Colonization patterns of soil microbial communities in the Atacama Desert
© Crits-Christoph et al.; licensee BioMed Central Ltd. 2013
Received: 23 August 2013
Accepted: 13 November 2013
Published: 20 November 2013
The Atacama Desert is one of the driest deserts in the world and its soil, with extremely low moisture, organic carbon content, and oxidizing conditions, is considered to be at the dry limit for life.
Analyses of high throughput DNA sequence data revealed that bacterial communities from six geographic locations in the hyper-arid core and along a North-South moisture gradient were structurally and phylogenetically distinct (ANOVA test for observed operating taxonomic units at 97% similarity (OTU0.03), P <0.001) and that communities from locations in the hyper-arid zone displayed the lowest levels of diversity. We found bacterial taxa similar to those found in other arid soil communities with an abundance of Rubrobacterales, Actinomycetales, Acidimicrobiales, and a number of families from the Thermoleophilia. The extremely low abundance of Firmicutes indicated that most bacteria in the soil were in the form of vegetative cells. Integrating molecular data with climate and soil geochemistry, we found that air relative humidity (RH) and soil conductivity significantly correlated with microbial communities’ diversity metrics (least squares linear regression for observed OTU0.03 and air RH and soil conductivity, P <0.001; UniFrac PCoA Spearman’s correlation for air RH and soil conductivity, P <0.0001), indicating that water availability and salt content are key factors in shaping the Atacama soil microbiome. Mineralization studies showed communities actively metabolizing in all soil samples, with increased rates in soils from the southern locations.
Our results suggest that microorganisms in the driest soils of the Atacama Desert are in a state of stasis for most of the time, but can potentially metabolize if presented with liquid water for a sufficient duration. Over geological time, rare rain events and physicochemical factors potentially played a major role in selecting micro-organisms that are most adapted to extreme desiccating conditions.
KeywordsSoil microbial communities Extreme environment Arid soil Atacama Desert Desertification High-throughput 16S rRNA sequencing
Life can adapt to some of the harshest environments on Earth, from deep-sea hydrothermal vents to hypersaline lakes and acidic hot springs , but can life adapt to places where there is essentially no water and no nutrients? The Atacama Desert is one of the oldest and driest deserts in the world and its hyper-arid core has been described as ‘the most barren region imaginable’ [2, 3]. While micro-organisms have been detected in the soil of the Atacama, little is known about the structure and composition of the microbial communities inhabiting its soil and the processes shaping the assembly of those communities.
The Atacama Desert stretches 600 miles along the Pacific Coast of Northern Chile (19º-27ºS) and its sedimentary records indicates semi-arid to hyper-arid climates from the Jurassic period (150 million years ago) to the present day, with extremely arid conditions arising in the Miocene (15 million years ago) [3–5]. The Atacama Desert owes its extreme aridity to a constant climate regime produced by a subtropical anticyclonic atmospheric subsidence - the Pacific Anticyclone. This is strengthened by the Humboldt Current - an upwelling, cold current along the west coast of South America - and the rain shadow effect from the Andean Cordillera to the East. The continentality effect that occurs when rain-bearing trade winds are blocked from penetrating continental interiors provides additional aridity in the desert [3, 6]. Between parallels 22°S and 26°S is the hyper-arid core of the Atacama, one of the places with the lowest pluviometric activity in the world [2, 6, 7]. Long-term mean annual rainfall is only a few millimeters, with rain events typically occurring once per decade (http://www.meteochile.cl/; ). In addition, the high coastal mountains block the marine fog . As a result, soil surfaces are bare with sparsely vegetated areas found only where groundwater discharges via localized springs . Geological and soil mineral analyses of the hyper-arid core report organic material detected at trace levels, nitrate accumulation - probably of atmospheric origin - and highly oxidizing conditions [2, 8, 9]. Other unique features include very low erosion and the accumulation of halite, gypsum, anhydrite, and unusual salts such as perchlorates, nitrates, and iodates [5, 10].
The extreme aridity of the Atacama Desert, together with broad daily temperature fluctuations and intense ultraviolet radiation, contribute to make the core of this desert an extreme habitat approaching ‘the dry limit of life on Earth’ . Nevertheless, micro-organisms inhabit this extreme environment. Studies have reported low numbers of culturable bacteria in soil samples of the arid core, ranging from not detectable to 106 CFU/g of soil, and reflecting a great spatial heterogeneity [8, 9, 11–15]. With the use of molecular methods, the subsurface layers of the hyper-arid core were shown to harbor a very limited microbial community dominated by Gemmatimonadetes and Plantomycetes bacteria and also including Actinobacteria, Thermomicrobia, and one member of the Proteobacteria[9, 11, 12]. These micro-organisms were identified in soil samples where no vascular plant has grown for millions of years and rain occurs only once every 20 to 50 years [8, 9, 11, 12]. In less arid parts of the desert, soil bacterial communities were characterized by a high abundance of novel Actinobacteria and Chloroflexi taxa, and low levels of Acidobacteria and Proteobacteria[11, 16]. Fungi cultured from samples collected in several locations of the Atacama were all spore-forming saprophytes, suggesting that they might not be indigenous to the desert but rather dispersed by wind .
Relatively diverse, photosynthetic-based microbial communities have been described colonizing diaphanous rocks and halite evaporites in various parts of the desert [18–23]. These endolithic and hypolithic habitats are considered environmental refuges for life in hot and cold deserts, and harbor highly specialized communities . Questions still remain about the presence of any stable and functional microbial communities in the Atacama soil, due to its physical instability, low nutrient content, and non-translucent properties [8, 23, 25].
Here, we use a combination of geological analyses, mineralization experiments, and non-culture based high throughput molecular methods to determine whether the Atacama soil is at the dry limit for life. Our analyses of community structure and composition, from soil samples collected in the hyper-arid core and along a North-South moisture gradient, revealed a relatively simple ecosystem and indicated that salt content, together with water availability, significantly correlated with the diversity of microbial communities. Metabolic activity detected in soil samples with added moisture suggest that the soil community can be activated by rainfalls or heavy fog events, providing a means of adaptation to their extreme environmental conditions.
Sampling, soil geochemistry, and climate data
Soil total elemental analysis was performed by ICAP spectrometry following HNO3/HClO4 digestion (method 2021; Cornell Nutrient Analysis Lab, Ithaca, NY, USA). Total carbon and total organic carbon (TOC) were determined by total dry combustion with a LECO CNS-2000 Carbon Analyzer (Cornell Nutrient Analysis Lab, Ithaca, NY, USA). Soil measurements, pH, conductivity, water content, and texture were performed according to protocols described in the Standard Procedures for Soil Research in the McMurdo Dry Valleys LTER available through the MCM LTER public database at http://www.mcmlter.org.
Climate data, air temperature, and air relative humidity (RH) were collected in situ during the 2009 and 2011 sampling expeditions. Historical climate data were obtained from the literature [2, 23, 26].
Cell counts were carried out with DAPI as previously described .
DNA extraction, PCR amplification, and sequencing
Total genomic DNA was extracted from soil samples using the PowerSoil DNA Isolation kit (MoBio Laboratories Inc., Solana Beach, CA, USA) following the manufacturer’s instructions. All sample manipulations and nucleic acid extractions were carried out in a laminar flow hood (AirClean Systems, Raleigh, NC, USA) and all materials and reagents were either filter sterilized, autoclaved, or UV-irradiated to prevent contamination. For 454 pyrosequencing, genomic DNA was amplified using the barcoded Universal primers 27 F (bacterial)/4Fa (archaeal) and 534R for the V1-V3 hypervariable region of the 16S rRNA gene. The amplification reaction mixture (25 μL) contained 200 μM deoxynucleoside triphosphates (dNTPs) each, 0.3 μM (each) primer, 1-5 ng/μL of DNA template, 0.02 U/μL of Phusion High-Fidelity DNA polymerase (New England BioLabs, Ipswich, MA), 1 × Phusion PCR buffer HF, 0.5 mM MgCl2, and 3% DMSO. PCR conditions were one initial step of 30 s at 98°C, followed by 25 cycles of 10 s at 98°C, 15 s at 55°C, and 15 s at 72°C, and with a final step of 10 min at 72°C, using a T3000 Thermal Cycler (Biometra, Horsham, PA, USA). Amplicons were purified with the AMPure Kit (Agencourt, Beckman Coulter Genomics, Danvers, MA, USA), and equimolar amounts (100 ng) of all amplicons were mixed in a single tube and sequenced by 454 pyrosequencing using a Roche GS-FLX sequencing system (Roche-454 Life Sciences, Branford, CT, USA) by the Genomics Resource Center (GRC) at the Institute for Genome Sciences (IGS), University of Maryland School of Medicine using protocols recommended by the manufacturer as amended by the GRC.
Processing of pyrosequencing data and analysis
The 454 sequences were processed using the QIIME package (v1.6.0) . Sequences were de-multiplexed by binning sequences with the same barcode and primer sequences in QIIME. Similar sequences with <3% dissimilarity were clustered together using USEARCH  and de novo chimera detection was conducted in UCHIME v5.1 . The resulting average sequence length was 494 bp. Taxonomic ranks were assigned to each sequence using Ribosomal Database Project (RDP) Naïve Bayes Classifier v.2.2 , using 0.8 confidence values as the cutoff to a pre-built greengenes database of 16S rRNA sequences (Oct, 2012 vers.) . Representative sequences of each OTU0.03 were aligned with PyNAST  against the Greengenes core set , gaps and parsimonious uninformative characters were removed, and the filtered sequences subsequently used to generate a phylogenetic tree with FastTree  for beta-diversity metrics using UniFrac [36, 37]. Richness and diversity estimators were calculated based on OTUs with QIIME . Principal Coordinate Analysis (PCoA) plots were generated with QIIME using unweighted and weighted UniFrac metrics, and Bray-Curtis distances [28, 36]. Detrending of PCoA plots was also performed with QIIME . The R statistical package was used to perform all statistical tests of diversity and geochemistry data . The non-parametric Kruskal-Wallis one-way analysis of variance  was used to test differences in both diversity metrics and geochemistry between geographic locations and groupings. Least Squares Linear Regression was used to test correlation hypotheses.
Soil microbial activity was assessed by monitoring the mineralization of 14C-acetate added to microcosms containing 5 g of soil and constructed according to . Each microcosm, in triplicate with sterile controls (baked for 5 h at 160°C), was amended with a mixture of 1 mL of 10 mM sodium acetate (autoclaved and filtered sterilized) and 0.045 μCi (1,2-14C) acetic acid (100,000 disintegrations per min) (Perkin Elmer, SA 54.3 mCi mmol-1) at the beginning of the experiment and at day 47. Microcosms were incubated at 20°C without shaking or illumination. CO2 traps containing 0.5 mL of 1 M KOH were sampled every 1 to 7 days and radioactive counts were determined by liquid scintillation spectrometry using a Packard Tri-Carb 2200CA Scintillation Counter (Waltham, MA, USA). Mineralization was expressed as the cumulative radiolabel recovered as 14CO2. For days 47 to 89, mineralization was calculated using the amount of radiolabeled substrate added at day 47.
We combined environmental factor measurements with molecular data from non-culture-based high throughput molecular methods to identify the factors underlying the structure and composition of microbial assemblages in soil samples from the driest areas of the Atacama Desert.
Sampling locations and soil geochemical features
Geographical and climate data for soil sampling locations in the Atacama Desert
Elevation (m above sea level)
Mean annual temp (°C)
Mean annual relative air humidity
Mean annual rainfall (mm)
Mean soil geochemical properties, composition, and cell counts for each sampling location in the Atacama Desert
Cell count 103cells.g-1soil
Soil pH, conductivity, and calcium/sulfur elemental composition were also significantly correlated across the dataset (Additional file 1: Tables S1 and S2). We found a positive linear correlation (β = 0.94, P <0.001) across locations between the sulfur and calcium elemental compositions - the components of gypsum and anhydrite (CaSO4, +/-2H2O). The calcium and sulfur values we measured for each location correlated strongly with average soil conductivity for each location. The soil in the AL and CH locations had lower amounts of elemental calcium and sulfur than the soil of the other four locations. The AC location shared geochemical features with both the southern and northern locations; while it has a low average pH (7.75, s (standard deviation) = 0.3) and high levels of calcium and sulfur like the three Yungay locations, a significantly lower average conductivity of 0.86 mS (millisiemens)/cm (s = 0.87) was recorded. The variation in conductivity at AC was higher than any other location (Figure 2). The lowest variations in soil conductivity were observed in the AL and CH samples (s = 0.03, s = 0.06). Soil composition for most samples was sandy loam and we measured extremely low levels of total organic carbon (Table 2; data for 2009).
Within each location, we found some variability for conductivity and pH values. There was a significant positive increase in pH (t = 4.55; P = 0.0002) with depth when the data were parsed for each sampling site, but no similar change in conductivity (Additional file 1: Table S10). Non-stochastic patterns of geochemistry across transects of sampling sites were not observed.
Molecular characterization of the soil microbial communities
Observed richness and diversity indices for soil samples based on 16S rRNA gene sequence assignments with a 97% sequence similarity threshold, rarefied to 1,000 sequence reads ( n = 48)
Shannon index estimated diversity
Faith’s phylogenetic diversity index
Chao 1 diversity estimate
Pielou’s evenness index
To test correlation between abiotic factors and soil microbial diversity metrics, we performed tests of Least Squares linear regression on the alpha diversity metrics generated at the 200-sequence level (n = 68). We found that conductivity and pH both significantly correlated with community richness, predicted diversity, evenness, phylogenetic diversity, and Shannon diversity across all locations (Additional file 1: Table S5). pH correlated directly with richness (P <0.0001) and conductivity correlated inversely with richness (P <0.001). Although the AC location had a slightly lower mean pH than either BEA or KEV, it had a significantly higher distribution of alpha diversity metrics (Table 3). The same correlations proved significant at the 1,000-sequence level (Additional file 1: Table S6). There were no significant relationships between both OTU0.03 count and Chao1 predicted diversity with soil depth at either the 1,000 or the 200 level. Location climatic data were significantly correlated with all metrics of diversity (Additional file 1: Table S7). The climatic data are location-specific as opposed to sample-specific, and the correlation demonstrates the difference in diversity levels between the hyper-arid northern sites and the southern sites. Mean air relative humidity (RH), mean air temperature, and rainfall correlated directly with observed OTUs0.03 (P <0.001). Within locations, diversity did not correlate with sample depth or with sampling site position and this included the sampling-transects for each of the three northern locations, KEV, BEA, and AND.
Phylogenetic diversity of soil microbial communities
Relative abundance of taxa at the order/family level (Figure 6b) greatly illustrated the change in community structure and composition revealed by analyses of alpha and beta diversity. Members of the Actinobacteria mostly belong to a small number of orders including Rubrobacterales, Actinomycetales, and Acidimicrobiales (Figure 6b). While Rubrobacterales were dominant in the KEV location, a shift toward Acidimicrobiales and Actinomycetales was observed for the BEA and AND locations. At the taxonomic level, the most southern locations (AC, AL, and CH) were more diverse with members of the Acidimicrobiales, Rubrobacterales but also of the Gemmatimonadetes, Bacteroidetes, and a number of families from the Thermoleophilia (class of Actinobacteria) . The evenness of these later communities, represented by the Pielou’s evenness index, was notably higher than that of the northern communities (Table 3) and expressed by a larger number of members per taxonomic group (Figure 6b). While a number of Chloroflexi taxa were found across all soil samples, very few members of the Firmicutes were detected.
Soil metabolic activity
The Atacama Desert presents a unique physiography, a range of hyper-arid conditions, climate regimes, and geology within a relatively small region, providing a number of unique habitats for microbial communities [24, 25]. Of particular relevance is a steep rainfall gradient along a North-South transect between 23ºS and 29ºS, where precipitation increases from <1 mm year-1 to >40 mm year-1[2, 23]. The Atacama rainfall gradient represents a unique natural setting to study how life responds to increasing water stress towards the hypothetical dry limit of life. We conducted a high-resolution sampling of near surface soils (0-10 cm) and applied a combination of geochemistry and molecular data to characterize the microbial community along the rainfall gradient, and to determine the environmental factors shaping the community structure in these soils.
Geochemical analyses of our study sites revealed a high degree of heterogeneity with the greatest variability in soil mineralogy between geographical locations. The southernmost soils were more alkaline than the other soils, which might reflect a greater influence from salts of marine origin [44, 45]. In contrast, more inland salt deposits in the Atacama are thought to be the result of eolian dispersion from local salars .
Our molecular data provided a good coverage of the soil microbial diversity, underlining the low microbial diversity of the Atacama soil microbiome. Similarly low numbers for OTUs0.03 richness were reported for comparable studies of Atacama soils at the hyper-arid margin  and for several locations in the Antarctica Dry Valleys . Alpha diversity metrics showed stochastic variations at multiple sampling sites within each geographic location, but significant differences were found between locations. Analyses of beta diversity indicated that communities from each geographic location were structurally and phylogenetically distinct.
Changes in soil microbiology along the North-South transect were correlated with water availability, described as air mean RH and mean annual rainfall. Changes were also inversely correlated with soil conductivity, a proxy for water availability (that is, more salt, less water) . Microbial diversity, community structure, and rates of metabolic activity were clearly distinct between the driest localities and the wettest ones, with an apparent intermediate transition zone (AC) located between S25º0’ and S25º30’. Lowest diversity was found in the northern samples where water availability reaches minimum values. These soils also had relatively high salt contents associated with high levels of Na, Ca, and S, and the presence of gypcrust close to the soil surface (within 10 cm), indicating persistent aridity over geological time . Microbial diversity was significantly higher at the southernmost sampling localities where mean annual rainfall was one order of magnitude higher and near-surface soils were likely wetted yearly. The higher level of precipitation experienced by the southern soils was substantiated by low salt contents as the result of leaching toward higher depths [48, 49].
Soil heterotrophic bacteria commonly encountered in arid environments were shared between all soil samples and included members of the Rubrobacterales, Actinomycetales, and Acidimicrobiales[16, 50]. The abundance of the various taxonomic groups varied significantly between soil locations. Radiation tolerant and desert dwelling bacteria from the Rubrobacterales were most abundant in the driest locations while the southern locations displayed a number of Thermoleophilia families, including Solirubrobacteraceae and Patulibacteraceae. These taxa, closely related to the Rubrobacteraceae, are found in biological soil crusts  and have been reported in less arid soils of the Atacama Desert . Chloroflexi were found across all soil locations and have been observed in hypolithic and various soil communities of the Atacama Desert [16, 52–54]. No archaeal sequences were found as was reported for Antarctic soils of similar composition [46, 55].
Using soil microcosms amended with radiolabeled acetate we detected metabolic activity in all tested samples, indicating a viable portion of the soil community in all localities. These are conventional methods typically used to detect metabolic activity in extreme environments such as at subzero temperatures and in hyper-arid deserts [8, 56–59]. Different experimental settings make it difficult to compare our results with previous experiments using Atacama soil [8, 57]; however, similarly to Quinn et al. , we observed a resumption of CO2 production after a second injection of substrate. Our mineralization rates were consistent with studies using Canadian high Arctic soil samples, taking into consideration differences in incubation temperatures [40, 60, 61]. Detectable mineralization rates in the northernmost Atacama samples were observed after 7 days of incubation, while the southernmost samples mineralized faster and in higher amounts. These trends could be due to a difference in cell abundance, resulting in smaller rates of mineralization and smaller consumption of labeled substrate in the northernmost samples. Alternatively, they could be explained by a difference in the physiological state of soil micro-organisms, with a rapid activation in the southernmost samples that witness yearly rainfall, and a slow activation in the northernmost samples that witness decadal rainfall. While estimated cell abundances vary by up to two orders of magnitude between the northernmost and the southernmost samples (Table 2), mineralization rates and net amounts were similar between AL (2.4×104 cells g-1 of soil) and CH (1×105 cells g-1 of soil), suggesting that both cell abundance and physiological state might be significant in explaining the different rates of mineralization. Soil micro-organisms at the dry end of our sampling transect are challenged by severe oligotrophic conditions, as illustrated by the extremely low TOC and total nitrogen levels in these soils (Table 2 and [11, 16, 62]), and it is therefore likely that both extreme water stress and restricted access to organic substrates are limiting factors for their in situ activity and growth. Determining the state of dormancy and the rate at which metabolic activity is recovered in Atacama soil communities will require careful isolation and in depth physiological and molecular studies of microbial strains from both the north and south locations.
Together, our results suggest that: (1) soil micro-organisms in the driest Atacama soils are in a state of stasis for most of the time, but can potentially metabolize if presented with liquid water for sufficient time; and (2) there is, or has been, a degree of selection on the soil microbial communities in response to environmental conditions. Correlation with water availability and soil salt content revealed that these factors are potentially the drivers for the variations in diversity observed in the soil, and likely the drivers for selection. One possible source of water in this extremely dry environment could be the deliquescence of soil salts such as NaCl, similar to micro-organisms inhabiting halite nodules in ancient saltpans within the same hyper-arid region [63, 64]. A similar mechanism was also suggested for halite- and perchlorate-rich soils, 2-m-deep in the Atacama subsurface . The soils we analyzed did not contain nearly as much salt as the hypersaline subsurface described by Parro et al. , suggesting that near-surface soil (up to 10 cm) of the hyperarid core, because of its loose structure and limited amount of hygroscopic salts, presents little potential for water retention. Only rain events with 2 mm of rainfall or more were shown to generate free water in the top few centimeters for this type of soil (measured by the increased voltage between two electrodes 5 mm apart ). These events are rare and short-lived, and seemingly linked to el Niño decadal cycles . Therefore, it appears that conditions for metabolic activity and selection in these hyper-arid soils only occur during infrequent rain events over decades or longer. This would explain the very long residence time of organic carbon in these soils (c.a. 104 yr, ), and the long-term preservation of labile organic compounds such as amino acids .
Our work suggests that soil micro-organisms in the hyper-arid core of the Atacama Desert are still viable, but possibly at the limit of survival. It further emphasizes the hypothesis that in extremely dry environments, habitability becomes heterogeneous and needs to be evaluated in terms of the physicochemical properties of different substrates potentially ‘habitable’. The meager biological content and metabolic activity in the hyper-arid soils of the Atacama is in stark contrast with other substrates found in the same hyper-arid region, such as calcite, gypsum, and ignimbrite rocks [19–21], and the interior of hygroscopic salts (halites) that can sustain diverse and metabolically active communities by way of salt deliquescence [63, 64, 68]. Similarly, hygroscopic salts on Mars could have become one of the last refuges for life on the planet, long after soils became uninhabitable . Hence, a rigorous search for life on Mars demands the study of a diversity of substrates, and particularly those that are known to sustain life in extremely dry environments on Earth.
Availability of supporting data
The datasets supporting the results of this article are available National Centre for Biotechnology Information Sequence Read Archive under SRA accession number SRA091062, and study accession number SRP026010, BioProject ID PRJNA208226.
Analysis of variance
- ICAP spectrometry:
Inductively coupled argon plasma spectrometry
Operational taxonomic unit
Principal coordinate analysis
The authors thank Dominique Seow, Yang Liu, Shabeg Singh, Kim Webb, and Alexandra Gresov for technical assistance, and Octavio Artieda for constructive comments. This work was funded by grant EXOB08-0033 from NASA and grant NSF-0918907 from the National Science foundation to JDR. CPM and AFD acknowledge ASTEP support for fieldwork in the Atacama. Publication of this article was funded in part by the Open Access Promotion Fund of the Johns Hopkins University Libraries.
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