Bacterial rhizosphere colonization is critical for phytobeneficial rhizobacteria such as phenazine-producing Pseudomonas spp. To better understand this colonization process, potential metabolic and genomic determinants required for rhizosphere colonization were identified using a collection of 60 phenazine-producing Pseudomonas strains isolated from multiple plant species and representative of the worldwide diversity. Arabidopsis thaliana and Solanum tuberosum (potato) were used as host plants. Bacterial rhizosphere colonization was measured by quantitative PCR using a newly designed primer pair and TaqMan probe targeting a conserved region of the phenazine biosynthetic operon. The metabolic abilities of the strains were assessed on 758 substrates using Biolog phenotype microarray technology. These data, along with available genomic sequences for all strains, were analyzed in light of rhizosphere colonization. Strains belonging to the P. chlororaphis subgroup colonized the rhizospheres of both plants more efficiently than strains belonging to the P. fluorescens subgroup. Metabolic results indicated that the ability to use amines and amino acids was associated with an increase in rhizosphere colonization capability in A. thaliana and/or in S. tuberosum. The presence of multiple genetic determinants in the genomes of the different strains involved in catabolic pathways and plant-microbe and microbe-microbe interactions correlated with increased or decreased rhizosphere colonization capabilities in both plants. These results suggest that the metabolic and genomic traits found in different phenazine-producing Pseudomonas strains reflect their rhizosphere competence in A. thaliana and S. tuberosum. Interestingly, most of these traits are associated with similar rhizosphere colonizing capabilities in both plant species. IMPORTANCE Rhizosphere colonization is crucial for plant growth promotion and biocontrol by antibiotic-producing Pseudomonas spp. This colonization process relies on different bacterial determinants which partly remain to be uncovered. In this study, we combined a metabolic and a genomic approach to decipher new rhizosphere colonization determinants which could improve our understanding of this process in Pseudomonas spp. Using 60 distinct strains of phenazine-producing Pseudomonas spp., we show that rhizosphere colonization abilities correlated with both metabolic and genomic traits when these bacteria were inoculated on two distant plants, Arabidopsis thaliana and Solanum tuberosum. Key metabolic and genomic determinants presumably required for efficient colonization of both plant species were identified. Upon further validation, these targets could lead to the development of simple screening tests to rapidly identify efficient rhizosphere colonizers.

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