Colonization patterns of soil microbial communities in the Atacama Desert

Abstract

Background: 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.

Results: 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.

Conclusions: 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.

Figure 1

Sampling site locations. (a) Relief map of northern Atacama Desert, Chile, with key field locations marked by green triangles; (b) photos of Kevin Garden (KEV), Bea Hill (BEA), Andrew Garden (AND), Aguas Calientes (AC), Altamira (AL), and Chañaral (CH) sampling locations.

Figure 2

Geochemical features of sampling locations (n = 68). (a) Boxplots for conductivity and (b) boxplots for pH.

Figure 3

Alpha diversity metrics for each sampling location, rarefied to the 1,000-sequence level (n = 48). (a) Boxplots of OTUs_0.03 richness and (b) boxplots of the Shannon diversity index, both at the 97% sequence similarity threshold.

Figure 4

A density plot of observed OTU_0.03 richness, rarefied to the 1,000-sequence level (n = 48), comparing the (1) northern (KEV, BEA, AND) locations, the (2) central (AC) location, and the (3) southern (AL, CH) locations. The vertical height of each grouping is the continuous probability that each group contains a sample with the given richness.

Figure 5

Unweighted Unifrac principal coordinate analyses (PCoA) of samples at the 200-rarefied level (n = 68), calculated with QIIME. (a) PCoA color-coded by conductivity values (low conductivity: red, average: white, high: blue), and (b) the same plot detrended with QIIME. (c) PCoA color coded by relative air humidity values (high humidity: green, average: yellow, low: orange), and (d) the same plot detrended with QIIME.

Figure 6

Relative abundance of major taxonomic groups in all Atacama soil samples based on environmental 16S rRNA gene sequences. (a) Phyla relative abundance; phyla with <1% abundance are represented in ‘others’; (b) relative abundance of order/families (>10 counts summed across all samples); first 25 taxa are described in the figure legend; a list of all taxa is in (Additional file 1: Table S9). Analyses were performed using samples at the 200-rarefied level (n = 68).

Figure 7

Mineralization of (1,2-¹⁴C) acetic acid at 20°C in microcosms with Atacama soil samples. Each point represents the mean cumulative mineralization expressed as the cumulative % of radiolabel recovered as ¹⁴CO₂ from triplicate assays including sterile controls (dashed lines). (a) Radiolabeled acetic acid (0.045 μCi) was added at the beginning of the experiment and (b) again at day 47 to the same microscosms. Black arrows: second addition of radiolabel substrate. Error bars are standard error of the mean.