Diversity of phytobeneficial traits revealed by whole-genome analysis of worldwide-isolated phenazine-producing Pseudomonas spp.

Authors: BIESSY, ADRIEN - University Of Moncton; NOVINSCAK, AMY - University Of Moncton; BLOM, JOCHEN - Justus-Liebig University; LEGER, GENEVIEVE - University Of Moncton; Thomashow, Linda; CAZORLA, FRANCISCO - University Of Malaga; JOSIC, DRAGANA - Institute For Plant Protection And Environment; FILION, MARTIN - University Of Moncton

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/16/2018
Publication Date: 12/17/2018
Citation: Biessy, A., Novinscak, A., Blom, J., Leger, G., Thomashow, L.S., Cazorla, F.M., Josic, D., Filion, M. 2018. Diversity of phytobeneficial traits revealed by whole-genome analysis of worldwide-isolated phenazine-producing Pseudomonas spp. Environmental Microbiology. 21(1):437-455. https://doi.org/10.1111/1462-2920.14476.
DOI: https://doi.org/10.1111/1462-2920.14476

Interpretive Summary: The rhizosphere is the narrow zone of soil influenced by plant roots and is the theater of a warfare between soilborne plant pathogens and plant-beneficial bacteria. Plant-beneficial bacteria inhabiting the rhizosphere, such as members of the genus Pseudomonas, produce antibiotics that may harm plant pathogens, thus protecting crops against plant diseases. Antibiotic-producing Pseudomonas spp. have been extensively studied in the last 30 years as environmentally friendly alternatives to the use of synthetic pesticides. Numerous research teams have isolated Pseudomonas spp. strains producing a family of broad-spectrum antibiotics called phenazines. In addition to their deleterious effects against plant pathogens, phenazines also enhance the ability of plant-beneficial Pseudomonas spp. to persist in the rhizosphere, thereby prolonging their phytobeneficial effects. We sequenced the genomes of 58 phenazine-producing plant-beneficial Pseudomonas spp. strains isolated from a large diversity of host plants across the globe. Comparative genomics revealed a tremendous diversity of phytobeneficial traits, such as antibiotics biosynthetic clusters and plant-bacteria interaction traits. While contributing greatly to improve genomic resources available, our results pave the way for comparative analyses to identify new genetic determinants involved in biocontrol, plant-growth promotion and rhizosphere competence.

Technical Abstract: Plant-beneficial Pseudomonas spp. aggressively colonize the rhizosphere and display plant-growth promotion and/or disease-suppression activities. Some plant-beneficial Pseudomonas spp. strains within the P. fluorescens species complex produce phenazine derivatives, such as phenazine-1-carboxylic acid (PCA). These antimicrobial compounds are broadly inhibitory to numerous soilborne plant fungal and bacterial pathogens and also play a role in the ecological competence of plant-beneficial phenazine-producing Pseudomonas spp. During the last 30 years, hundreds of plant-beneficial Pseudomonas spp. have been isolated worldwide from the rhizosphere of many host plants. However, the genomic resources available for these organisms remain scarce as only a handful of genomes have been sequenced. To bridge this gap, we assembled a collection encompassing 63 strains representative of the worldwide diversity of plant-beneficial phenazine-producing Pseudomonas spp. In this study, we report the sequencing of 58 genomes using the PacBio RS II sequencing technology. Distributed among four different subgroups within the P. fluorescens species complex, the diversity of our collection is reflected by the large pangenome which account for 25,413 protein-coding genes. We identified genes and clusters encoding for numerous phytobeneficial traits, including antibiotics, siderophores and cyclic lipopeptides biosynthesis, some of which were previously unknown in these microorganisms. Finally, we gained insight into the evolutionary history of the phenazine biosynthetic operon. Given its diverse genomic context, it is likely that this operon was relocated several times during Pseudomonas evolution. Our findings acknowledge the tremendous diversity of plant-beneficial phenazine-producing Pseudomonas spp., paving the way for comparative analyses to identify new genetic determinants involved in biocontrol, plant-growth promotion and rhizosphere competence.