Significant Impacts of Increasing Aridity on the Arid Soil Microbiome

Global deserts occupy one-third of the Earth's surface and contribute significantly to organic carbon storage, a process at risk in dryland ecosystems that are highly vulnerable to climate-driven ecosystem degradation. The forces controlling desert ecosystem degradation rates are poorly understood, particularly with respect to the relevance of the arid-soil microbiome. Here we document correlations between increasing aridity and soil bacterial and archaeal microbiome composition along arid to hyperarid transects traversing the Atacama Desert, Chile. A meta-analysis reveals that Atacama soil microbiomes exhibit a gradient in composition, are distinct from a broad cross-section of nondesert soils, and yet are similar to three deserts from different continents. Community richness and diversity were significantly positively correlated with soil relative humidity (SoilRH). Phylogenetic composition was strongly correlated with SoilRH, temperature, and electrical conductivity. The strongest and most significant correlations between SoilRH and phylum relative abundance were observed for Acidobacteria, Proteobacteria, Planctomycetes, Verrucomicrobia, and Euryarchaeota (Spearman's rank correlation [r(s)] = >0.81; false-discovery rate [q] = <= 0.005), characterized by 10- to 300-fold decreases in the relative abundance of each taxon. In addition, network analysis revealed a deterioration in the density of significant associations between taxa along the arid to hyperarid gradient, a pattern that may compromise the resilience of hyperarid communities because they lack properties associated with communities that are more integrated. In summary, results suggest that arid-soil microbiome stability is sensitive to aridity as demonstrated by decreased community connectivity associated with the transition from the arid class to the hyperarid class and the significant correlations observed between soilRH and both diversity and the relative abundances of key microbial phyla typically dominant in global soils. IMPORTANCE We identify key environmental and geochemical factors that shape the arid soil microbiome along aridity and vegetation gradients spanning over 300 km of the Atacama Desert, Chile. Decreasing average soil relative humidity and increasing temperature explain significant reductions in the diversity and connectivity of these desert soil microbial communities and lead to significant reductions in the abundance of key taxa typically associated with fertile soils. This finding is important because it suggests that predicted climate change-driven increases in aridity may compromise the capacity of the arid-soil microbiome to sustain necessary nutrient cycling and carbon sequestration functions as well as vegetative cover in desert ecosystems, which comprise one-third of the terrestrial biomes on Earth.National Institute of Environmental Health Sciences Superfund Research Program [P42 ES004940]; National Science Foundation Microbial Observatory grant [MCB0604300]; Lewis and Clark Fund for Exploration and Field Research in Astrobiology; Earth Microbiome Project - WM Keck Foundation; John Templeton Foundation; Argonne National LaboratoryOpen Access Journal.This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

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<div><p><i>Burkholderia pseudomallei</i> is the causative agent of melioidosis and a potential bioterrorism agent. In the development of medical countermeasures against <i>B</i>. <i>pseudomallei</i> infection, the US Food and Drug Administration (FDA) animal Rule recommends using well-characterized strains in animal challenge studies. In this study, whole genome sequence data were generated for 6 <i>B</i>. <i>pseudomallei</i> isolates previously identified as candidates for animal challenge studies; an additional 5 isolates were sequenced that were associated with human inhalational melioidosis. A core genome single nucleotide polymorphism (SNP) phylogeny inferred from a concatenated SNP alignment from the 11 isolates sequenced in this study and a diverse global collection of isolates demonstrated the diversity of the proposed Animal Rule isolates. To understand the genomic composition of each isolate, a large-scale blast score ratio (LS-BSR) analysis was performed on the entire pan-genome; this demonstrated the variable composition of genes across the panel and also helped to identify genes unique to individual isolates. In addition, a set of ~550 genes associated with pathogenesis in <i>B</i>. <i>pseudomallei</i> were screened against the 11 sequenced genomes with LS-BSR. Differential gene distribution for 54 virulence-associated genes was observed between genomes and three of these genes were correlated with differential virulence observed in animal challenge studies using BALB/c mice. Differentially conserved genes and SNPs associated with disease severity were identified and could be the basis for future studies investigating the pathogenesis of <i>B</i>. <i>pseudomallei</i>. Overall, the genetic characterization of the 11 proposed Animal Rule isolates provides context for future studies involving <i>B</i>. <i>pseudomallei</i> pathogenesis, differential virulence, and efficacy to therapeutics.</p></div

Correlations of LS-BSR values with observed differential virulence in BALB/c mice.

<p>*High, intermediate and low virulence determined by intranasal challenge at ~10 colony forming units.</p><p>Correlations of LS-BSR values with observed differential virulence in BALB/c mice.</p

Annotation for unique genes identified in genomes sequenced in the current study.

<p>Annotation for unique genes identified in genomes sequenced in the current study.</p

Nucleotide variant information for re-sequencing projects conducted in current study.

<p>Nucleotide variant information for re-sequencing projects conducted in current study.</p

Details of isolates sequenced in current study.

<p>*genome has been sequenced previously</p><p>Details of isolates sequenced in current study.</p

A heatmap of blast score ratio (BSR) values [44] calculated from a known set of virulence factors characterized in <i>B</i>. <i>pseudomallei</i> (S3 Table) with the large-scale blast score ratio (LS-BSR) pipeline [43].

<p>A maximum likelihood phylogeny was inferred on a concatenation of single nucleotide polymorphisms (SNPs) and was correlated to the heatmap.</p

A maximum likelihood phylogeny inferred from a concatenation of ~63,000 core-genome single nucleotide polymorphisms (SNPs) identified in the eleven genomes sequenced in this study, shown in red, and a reference set of genomes (S2 Table).

<p>The tree was inferred with RAxML v8 [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121052#pone.0121052.ref031" target="_blank">31</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121052#pone.0121052.ref032" target="_blank">32</a>] using the ASC_GTRGAMMA model and 100 bootstrap replicates. Filled circles are placed at nodes where the bootstrap support values are >90%.</p