The effect of root exudates on the transcriptome of rhizosphere Pseudomonas spp.

Authors: MAVRODI, OLGA - University Of Southern Mississippi; MCWILLIAMS, JANIECE - University Of Southern Mississippi; PETER, JACOB - University Of Southern Mississippi; BERIM, ANNA - Washington State University; HASSAN, KARL - University Of Newcastle; ELBOURNE, LIAM - Macquarie University; Letourneau, Melissa; GANG, DAVID - Washington State University; PAULSEN, IAN - Macquarie University; Weller, David; Thomashow, Linda; FLYNT, ALEX - University Of Southern Mississippi; MAVRODI, DMITRI - University Of Southern Mississippi

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/8/2021
Publication Date: 4/14/2021
Citation: Mavrodi, O.V., McWilliams, J.R., Peter, J.O., Berim, A., Hassan, K.A., Elbourne, L.D., LeTourneau, M., Gang, D.R., Paulsen, I.T., Weller, D.M., Thomashow, L.S., Flynt, A.S., Mavrodi, D.V. 2021. The effect of root exudates on the transcriptome of rhizosphere Pseudomonas spp.. Frontiers in Microbiology. 12. Article 651282. https://doi.org/10.3389/fmicb.2021.651282.
DOI: https://doi.org/10.3389/fmicb.2021.651282

Interpretive Summary: Plants live in close association with microorganisms that positively influence plant development, vigor, and fitness in response to pathogens and environmental stresses. Most of these plant-associated microbes are concentrated at the plant root-soil interface. Plant roots secrete carbon-rich exudates containing low molecular-weight metabolites, cell lysates and other secretions. These root exudates provide nutrients for soil microorganisms and modulate their interactions with host plants, but molecular details of this process are largely unresolved. Our study addressed this gap by focusing on the molecular dialogue between eight well-characterized strains of the Pseudomonas fluorescens group and Brachypodium distachyon, a model for economically important food, feed, forage, and biomass crops of the grass family. We collected and analyzed root exudates of B. distachyon and demonstrated the presence of multiple carbohydrates, amino acids, organic acids and phenolic compounds. The subsequent screening of root-associated bacteria revealed that many of these metabolites provide carbon and energy for the studied strains. Gene expression profiling of bacterial cultures amended with root exudates revealed changes in the expression of genes encoding numerous biosynthetic and compound-degrading enzymes, transporters, transcriptional regulators, stress response, and conserved hypothetical proteins. Almost half of the differentially expressed genes mapped to the variable part of the collective genome, of all of the strains reflecting the importance of the entire gene content in the adaptation of P. fluorescens to the rroot-associated lifestyle. Our results collectively reveal the diversity of cellular pathways and physiological responses underlying the establishment of mutual interactions between beneficial root-associated bacteria and their plant hosts.

Technical Abstract: Plants are meta-organisms or holobionts that live in association with microorganisms, which positively influence plant development, vigor, and fitness in response to pathogens and abiotic stressors. The bulk of the plant microbiome is concentrated belowground at the plant root-soil interface. Plant roots secrete carbon-rich rhizodeposits containing primary and secondary low molecular-weight metabolites, lysates, and mucilages. It is thought that these root exudates provide nutrients for soil microorganisms and modulate their affinity towards host plants, but molecular details of this process are largely unresolved. Our study addressed this gap by focusing on the molecular dialogue between eight well-characterized strains of the Pseudomonas fluorescens group and Brachypodium distachyon, a model for economically important food, feed, forage, and biomass crops of the grass family. We collected and analyzed root exudates of B. distachyon and demonstrated the presence of multiple carbohydrates, amino acids, organic acids and phenolic compounds. The subsequent screening of bacteria by Biolog Phenotype MicroArrays revealed that many of these metabolites provide carbon and energy for the studied Pseudomonas strains. The RNA-seq profiling of bacterial cultures amended with root exudates revealed changes in the expression of genes encoding numerous catabolic and anabolic enzymes, transporters, transcriptional regulators, stress response, and conserved hypothetical proteins. Almost half of the differentially expressed genes mapped to the variable part of the strains’ pangenome, reflecting the importance of the variable gene content in the adaptation of P. fluorescens to the rhizosphere lifestyle. Our results collectively reveal the diversity of cellular pathways and physiological responses underlying the establishment of mutualistic interactions between beneficial rhizobacteria and their plant hosts.