RpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant disease

<p>Contaminated fresh produce has been routinely linked to outbreaks of Salmonellosis. Multiple studies have identified Salmonella enterica factors associated with successful colonization of diverse plant niches and tissues. It has also been well documented that <em>S. enterica</em>...

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Main Authors: Lovelace, AH, Chen, H-C, Lee, S, Soufi, Z, Bota, P, Preston, GM, Kvitko, BH
Format: Journal article
Language:English
Published: Frontiers Media 2022
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author Lovelace, AH
Chen, H-C
Lee, S
Soufi, Z
Bota, P
Preston, GM
Kvitko, BH
author_facet Lovelace, AH
Chen, H-C
Lee, S
Soufi, Z
Bota, P
Preston, GM
Kvitko, BH
author_sort Lovelace, AH
collection OXFORD
description <p>Contaminated fresh produce has been routinely linked to outbreaks of Salmonellosis. Multiple studies have identified Salmonella enterica factors associated with successful colonization of diverse plant niches and tissues. It has also been well documented that <em>S. enterica</em> can benefit from the conditions generated during plant disease by host-compatible plant pathogens. In this study, we compared the capacity of two common <em>S. enterica</em> research strains, 14028s and LT2 (strain DM10000) to opportunistically colonize the leaf apoplast of two model plant hosts <em>Arabidopsis thaliana</em> and <em>Nicotiana benthamiana</em> during disease. While <em>S. enterica</em> 14028s benefited from co-colonization with plant-pathogenic <em>Pseudomonas syringae</em> in both plant hosts, <em>S. enterica</em> LT2 was unable to benefit from Pto co-colonization in <em>N. benthamiana</em>. Counterintuitively, LT2 grew more rapidly in ex planta <em>N. benthamiana</em> apoplastic wash fluid with a distinctly pronounced biphasic growth curve in comparison with 14028s. Using allelic exchange, we demonstrated that both the <em>N. benthamiana</em> infection-depedent colonization and apoplastic wash fluid growth phenotypes of LT2 were associated with mutations in the <em>S. enterica</em> <em>rpoS</em> stress-response sigma factor gene. Mutations of <em>S. enterica</em> <em>rpoS</em> have been previously shown to decrease tolerance to oxidative stress and alter metabolic regulation. We identified <em>rpoS</em>-dependent alterations in the utilization of L-malic acid, an abundant carbon source in <em>N. benthamiana</em> apoplastic wash fluid. We also present data consistent with higher relative basal reactive oxygen species (ROS) in <em>N. benthamiana</em> leaves than in A. thaliana leaves. The differences in basal ROS may explain the host-dependent disease co-colonization defect of the <em>rpoS</em>-mutated LT2 strain. Our results indicate that the conducive environment generated by pathogen modulation of the apoplast niche can vary from hosts to host even with a common disease-compatible pathogen.</p>
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spelling oxford-uuid:662002e3-b5db-4dfd-9ebd-2e303f8426442023-03-29T14:30:01ZRpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant diseaseJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:662002e3-b5db-4dfd-9ebd-2e303f842644EnglishSymplectic ElementsFrontiers Media2022Lovelace, AHChen, H-CLee, SSoufi, ZBota, PPreston, GMKvitko, BH<p>Contaminated fresh produce has been routinely linked to outbreaks of Salmonellosis. Multiple studies have identified Salmonella enterica factors associated with successful colonization of diverse plant niches and tissues. It has also been well documented that <em>S. enterica</em> can benefit from the conditions generated during plant disease by host-compatible plant pathogens. In this study, we compared the capacity of two common <em>S. enterica</em> research strains, 14028s and LT2 (strain DM10000) to opportunistically colonize the leaf apoplast of two model plant hosts <em>Arabidopsis thaliana</em> and <em>Nicotiana benthamiana</em> during disease. While <em>S. enterica</em> 14028s benefited from co-colonization with plant-pathogenic <em>Pseudomonas syringae</em> in both plant hosts, <em>S. enterica</em> LT2 was unable to benefit from Pto co-colonization in <em>N. benthamiana</em>. Counterintuitively, LT2 grew more rapidly in ex planta <em>N. benthamiana</em> apoplastic wash fluid with a distinctly pronounced biphasic growth curve in comparison with 14028s. Using allelic exchange, we demonstrated that both the <em>N. benthamiana</em> infection-depedent colonization and apoplastic wash fluid growth phenotypes of LT2 were associated with mutations in the <em>S. enterica</em> <em>rpoS</em> stress-response sigma factor gene. Mutations of <em>S. enterica</em> <em>rpoS</em> have been previously shown to decrease tolerance to oxidative stress and alter metabolic regulation. We identified <em>rpoS</em>-dependent alterations in the utilization of L-malic acid, an abundant carbon source in <em>N. benthamiana</em> apoplastic wash fluid. We also present data consistent with higher relative basal reactive oxygen species (ROS) in <em>N. benthamiana</em> leaves than in A. thaliana leaves. The differences in basal ROS may explain the host-dependent disease co-colonization defect of the <em>rpoS</em>-mutated LT2 strain. Our results indicate that the conducive environment generated by pathogen modulation of the apoplast niche can vary from hosts to host even with a common disease-compatible pathogen.</p>
spellingShingle Lovelace, AH
Chen, H-C
Lee, S
Soufi, Z
Bota, P
Preston, GM
Kvitko, BH
RpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant disease
title RpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant disease
title_full RpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant disease
title_fullStr RpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant disease
title_full_unstemmed RpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant disease
title_short RpoS contributes in a host-dependent manner to Salmonella colonization of the leaf apoplast during plant disease
title_sort rpos contributes in a host dependent manner to salmonella colonization of the leaf apoplast during plant disease
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