Plant Hosts Modify Belowground Microbial Community Response to Extreme Drought

Abstract

Drought stress negatively impacts microbial activity, but the magnitude of stress responses is likely dependent on a diversity of belowground interactions. Populus trichocarpa individuals and no-plant bulk soils were exposed to extended drought (∼0.03% gravimetric water content [GWC] after 12 days), rewet, and a 12-day "recovery" period to determine the effects of plant presence in mediating soil microbiome stability to water stress. Plant metabolomic analyses indicated that drought exposure increased host investment in C and N metabolic pathways (amino acids, fatty acids, phenolic glycosides) regardless of recovery. Several metabolites positively correlated with root-associated microbial alpha-diversity, but not those of soil communities. Soil bacterial community composition shifted with P. trichocarpa presence and with drought relative to irrigated controls, whereas soil fungal composition shifted only with plant presence. However, root fungal communities strongly shifted with drought, whereas root bacterial communities changed to a lesser degree. The proportion of bacterial water-stress opportunistic operational taxonomic units (OTUs) (enriched counts in drought) was high (∼11%) at the end of drying phases and maintained after rewet and recovery phases in bulk soils, but it declined over time in soils with plants present. For root fungi, opportunistic OTUs were high at the end of recovery in drought treatments (∼17% abundance), although relatively not responsive in soils, particularly planted soils (<0.5% abundance for sensitive or opportunistic). These data indicate that plants modulate soil and root-associated microbial drought responses via tight plant-microbe linkages during extreme drought scenarios, but trajectories after extreme drought vary with plant habitat and microbial functional groups.IMPORTANCE Climate change causes significant alterations in precipitation and temperature regimes that are predicted to become more extreme throughout the next century. Microorganisms are important members within ecosystems, and how they respond to these changing abiotic stressors has large implications for the functioning of ecosystems, the recycling of nutrients, and the health of the aboveground plant community. Drought stress negatively impacts microbial activity, but the magnitude of this stress response may be dependent on above- and belowground interactions. This study demonstrates that beneficial associations between plants and microbes can enhance tolerance to abiotic stress.

Keywords: Populus; bacteria; drought; fungi.

FIG 1

Mean ± standard error (SE) soil gravimetric water content (GWC) of irrigated control and drought treatments (A) which underwent a drought period resulting in significant leaf wilt, a rewet, and recovery period with irrigation maintained at rewet (images provided in panel B). Plant metabolomic profiling of phenolic glycosides (C), amino acids (D), fatty acids (E), and sugar alcohols (F) indicates plants underwent significant metabolic changes after drought. Letters denote pairwise differences for a drought-by-time significant interaction for amino acids only. Other metabolites differed only by drought treatment and not by time. Blue points indicate control treatments, green points indicate drought treatments, and shading indicates increases from drying through rewet to recovery periods.

FIG 2

Centroids (mean ordination scores) with standard error (SE) bars of principal-component analysis (PCA) for bacteria/archaea (A and C) and fungal communities (B and D) in soils (A and B) and roots (C and D). Raw OTU counts were centered log-ratio transformed, and Euclidean distances were calculated and input in PCAs. Symbols represent plant presence or no presence for bulk soils (circle = plant presence, triangle = no plants), colors denote treatment (blue = control, green = drought), and shading from light to dark refers to time of sampling.

FIG 3

Relative abundance of dominant (≥1.0%) bacterial/archaeal phyla (and class for Proteobacteria) (A to C) and fungal phyla (D to F) across drying, rewet, and recovery periods within bulk soils (A and D), planted soils (B and E), and root endospheres (C and F).

FIG 4

The absolute log₂ fold value change of DESeq-detected differential bacterial/archaeal OTUs that were opportunistic (enriched in drought versus controls) or sensitive (depleted in drought versus controls) over time at end of drying (A and D), rewet (B and E), and recovery (C and F) for bulk soils (A to C) and planted soils (D to E). Each dot represented a significantly differentially abundant OTU. Only one bacterial OTU over time was differentially abundant in roots. Asterisks denote if strategy (sensitivity or opportunism) fold change significantly differed at each time for bulk soils and planted soil separately.

FIG 5

The absolute log₂ fold value change of DESeq-detected differential fungal OTUs that were opportunistic (enriched in drought versus controls) or sensitive (depleted in drought versus controls) over time at end of drying (A), rewet (B), and recovery (C) for roots. Each dot represents a significant differentially abundant OTU. No sensitive OTUs were detected for fungal communities at rewet (B). Asterisks denote if strategy (sensitivity or opportunism) fold change significantly differed at each time.