Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species

Abstract

Desert plants are hypothesized to survive the environmental stress inherent to these regions in part thanks to symbioses with microorganisms, and yet these microbial species, the communities they form, and the forces that influence them are poorly understood. Here we report the first comprehensive investigation of the microbial communities associated with species of Agave, which are native to semiarid and arid regions of Central and North America and are emerging as biofuel feedstocks. We examined prokaryotic and fungal communities in the rhizosphere, phyllosphere, leaf and root endosphere, as well as proximal and distal soil samples from cultivated and native agaves, through Illumina amplicon sequencing. Phylogenetic profiling revealed that the composition of prokaryotic communities was primarily determined by the plant compartment, whereas the composition of fungal communities was mainly influenced by the biogeography of the host species. Cultivated A. tequilana exhibited lower levels of prokaryotic diversity compared with native agaves, although no differences in microbial diversity were found in the endosphere. Agaves shared core prokaryotic and fungal taxa known to promote plant growth and confer tolerance to abiotic stress, which suggests common principles underpinning Agave-microbe interactions.

Keywords: Agave; biogeography; cultivation; desert; iTags; microbial diversity; plant microbiome; plant-microbe interactions.

Figure 1

Experimental design of this study. (a) Study sites and biogeography of selected Agave species. (b) The six samples analyzed from each plant. (c) Pictures of A. tequilana, A. salmiana and A. deserti. (d, e) Venn diagrams of shared prokaryotic (red) and fungal (blue) operational taxonomic units across groups of sample types and across Agave species.

Figure 2

Estimated Shannon (H’) index in the (a) prokaryotic and (b) fungal communities associated with each sample type for the three Agave species, shown with ± SE. Superscripts (a–d) indicate significant differences in the marked plant compartment between plant species, while superscripts (e–g) indicate significant differences between sample types associated with a plant species. Statistical support is detailed in Supporting Information Table S1.

Figure 3

Order‐level relative abundance plots of prokaryotic (a, c, e) and fungal (b, d, f) communities by sample type for A. tequilana (a, b), A. salmiana (c, d), and A. deserti (e, f). Asterisks in the legend indicate taxonomic bins containing operational taxonomic units that could not be resolved to the order level.

Figure 4

Nonmetric multidimensional scaling (NMDS) plots for Bray–Curtis distances of prokaryotic and fungal communities associated with Agave species. (a, b) All six sample types; (c, d) only rhizospheres and phyllospheres; (e, f) only root and leaf endospheres.

Figure 5

Relative frequency versus relative abundance of major operational taxonomic unit (OTU) players associated with the root endosphere of agaves for (a) prokaryotes and (b) fungi. Arrows indicate most abundant genera in each case. The number of OTUs and the number of samples (n) are indicated in the bottom right corner of each plot.

Figure 6

Endophytic core of agaves. (a) Nonmetric multidimensional scaling (NMDS) plot of the endophytic prokaryotic communities from Agave tequilana and A. salmiana; grey ellipses note dry season samples. As.Ma, A. salmiana from site El Magyuel; As.Sf, A. salmiana from San Felipe; At.Am, A. tequilana from Amatitan; At.Pe, A. tequilana from Penjamo. (b) Shared core bacterial operational taxonomic units (belonging to Actinobacteria, Bacilli, and Alpha‐, Beta‐ and Gammaproteobacteria) in the root and leaf endosphere of agaves in the dry and rainy seasons. Kruskal–Wallis test (leaf: χ² = 7.5; df = 1; P‐value = 0.00617 for A. tequilana; χ² = 4.5; df = 1; P‐value = 0.03389 for A. salmiana; root: χ² = 8.31; df = 1, P‐value = 0.0039 for A. tequilana). Relative abundance profiles of the core prokaryotic taxa, indicated in the legend ± SD for the total relative abundance, are displayed.