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.     

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.     

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.     

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.     

An Unusual Inverted Saline Microbial Mat Community in an Interdune Sabkha in the Rub' al Khali (the Empty Quarter), United Arab Emirates

Salt flats (sabkha) are a recognized habitat for microbial life in desert environments and as analogs of habitats for possible life on Mars. Here we report on the physical setting and microbiology of interdune sabkhas among the large dunes in the Rub'' al Khali (the Empty Quarter) in Liwa Oasis, United Arab Emirates. The salt flats, composed of gypsum and halite, are moistened by relatively fresh ground water. The result is a salinity gradient that is inverted compared to most salt flat communities with the hypersaline layer at the top and freshwater layers below. We describe and characterize a rich photosynthetically-based microbial ecosystem that is protected from the arid outside environment by a translucent salt crust. Gases collected from sediments under shallow ponds in the sabkha contain methane in concentrations as high as 3400 ppm. The salt crust could preserve biomarkers and other evidence for life in the salt after it dries out. Chloride-filled depressions have been identified on Mars and although surface flow of water is unlikely on Mars today, ground water is possible. Such a near surface system with modern groundwater flowing under ancient salt deposits could be present on Mars and could be accessed by surface rovers.     

Systematic placement and biogeographical relationships of the monotypic genera Gypothamnium and Oxyphyllum (Asteraceae: Mutisioideae) from the Atacama Desert

Gypothamnium and Oxyphyllum (Asteraceae) are two monotypic genera endemic to the Atacama Desert of northern Chile. We performed a phylogenetic analysis using published sequences of the plastid rbcL and ndhF genes, the trnL‐trnF region and the nuclear ribosomal internal transcribed spacer (ITS) to assess the systematic placement of the two genera within Mutisioideae. On the basis of the phylogenetic results, we constructed area cladograms to explore the biogeographical relationships and origin of the genera. The phylogenetic analysis showed that Gypothamnium is closely related to Aphylloclados, Plazia, Urmenetia, Lycoseris and Onoseris, whereas Oxyphyllum is closely related to Leucheria, Moscharia, Polyachyrus and, with low support, Jungia. These results do not differ substantially from those proposed in previous treatments based on morphological characters. The biogeographical analysis suggests that Gypothamnium in the coastal Atacama Desert is related to taxa that are currently distributed in eastern subtropical South America and in the Puna. Oxyphyllum may have originated from central Chile and other areas in southern South America, but its sister group (Leucheria + Polyachyrus) also reaches the Puna and the coastal Atacama Desert. Both groups show ancestral affinities with elements currently distributed in north‐western South America and Mesoamerica. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159 , 32–51.     

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.     

大气降尘沉积对塔克拉玛干沙漠腹地土壤水盐运移的影响

利用微型蒸渗仪(MLS)对不同粒级和不同厚度大气降尘沉积条件下塔克拉玛干沙漠腹地土壤水分蒸发和盐分运移进行了模拟试验.结果表明：不同粒级和不同厚度大气降尘沉积均对研究区土壤水分蒸发和盐分运移有显著影响;在相同的沉积厚度和相同的初始含水量条件下,细粒物质（粒径<0.063 mm）沉积可促进土体蒸发、加速下层土体的干旱和盐分的表聚,而粗粒物质（粒径0.063～2 mm）沉积则抑制了土壤水分蒸发、降低了深层土壤水分的损失和盐分的表聚;研究区土壤水分蒸发抑制效率在0.20 mm粒径处出现拐点,粒径在0.063～0.20 mm时,蒸发抑制效率随粒径增大而增大,当粒径>0.20 mm时,蒸发抑制效率则随粒径增大而减小.在相同粒级和相同的初始含水量条件下,不同厚度大气降尘沉积对土壤水分蒸发具有抑制作用,且土壤水分蒸发抑制效率随着沉积厚度的增大而增大,蒸发抑制效率与沉积厚度呈对数关系;沉积厚度越大,盐分向表层积聚越困难.降尘的加入可能导致干旱荒漠区生态系统的不稳定.     

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.     

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.     

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.     

Halotolerant Aerobic Heterotrophic Bacteria from the Great Salt Plains of Oklahoma

The Salt Plains National Wildlife Refuge (SPNWR) near Cherokee, Oklahoma, contains a barren salt flat where Permian brine rises to the surface and evaporates under dry conditions to leave a crust of white salt. Rainfall events dissolve the salt crust and create ephemeral streams and ponds. The rapidly changing salinity and high surface temperatures, salinity, and UV exposure make this an extreme environment. The Salt Plains Microbial Observatory (SPMO) examined the soil microbial community of this habitat using classic enrichment and isolation techniques and phylogenetic rDNA studies. Rich growth media have been emphasized that differ in total salt concentration and composition. Aerobic heterotrophic enrichments were performed under a variety of conditions. Heterotrophic enrichments and dilution plates have generated 105 bacterial isolates, representing 46 phylotypes. The bacterial isolates have been characterized phenotypically and subjected to rDNA sequencing and phylogenetic analyses. Fast-growing isolates obtained from enrichments with 10% salt are predominantly from the gamma subgroup of the Proteobacteria and from the low GC Gram-positive cluster. Several different areas on the salt flats have yielded a variety of isolates from the Gram-negative genera Halomonas, Idiomarina, Salinivibrio, and Bacteroidetes. Gram-positive bacteria are well represented in the culture collection including members of the Bacillus, Salibacillus, Oceanobacillus, and Halobacillus.     

Major plant communities of North America's most arid region: The San Felipe Desert,Baja California,México

Abstract

This vegetation study describes the landscape of the San Felipe Desert (Baja California, México) based on the phytosociological analysis of its major plant associations, as determined by the Braun-Blanquet method and supported by cluster analysis. Four geomorphological or phytotopographical units were identified in the landscape of the San Felipe Desert (salt marshes, playas or sandy flats, bajadas or alluvial fans, and malpaíses or badlands), each characterized by its own plant communities. Two communities and eleven associations were identified, four of which are described and typified for the first time: Atriplici linearis-Frankenietum palmeri, Parkinsonio microphyllae-Olneyetum tesotae, Errazurizio megacarpae-Ephedretum trifurcae and Pachycereo schottii-Prosopidetum torreyanae. Ecological, phytogeographical, bioclimatic, syntaxonomical and floristic data are provided for each of these new associations.     

Water availability shapes edaphic and lithic cyanobacterial communities in the Atacama Desert

In the Atacama Desert, cyanobacteria grow on various substrates such as soils (edaphic) and quartz or granitoid stones (lithic). Both edaphic and lithic cyanobacterial communities have been described but no comparison between both communities of the same locality has yet been undertaken. In the present study, we compared both cyanobacterial communities along a precipitation gradient ranging from the arid National Park Pan de Azúcar (PA), which resembles a large fog oasis in the Atacama Desert extending to the semiarid Santa Gracia Natural Reserve (SG) further south, as well as along a precipitation gradient within PA. Various microscopic techniques, as well as culturing and partial 16S rRNA sequencing, were applied to identify 21 cyanobacterial species; the diversity was found to decline as precipitation levels decreased. Additionally, under increasing xeric stress, lithic community species composition showed higher divergence from the surrounding edaphic community, resulting in indigenous hypolithic and chasmoendolithic cyanobacterial communities. We conclude that rain and fog water, respectively, cause contrasting trends regarding cyanobacterial species richness in the edaphic and lithic microhabitats.     

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).     

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.     

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.     

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.