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.

Highlights

  • The Atacama Desert in Chile is one of the most arid and ancient deserts on the planet (Hartley et al, 2005; Bull et al, 2016), where small and irregular water pulses allow the survival of an adapted plant cover composed primarily of annual species (Noy-Meir, 1973)

  • Actinobacteria (43.4 ± 10.4%) and Proteobacteria (20.7 ± 5.1%) were significantly most abundant (ANOVA, p < 0.01, Tukey post hoc test), followed by Chloroflexi (8.9 ± 2.5%), Firmicutes (6.9 ± 5.1%), Bacteroidetes (6.5 ± 4.5%), Acidobacteria (4.5 ± 4.6%), Planctomycetes (3.5 ± 1.3%) and Gemmatimonadetes (2.1 ± 1.13%), which represented together more than 95% of the total reads over all samples (Supplementary Figure S2c)

  • Locations with a higher degree of aridity (Quebrada Seca and El Algarrobo) differed in community composition between rhizosphere and bulk soil, where Proteobacteria and Bacteroidetes were significantly increased in the rhizosphere of Quebrada Seca (t-test false discovery rate (FDR) p < 0.05), while Actinobacteria and Firmicutes were significantly enriched in the rhizosphere of El Algarrobo (t-test p < 0.05), whereas Pajonales exhibited subtle variations between the soil habitats (Supplementary Figure S2d)

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Summary

Introduction

The Atacama Desert in Chile is one of the most arid and ancient deserts on the planet (Hartley et al, 2005; Bull et al, 2016), where small and irregular water pulses allow the survival of an adapted plant cover composed primarily of annual species (Noy-Meir, 1973). During rainy periods (years involving the “El Niño” phenomenon), the increased water availability can cause a desert bloom event, where multiple annual plants quickly respond by germinating, emerging and flowering, varying in their time of growth, permanence and abundance. During this event, the desert landscapes between 27 and 29◦S are covered with intense pink, white, yellow and purple colors, transforming the Atacama Desert into an exuberant garden between the months of August and October. Plant cover is known to be important for ecological interactions in desert soil, few studies have investigated microbial ecology, community structure and their interactions with plants, the latter of which can improve the fitness of the plant under conditions of limited environmental resources (Lugtenberg and Kamilova, 2009; Bresson et al, 2013)

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