Wild rice-associated Vibrio promotes plant growth and exhibits genomic and phenotypic plasticity for plant adaptations

Abstract

Vibrio is an important marine heterotroph, primarily studied for its pathogenesis or symbiotic relationship with marine organisms and humans. However, little is known about the association of vibrios with plants in brackish environments and their potential benefits. To address this knowledge gap, we focused on Vibrio porteresiae MSSRF30T and brackish-grown Pokkali rice as our research subjects for this study. MSSRF30T displays multifaceted plant beneficial traits, including nitrogen fixation, 1-aminocyclopropane-1-carboxylate (ACC) deaminase production, and zinc and tricalcium phosphate solubilization. Further, MSSRF30T efficiently colonizes the host roots and significantly improves the Pokkali rice growth in nitrogen-replete and nitrogen-limiting brackish conditions, highlighting its plant growth-promoting ability, a trait previously not well recognized in vibrios. Additionally, MSSRF30T can utilize various carbon-rich substrates derived from plant roots, demonstrating its metabolic adaptation to the plant rhizosphere niche. Using in planta root transcriptome analysis and whole-genome sequencing, we provide the first insights into how MSSRF30T interacts with Pokkali rice in brackish conditions. Additionally, we have identified several genome features for a plant-associated lifestyle, previously unreported in this genus. These features include plant expansin, PEP-CTERM surface anchoring with exopolysaccharides, plant-associated Hrp-type three secretion system, ACC deaminase production, PQQ-independent glucose dehydrogenase pathway for phosphate solubilization, plant-derived sugar/organic acids utilization operons, carbohydrate utilization loci, and specific plant depolymerizing CAZymes. Notably, MSSRF30T lacks key genome features critical for the animal association. Overall, this study adds new knowledge in the field of Vibrio biology, especially Vibrio-plant beneficial interactions, a relationship largely underexplored.