Severe and mild drought cause distinct phylogenetically linked shifts in the blue grama (Bouteloua gracilis) rhizobiome

Authors: GOEMANN, HANNAH - Montana State University; ULRICH, DANIELLE - Montana State University; PEYTON, BRENT - Montana State University; GALLEGOS-GRAVES, LA VERNE - Los Alamos National Research Laboratory; Mueller, Rebecca

Submitted to: Frontiers in Microbiomes
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/18/2023
Publication Date: 1/11/2024
Citation: Goemann, H.M., Ulrich, D.E., Peyton, B.M., Gallegos-Graves, L., Mueller, R.C. 2024. Severe and mild drought cause distinct phylogenetically linked shifts in the blue grama (Bouteloua gracilis) rhizobiome. Frontiers in Microbiomes. 2. Article 1310790. https://doi.org/10.3389/frmbi.2023.1310790.
DOI: https://doi.org/10.3389/frmbi.2023.1310790

Interpretive Summary: Understanding the relationships among plants, microbes and climate is increasingly important given the critical roles microbes play in plant health, and predicted increases in climate disturbances, such as drought. Here, we examined the effects of drought on the rhizosphere microbiome of a widespread native perennial grass with high drought tolerance, Bouteloua gracilis, and linked those responses to shifts in the root exudates produced by plants suffering from water deficits. Responses to experiment drought were non-randomly distributed across the phylogenies of both bacteria and archaea and fungi, altering the relative abundances of organisms that play key roles in nitrogen cycling and nutrient uptake. Weak correlations were found between microbiome composition and root exudate compounds with strong responses to drought. Together these findings show synchrony in plant and microbiome responses to drought that could have broader scale effects of ecosystem processes.

Technical Abstract: Plants rely on a diverse rhizobiome to regulate nutrient acquisition and plant health. With increasing severity and frequency of droughts worldwide due to climate change, untangling the relationships between plants and their rhizobiomes is vital to maintaining agricultural productivity and protecting ecosystem diversity. While some plant physiological responses to drought are generally conserved, patterns of root exudation (release of small metabolites shown to influence microbes) and the consequential effects on the plant rhizobiome can differ widely across plant species under drought. To address this knowledge gap, we conducted a greenhouse study using blue grama (Bouteloua gracilis), a drought-tolerant C4 grass native to shortgrass prairie across North American plains, as a model organism to study the effect of increasing drought severity (ambient, mild drought, severe drought) on root exudation and the rhizobiome. Our previous results demonstrated physiological effects of increasing drought severity including an increase in belowground carbon allocation through root exudation and shifts in root exudate composition concurrent with the gradient of drought severity. This work is focused on the rhizobiome community structure using targeted sequencing and found that mild and severe drought resulted in unique shifts in the bacterial + archaeal and fungal communities relative to ambient, non-droughted controls. Specifically, using the change in relative abundance between ambient and drought conditions for each ZOTU as a surrogate for population-scale drought tolerance (e.g., as a response trait), we found that rhizobiome response to drought was non-randomly distributed across the phylogenies of both communities, suggesting that Planctomycetota, Thermoproteota (formerly Thaumarchaeota), and the Glomeromycota were the primary clades driving these changes. Correlation analyses indicated marginally positive correlations between droughted community composition and a select few root exudate compounds previously implicated in plant drought responses including pyruvic acid, D-glucose, L-threonine, and myoinositol. This study advances our understanding of the effects of drought on plant-microbe interactions and provides a platform for hypothesis generation for targeted functional studies of specific taxa involved in plant drought response.