Metagenomic Signatures of Bacterial Adaptation to Life in the Phyllosphere of a Salt-Secreting Desert Tree

Abstract

The leaves of Tamarix aphylla, a globally distributed, salt-secreting desert tree, are dotted with alkaline droplets of high salinity. To successfully inhabit these organic carbon-rich droplets, bacteria need to be adapted to multiple stress factors, including high salinity, high alkalinity, high UV radiation, and periodic desiccation. To identify genes that are important for survival in this harsh habitat, microbial community DNA was extracted from the leaf surfaces of 10 Tamarix aphylla trees along a 350-km longitudinal gradient. Shotgun metagenomic sequencing, contig assembly, and binning yielded 17 genome bins, six of which were >80% complete. These genomic bins, representing three phyla (Proteobacteria, Bacteroidetes, and Firmicutes), were closely related to halophilic and alkaliphilic taxa isolated from aquatic and soil environments. Comparison of these genomic bins to the genomes of their closest relatives revealed functional traits characteristic of bacterial populations inhabiting the Tamarix phyllosphere, independent of their taxonomic affiliation. These functions, most notably light-sensing genes, are postulated to represent important adaptations toward colonization of this habitat. IMPORTANCEPlant leaves are an extensive and diverse microbial habitat, forming the main interface between solar energy and the terrestrial biosphere. There are hundreds of thousands of plant species in the world, exhibiting a wide range of morphologies, leaf surface chemistries, and ecological ranges. In order to understand the core adaptations of microorganisms to this habitat, it is important to diversify the type of leaves that are studied. This study provides an analysis of the genomic content of the most abundant bacterial inhabitants of the globally distributed, salt-secreting desert tree Tamarix aphylla. Draft genomes of these bacteria were assembled, using the culture-independent technique of assembly and binning of metagenomic data. Analysis of the genomes reveals traits that are important for survival in this habitat, most notably, light-sensing and light utilization genes.

Understanding and exploiting plant beneficial microbes

“…Shotgun metagenomics to compare plant-associated microbiome functions can be used to search for plant colonization markers [12,13]; this can be complemented by read-binning and assembly of bacterial genomes from plant-associated environments [14]. However, metagenomic datasets from different rhizospheres exhibit little overlap in plant-enriched functions [13,15].…”

Combining whole genome shotgun sequencing and rDNA amplicon analyses to improve detection of microbe-microbe interaction networks in plant leaves

“…Whole metagenome shotgun sequencing of DNA extracts has become an attractive tool for dissecting complex microbial communities, and databases and algorithms that support such efforts are being developed [11,12] . Shotgun sequencing supplies information on the total DNA content of microorganisms as opposed to a specific locus, which in principle enables us to ask many new types of questions [8,13,14] .…”

Temporal and spatial changes in phyllosphere microbiome of acacia trees growing in super arid environments

“…Recent study investigated the adaptation of three Negev desert plant species finding Bacteroidetes to dominated the leaves of H. scoparia for instance and were not abundant in the other species they investigated (7). Plants phyllosphere microbes were also found to differ among different habitat and climate conditions comparing between arid, semi-arid and temperate habitat (8). These microbes were also found to correlate with high temperature, droughts and UN radiation (9,10), regardless of their geographical distance (11).…”