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. 2020 Jan 22:10:3160.
doi: 10.3389/fmicb.2019.03160. eCollection 2019.

Microbiome Dynamics Associated With the Atacama Flowering Desert

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Microbiome Dynamics Associated With the Atacama Flowering Desert

Juan Pablo Araya et al. Front Microbiol. .

Abstract

In a desert, plants as holobionts quickly respond to resource pulses like precipitation. However, little is known on how environment and plants modulate the rhizosphere-associated microbiome. As a model species to represent the Atacama Desert bloom, Cistanthe longiscapa (Montiaceae family) was selected to study the influence of abiotic and biotic environment on the diversity and structure of the microbiota associated to its rhizosphere. We analyzed the rhizosphere and soil microbiome along a North-South precipitation gradient and between a dry and rainy year by using Illumina high-throughput sequencing of 16S rRNA gene fragments and ITS2 regions for prokaryotes and fungi, respectively. In the rhizosphere of C. longiscapa the microbiota clearly differs in composition and structure from the surrounding bulk soil. The fungal and bacterial communities respond differently to environmental conditions. The diversity and richness of fungal OTUs were negatively correlated with aridity, as predicted. The community structure was predominantly influenced by other soil characteristics (pH, organic matter content) but not by aridity. In contrast, diversity, composition, and structure of the bacterial community were not influenced by aridity or any other evaluated soil parameter. These findings coincide with the identification of mainly site-specific microbial communities, not shared along the sites. These local communities contain a group of OTUs, which are exclusive to the rhizosphere of each site and presumably vertically inherited as seed endophytes. Their ecological functions and dispersal mechanisms remain unclear. The analysis of co-occurrence patterns highlights the strong effect of the desert habitat over the soil- and rhizosphere-microbiome. The site-independent enrichment of only a small bacterial cluster consistently associated with the rhizosphere of C. longiscapa further supports this conclusion. In a rainy year, the rhizosphere microbiota significantly differed from bulk and bare soil, whereas in a dry year, the community structure of the former rhizosphere approximates to the one found in the bulk. In the context of plant-microbe interactions in desert environments, our study contributes new insights into the importance of aridity in microbial community structure and composition, discovering the influence of other soil parameters in this complex dynamic network, which needs further to be investigated.

Keywords: Atacama Desert; Cistanthe longiscapa; co-occurrence patterns; core microbiome; desert bloom; precipitation gradient; rhizosphere community.

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Figures

FIGURE 1
FIGURE 1
Natural habitat of Cistanthe longiscapa, sampling sites and sampling strategy per site. (A) Photograph of C. longiscapa population in a rainy year; (B) Photograph of C. longiscapa population in a dry year; (C) Geographical localization of sampling sites in Quebrada Seca, El Algarrobo, and Pajonales; (D) Schematic illustration of sample types from each site: starting from a C. longiscapa individual three sample types were distinguished: Rhizosphere, Bulk soil, and Bare soil. Bare soil was only collected at site Quebrada Seca, for comparison of rainy and dry year.
FIGURE 2
FIGURE 2
Alpha-diversity analysis per locality and sample type (rhizosphere and bulk soil). (A) Shannon Index for fungi; (B) Chao1 Index for fungi; (C) Shannon Index for prokaryotes; (D) Chao1 Index for prokaryotes. Different letters above the bars indicate statistically different means (Tukey test p < 0.05).
FIGURE 3
FIGURE 3
Beta-diversity analysis and Venn diagrams: comparison between localities. Principal coordinates analysis (PCoA) based on weighted UniFrac Distances per locality and sample type, for fungi (A) and for prokaryotes (B); symbols represent localities: Circles: Quebrada Seca, Squares: El Algarrobo, Triangles: Pajonales; (C) Venn diagram for fungal OTUs registered in rhizosphere per locality; (D) Venn diagram for prokaryotic OTUs registered in rhizosphere per locality; (E) Venn diagram for rhizosphere specific fungal OTUs (fold change ≥ 3, between Rhizosphere and Bulk soil OTUs); (F) Venn diagram for rhizosphere specific prokaryotic OTUs (fold change > 3, between Rhizosphere and Bulk soil). QS, Quebrada Seca; EA, El Algarrobo; PA, Pajonales.
FIGURE 4
FIGURE 4
Network analysis of the bacterial-fungal microbiome associated to C. longiscapa during the Atacama flowering desert event. (A) Bacterial and fungal OTUs (round and squared nodes, respectively) are correlated to each other if connected by a green line. Node size indicates the respective mean OTU abundance. Node color indicates the taxonomic affiliation. The three main clusters detected are labeled. (B) Distribution of the three clusters across the three sites and the two habitats (rhizosphere/bulk). Different letters indicates significantly different means for each cluster (Tukey test, p < 0.05).
FIGURE 5
FIGURE 5
Alpha-diversity analysis per year and sample type (rhizosphere, bulk soil, bare soil). (A) Shannon Index for fungi; (B) Chao1 Index for fungi; (C) Shannon Index for prokaryotes; (D) Chao1 Index for prokaryotes. Different letters above the bars indicate statistically different means (Tukey test, p < 0.05).
FIGURE 6
FIGURE 6
Beta-diversity analysis and Venn diagrams: comparison between years at Quebrada Seca (QS). Principal Coordinates Analysis (PCoA) based on weighted UniFrac Distances per year and sample type, for fungi (A) and for prokaryotes (B); symbols represent sample types: Circles: Rhizosphere, Squares: Bulk soil, Triangles: Bare soil; (C) Venn diagram for rhizosphere specific fungal OTUs [fold change > 3 in case of rainy year (QS15-R); complete OTU table for rhizosphere dry year (QS16-R)]; (D) Venn diagram for rhizosphere specific prokaryotic OTUs (fold change > 3 in case of rainy year (QS15-R); complete OTU table for rhizosphere dry year QS16-R). Fold change > 3 is the rhizosphere OTUs divided by the sum of Bulk- and Bare- soil.

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