high incidence of non-ribosomal peptide synthase genes in our isolates recommend them as promising material in screening for new bioactive natural products.     

Bacterial Community Structure in the Hyperarid Core of the Atacama Desert, Chile

Soils from the hyperarid Atacama Desert of northern Chile were sampled along an east-west elevational transect (23.75 to 24.70°S) through the driest sector to compare the relative structure of bacterial communities. Analysis of denaturing gradient gel electrophoresis (DGGE) profiles from each of the samples revealed that microbial communities from the extreme hyperarid core of the desert clustered separately from all of the remaining communities. Bands sequenced from DGGE profiles of two samples taken at a 22-month interval from this core region revealed the presence of similar populations dominated by bacteria from the Gemmatimonadetes and Planctomycetes phyla.     

Metabolic modelling and flux analysis of microorganisms from the Atacama Desert used in biotechnological processes

Metabolic modelling is a useful tool that enables the rational design of metabolic engineering experiments and the study of the unique capabilities of biotechnologically important microorganisms. The extreme abiotic conditions of the Atacama Desert have selected microbial diversity with exceptional characteristics that can be applied in the mining industry for bioleaching processes and for production of specialised metabolites with antimicrobial, antifungal, antiviral, antitumoral, among other activities. In this review we summarise the scientific data available of the use of metabolic modelling and flux analysis to improve the performance of Atacama Desert microorganisms in biotechnological applications.     

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.     

A novel subaerial Dunaliella species growing on cave spiderwebs in the Atacama Desert

Strategies for life adaptation to extreme environments often lead to novel solutions. As an example of this assertion, here we describe the first species of the well-known genus of green unicellular alga Dunaliella able to thrive in a subaerial habitat. All previously reported members of this microalga are found in extremely saline aquatic environments. Strikingly, the new species was found on the walls of a cave located in the Atacama Desert (Chile). Moreover, on further inspection we noticed that it grows upon spiderwebs attached to the walls of the entrance-twilight transition zone of the cave. This peculiar growth habitat suggests that this Dunaliella species uses air moisture condensing on the spiderweb silk threads as a source of water for doing photosynthesis in the driest desert of the world. This process of adaptation recapitulates the transition that allowed land colonization by primitive plants and shows an unexpected way of expansion of the life habitability range by a microbial species.     

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.     

Nest placement and nesting success in two finch species colonizing a recently established plantation in an arid region

This study examines variations in nest placement and its effects on nesting success in the Desert Finch (Rhodospiza obsoleta) and the Linnet (Carduelis cannabina) which coexist in a recently established plantation (novel habitat) in a desert region in Jordan. A comparison with other habitats (old plantation in the desert and native, Mediterranean-type, habitat of the Linnet) showed that each species displayed similarity in nest placement patterns across habitats. Nest concealment predicted nesting outcome in the Linnet, whereas nest height predicted nesting outcome in the Desert Finch. Daily survival rates were significantly higher in Desert Finch nests compared to the Linnet's, perhaps because Desert Finches placed nests higher in the novel habitat, which lacked aerial nest predators. In accordance with predation theories of life history evolution, we provide evidence that variation in nest placement among the two species in a novel habitat resulted from previous exposure to different predation risks.     

Microbial community composition and trophic role along a marked salinity gradient in Laguna Puilar,Salar de Atacama,Chile

The geological, hydrological and microbiological features of the Salar de Atacama, the most extensive evaporitic sedimentary basin in the Atacama Desert of northern Chile, have been extensively studied. In contrast, relatively little attention has been paid to the composition and roles of microbial communities in hypersaline lakes which are a unique feature in the Salar. In the present study biochemical, chemical and molecular biological tools were used to determine the composition and roles of microbial communities in water, microbial mats and sediments along a marked salinity gradient in Laguna Puilar which is located in the “Los Flamencos” National Reserve. The bacterial communities at the sampling sites were dominated by members of the phyla Bacteroidetes, Chloroflexi, Cyanobacteria and Proteobacteria. Stable isotope and fatty acid analyses revealed marked variability in the composition of microbial mats at different sampling sites both horizontally (at different sites) and vertically (in the different layers). The Laguna Puilar was shown to be a microbially dominated ecosystem in which more than 60% of the fatty acids at particular sites are of bacterial origin. Our pioneering studies also suggest that the energy budgets of avian consumers (three flamingo species) and dominant invertebrates (amphipods and gastropods) use minerals as a source of energy and nutrients. Overall, the results of this study support the view that the Salar de Atacama is a heterogeneous and fragile ecosystem where small changes in environmental conditions may alter the balance of microbial communities with possible consequences at different trophic levels.     

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.     

Microbial colonization of Ca‐sulfate crusts in the hyperarid core of the Atacama Desert: implications for the search for life on Mars

The scarcity of liquid water in the hyperarid core of the Atacama Desert makes this region one of the most challenging environments for life on Earth. The low numbers of microbial cells in the soils suggest that within the Atacama Desert lies the dry limit for life on our planet. Here, we show that the Ca‐sulfate crusts of this hyperarid core are the habitats of lithobiontic micro‐organisms. This microporous, translucent substrate is colonized by epilithic lichens, as well as endolithic free‐living algae, fungal hyphae, cyanobacteria and non photosynthetic bacteria. We also report a novel type of endolithic community, “hypoendoliths”, colonizing the undermost layer of the crusts. The colonization of gypsum crusts within the hyperarid core appears to be controlled by the moisture regime. Our data shows that the threshold for colonization is crossed within the dry core, with abundant colonization in gypsum crusts at one study site, while crusts at a drier site are virtually devoid of life. We show that the cumulative time in 1 year of relative humidity (RH) above 60% is the best parameter to explain the difference in colonization between both sites. This is supported by controlled humidity experiments, where we show that colonies of endolithic cyanobacteria in the Ca‐sulfate crust undergo imbibition process at RH >60%. Assuming that life once arose on Mars, it is conceivable that Martian micro‐organisms sought refuge in similar isolated evaporite microenvironments during their last struggle for life as their planet turned arid.     

Strong genetic differentiation in the invasive annual grass <Emphasis Type="Italic">Bromus tectorum</Emphasis> across the Mojave–Great Basin ecological transition zone

Bromus tectorum, an inbreeding annual grass, is a dominant invader in sagebrush steppe habitat in North America. It is also common in warm and salt deserts, displaying a larger environmental tolerance than most native species. We tested the hypothesis that a suite of habitat-specific B. tectorum lineages dominates warm desert habitats. We sampled 30 B. tectorum Mojave Desert and desert fringe populations and genotyped 10–26 individuals per population using 69 single nucleotide polymorphic (SNP) markers. We compared these populations to 11 Great Basin steppe and salt desert populations. Populations from warm desert habitats were dominated by members of two haplogroups (87 % of individuals) that were distinct from haplogroups common in Great Basin habitats. We conducted common garden studies comparing adaptive traits and field performance among haplogroups typically found in different habitats. In contrast to the haplogroup abundant in sagebrush steppe, warm desert haplogroups generally lacked a vernalization requirement for flowering. The most widespread warm desert haplogroup (Warm Desert 1) also had larger seeds and a higher root:shoot ratio than other haplogroups. In the field, performance of warm desert haplogroups was dramatically lower than the sagebrush steppe haplogroup at one steppe site, but one warm desert haplogroup performed as well as the steppe haplogroup under drought conditions at the other site. Our results suggest that B. tectorum succeeds in widely disparate environments through ecotypic variation displayed by distinct lineages of plants. Accounting for this ecotypic variation is essential in modeling its future distribution in response to climate change.     

Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence,regional expansion and asymmetric gene flow

The complex interactions of historical, geological and climatic events on plant evolution have been an important research focus for many years. However, the role of desert formation and expansion in shaping the genetic structures and demographic histories of plants occurring in arid areas has not been well explored. In the present study, we investigated the phylogeography of Arnebia szechenyi, a desert herb showing a near-circular distribution surrounding the Tengger Desert in Northwest China. We measured genetic diversity of populations using three maternally inherited chloroplast DNA (cpDNA) fragments and seven bi-paternally inherited nuclear DNA (nDNA) loci that were sequenced from individuals collected from 16 natural populations across its range and modelled current and historical potential habitats of the species. Our data indicated a considerably high level of genetic variation within A. szechenyi and noteworthy asymmetry in historical migration from the east to the west. Moreover, two nuclear genetic groups of populations were revealed, corresponding to the two geographic regions separated by the Tengger Desert. However, analysis of cpDNA data did not show significant geographic structure. The most plausible explanation for the discrepancy between our findings based on cpDNA and nDNA data is that A. szechenyi populations experienced long periods of geographic isolation followed by range expansion, which would have promoted generalized recombination of the nuclear genome. Our findings further highlight the important role that the Tengger Desert, together with the Helan Mountains, has played in the evolution of desert plants and the preservation of biodiversity in arid Northwest China.     

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.     

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.