Long-term irrigation affects the dynamics and activity of the wheat rhizosphere microbiome

Authors: MAVRODI, DMITRI - University Of Southern Mississippi; MAVRODI, OLGA - University Of Southern Mississippi; ELBOURNE, LIAM - Macquarie University; TETU, SASHA - Macquarie University; BONSALL, ROBERT - Washington State University; PAREJKO, JAMES - Washington State University; YANG, MINGMING - Washington State University; PAULSEN, IAN - Macquarie University; Weller, David; Thomashow, Linda

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/28/2018
Publication Date: 3/21/2018
Citation: Mavrodi, D., Mavrodi, O., Elbourne, L., Tetu, S., Bonsall, R., Parejko, J., Yang, M., Paulsen, I., Weller, D.M., Thomashow, L.S. 2018. Long-term irrigation affects the dynamics and activity of the wheat rhizosphere microbiome. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2018.00345.
DOI: https://doi.org/10.3389/fpls.2018.00345

Interpretive Summary: This manuscript addresses unresolved questions stemming from the unprecedented discovery in 2012 of biologically relevant concentrations of the natural antibiotic phenazine-1-carboxylic acid (PCA) on the roots of dryland wheat across 1.56-million hectares on the Columbia Plateau in the Inland Pacific Northwest, USA. We present the results of a three-year field study documenting the establishment and activity of microbial communities on the roots of irrigated and dryland (rainfed) wheat, including the impact of soil moisture on the population dynamics and activity of the indigenous phenazine-producing (Phz+) microbial populations. We show that whereas three seasons of irrigation had only a slight effect on the overall diversity within the microbiome, they led to significant differences in the relative abundances of specific groups of bacteria, including multiple groups of Bacteroidetes and Proteobacteria and taxa with known plant growth-promoting activity. In particular, irrigation adversely affected Phz+ bacteria as manifested by significantly reduced plant colonization frequencies and levels of PCA over time. Nonetheless, the persistence in dryland plots of PCA over the entire growing season provided evidence that the production of biologically active compounds on wheat roots is a sustained and highly dynamic process. Thus, our long-term study provides insights into how the availability of water in a semi-arid agroecosystem shapes the composition and activity of the belowground wheat microbiome.

Technical Abstract: The Inland Pacific Northwest encompasses 1.6 million cropland hectares and is a major wheat-producing area in the western United States. The climate throughout the region is semi-arid, making the availability of water a significant challenge for agriculture. We conducted a three-year field study involving wheat grown in adjacent irrigated and dryland (rainfed) plots established in Lind, Washington State. We used deep amplicon sequencing of the V4 region of the 16S rDNA to characterize the responses of the wheat rhizosphere microbiome to overhead irrigation. We also characterized the population dynamics and activity of indigenous Phz+ rhizobacteria that produce the antibiotic phenazine-1-carboxylic acid (PCA) and contribute to the natural suppression of soilborne pathogens of wheat. Irrigation affected the Phz+ rhizobacteria adversely, which was evident from the significantly reduced plant colonization frequency and levels of PCA in the field. The observed differences were reproducible and amplified over the course of the study, thus identifying soil moisture as a critical abiotic factor that influences the dynamics and activity of indigenous Phz+ communities. The three seasons of irrigation had a slight effect on the overall diversity within the rhizosphere microbiome but led to significant differences in the relative abundances of specific OTUs. In particular, irrigation differentially affected multiple groups of Bacteroidetes and Proteobacteria, including taxa with known plant growth-promoting activity. Analysis of environmental variables revealed that the separation between irrigated and dryland treatments was due to changes in the water potential ('m) and pH. In contrast, the temporal changes in the composition of the rhizosphere microbiome correlated with temperature and precipitation. In summary, our long-term study provides insights into how the availability of water in a semi-arid agroecosystem shapes the belowground wheat microbiome.