Paper · 2025 · mSystems

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

Kirti Kulanthaivel; Natarajan Rameshkumar

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claims
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verbatim quotes
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citations
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Open access · cc-by

Abstract

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 MSSRF30 T and brackish-grown Pokkali rice as our research subjects for this study. MSSRF30 T displays multifaceted plant beneficial traits, including nitrogen fixation, 1-aminocyclopropane-1-carboxylate (ACC) deaminase production, and zinc and tricalcium phosphate solubilization. Further, MSSRF30 T 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, MSSRF30 T 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 MSSRF30 T 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, MSSRF30 T 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. IMPORTANCE The genus Vibrio comprises over 150 species of marine heterotrophic bacteria, many of which are opportunistic pathogens affecting humans and marine animals. Most research has predominantly focused on pathogenic Vibrio species, often overlooking the significance of other Vibrio species inhabiting other ecological niches, such as plants, a relationship largely uncharacterized. This study focused on V. porteresiae MSSRF30 T and its relationship with brackish-grown Pokkali rice. We discovered that MSSRF30 T possesses multiple plant growth-promoting traits, effectively colonizes roots, and enhances plant growth in brackish conditions. Additionally, MSSRF30 T possesses several genome features commonly associated with plant-microbe interactions, previously unrecognized in Vibrio species, and lacks features typically associated with animal interactions, underscoring its specialized adaptation for plant niches. For the first time, this study highlights the beneficial interactions between Vibrio and plants, emphasizing their role in promoting plant growth and health in brackish environments.

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Claims 5

Observationobservedoriginal resultmeasured

Claim · model-written summary

Vibrio porteresiae MSSRF30 T fixes nitrogen, produces ACC deaminase and solubilizes zinc and tricalcium phosphate.

Taxon
Vibrio porteresiae MSSRF30 TVibrio porteresiaee1
Outcome
nitrogen fixation, 1-aminocyclopropane-1-carboxylate (ACC) deaminase production, and zinc and tricalcium phosphate solubilizatione0

Verbatim

e0

“MSSRF30 T displays multifaceted plant beneficial traits, including nitrogen fixation, 1-aminocyclopropane-1-carboxylate (ACC) deaminase production, and zinc and tricalcium phosphate solubilization.”

✓ located verbatim in the source · abstract, characters 423–620 · show in text ↑
e1

“Vibrio porteresiae MSSRF30 T”

✓ located verbatim in the source · abstract, characters 321–349 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

MSSRF30 T significantly improves Pokkali rice growth in nitrogen-replete and nitrogen-limiting brackish conditions.

Taxon
Pokkali ricee0
Treatment
MSSRF30 Te0
Interactor
MSSRF30 Te0symbiont
Outcome
Pokkali rice growthe0
Direction
improvese0
Qualifier
nitrogen-replete and nitrogen-limiting brackish conditionse0

Not reportedComparator

Verbatim

e0

“MSSRF30 T efficiently colonizes the host roots and significantly improves the Pokkali rice growth in nitrogen-replete and nitrogen-limiting brackish conditions”

✓ located verbatim in the source · abstract, characters 630–789 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

MSSRF30 T utilizes diverse carbon-rich plant-root substrates.

Taxon
Vibrio porteresiae MSSRF30 TVibrio porteresiaee1
Outcome
utilize various carbon-rich substrates derived from plant rootse0

Verbatim

e0

“MSSRF30 T can utilize various carbon-rich substrates derived from plant roots”

✓ located verbatim in the source · abstract, characters 905–982 · show in text ↑
e1

“Vibrio porteresiae MSSRF30 T”

✓ located verbatim in the source · abstract, characters 321–349 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Plant-associated genome features were identified in MSSRF30 T, including expansin, secretion and metabolic pathways.

Taxon
Vibrio porteresiae MSSRF30 TVibrio porteresiaee1
Outcome
genome features for a plant-associated lifestylee0

Verbatim

e0

“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.”

✓ located verbatim in the source · abstract, characters 1243–1729 · show in text ↑
e1

“Vibrio porteresiae MSSRF30 T”

✓ located verbatim in the source · abstract, characters 321–349 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

MSSRF30 T lacks key genome features for animal association.

Taxon
Vibrio porteresiae MSSRF30 TVibrio porteresiaee1
Outcome
key genome features critical for the animal associatione0

Verbatim

e0

“MSSRF30 T lacks key genome features critical for the animal association.”

✓ located verbatim in the source · abstract, characters 1739–1811 · show in text ↑
e1

“Vibrio porteresiae MSSRF30 T”

✓ located verbatim in the source · abstract, characters 321–349 · show in text ↑