Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere

Abstract While the physiological and transcriptional response of the host to biotic and abiotic stresses have been intensely studied, little is known about the resilience of associated microbiomes and their contribution towards tolerance or response to these stresses. We evaluated the impact of elev...

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Main Authors: Rishi Bhandari, Alvaro Sanz-Saez, Courtney P. Leisner, Neha Potnis
Format: Article
Language:English
Published: Oxford University Press 2023-03-01
Series:ISME Communications
Online Access:https://doi.org/10.1038/s43705-023-00232-w
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author Rishi Bhandari
Alvaro Sanz-Saez
Courtney P. Leisner
Neha Potnis
author_facet Rishi Bhandari
Alvaro Sanz-Saez
Courtney P. Leisner
Neha Potnis
author_sort Rishi Bhandari
collection DOAJ
description Abstract While the physiological and transcriptional response of the host to biotic and abiotic stresses have been intensely studied, little is known about the resilience of associated microbiomes and their contribution towards tolerance or response to these stresses. We evaluated the impact of elevated tropospheric ozone (O3), individually and in combination with Xanthomonas perforans infection, under open-top chamber field conditions on overall disease outcome on resistant and susceptible pepper cultivars, and their associated microbiome structure, function, and interaction network across the growing season. Pathogen infection resulted in a distinct microbial community structure and functions on the susceptible cultivar, while concurrent O3 stress did not further alter the community structure, and function. However, O3 stress exacerbated the disease severity on resistant cultivar. This altered diseased severity was accompanied by enhanced heterogeneity in associated Xanthomonas population counts, although no significant shift in overall microbiota density, microbial community structure, and function was evident. Microbial co-occurrence networks under simultaneous O3 stress and pathogen challenge indicated a shift in the most influential taxa and a less connected network, which may reflect the altered stability of interactions among community members. Increased disease severity on resistant cultivar may be explained by such altered microbial co-occurrence network, indicating the altered microbiome-associated prophylactic shield against pathogens under elevated O3. Our findings demonstrate that microbial communities respond distinctly to individual and simultaneous stressors, in this case, O3 stress and pathogen infection, and can play a significant role in predicting how plant-pathogen interactions would change in the face of climate change.
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spelling doaj.art-210a992a18bc46f1b36decc3e0bfe3dd2024-04-03T06:06:20ZengOxford University PressISME Communications2730-61512023-03-013111310.1038/s43705-023-00232-wXanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphereRishi Bhandari0Alvaro Sanz-Saez1Courtney P. Leisner2Neha Potnis3Department of Entomology and Plant Pathology, Auburn UniversityDepartment of Crop, Soil and Environmental Sciences, Auburn UniversityDepartment of Biological Sciences, Auburn UniversityDepartment of Entomology and Plant Pathology, Auburn UniversityAbstract While the physiological and transcriptional response of the host to biotic and abiotic stresses have been intensely studied, little is known about the resilience of associated microbiomes and their contribution towards tolerance or response to these stresses. We evaluated the impact of elevated tropospheric ozone (O3), individually and in combination with Xanthomonas perforans infection, under open-top chamber field conditions on overall disease outcome on resistant and susceptible pepper cultivars, and their associated microbiome structure, function, and interaction network across the growing season. Pathogen infection resulted in a distinct microbial community structure and functions on the susceptible cultivar, while concurrent O3 stress did not further alter the community structure, and function. However, O3 stress exacerbated the disease severity on resistant cultivar. This altered diseased severity was accompanied by enhanced heterogeneity in associated Xanthomonas population counts, although no significant shift in overall microbiota density, microbial community structure, and function was evident. Microbial co-occurrence networks under simultaneous O3 stress and pathogen challenge indicated a shift in the most influential taxa and a less connected network, which may reflect the altered stability of interactions among community members. Increased disease severity on resistant cultivar may be explained by such altered microbial co-occurrence network, indicating the altered microbiome-associated prophylactic shield against pathogens under elevated O3. Our findings demonstrate that microbial communities respond distinctly to individual and simultaneous stressors, in this case, O3 stress and pathogen infection, and can play a significant role in predicting how plant-pathogen interactions would change in the face of climate change.https://doi.org/10.1038/s43705-023-00232-w
spellingShingle Rishi Bhandari
Alvaro Sanz-Saez
Courtney P. Leisner
Neha Potnis
Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere
ISME Communications
title Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere
title_full Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere
title_fullStr Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere
title_full_unstemmed Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere
title_short Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere
title_sort xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere
url https://doi.org/10.1038/s43705-023-00232-w
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