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Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots

In spite of its relevance as a foodborne pathogen, we have limited knowledge about Listeria monocytogenes in the environment. L. monocytogenes outbreaks have been linked to fruits and vegetables; thus, a better understanding of the factors influencing its ability to colonize plants is important. We...

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Autores principales: Schoenborn, Alexi A., Clapper, Haley, Eckshtain-Levi, Noam, Shank, Elizabeth A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579980/
https://www.ncbi.nlm.nih.gov/pubmed/34550783
http://dx.doi.org/10.1128/AEM.01411-21
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author Schoenborn, Alexi A.
Clapper, Haley
Eckshtain-Levi, Noam
Shank, Elizabeth A.
author_facet Schoenborn, Alexi A.
Clapper, Haley
Eckshtain-Levi, Noam
Shank, Elizabeth A.
author_sort Schoenborn, Alexi A.
collection PubMed
description In spite of its relevance as a foodborne pathogen, we have limited knowledge about Listeria monocytogenes in the environment. L. monocytogenes outbreaks have been linked to fruits and vegetables; thus, a better understanding of the factors influencing its ability to colonize plants is important. We tested how environmental factors and other soil- and plant-associated bacteria influenced L. monocytogenes’ ability to colonize plant roots using Arabidopsis thaliana seedlings in a hydroponic growth system. We determined that the successful root colonization of L. monocytogenes 10403S was modestly but significantly enhanced by the bacterium being pregrown at higher temperatures, and this effect was independent of the biofilm and virulence regulator PrfA. We tested 14 rhizosphere-derived bacteria for their impact on L. monocytogenes 10403S, identifying one that enhanced and 10 that inhibited the association of 10403S with plant roots. We also characterized the outcomes of these interactions under both coinoculation and invasion conditions. We characterized the physical requirements of five of these rhizobacteria to impact the association of L. monocytogenes 10403S with roots, visualizing one of these interactions by microscopy. Furthermore, we determined that two rhizobacteria (one an inhibitor, the other an enhancer of 10403S root association) were able to similarly impact 10 different L. monocytogenes strains, indicating that the effects of these rhizobacteria on L. monocytogenes are not strain specific. Taken together, our results advance our understanding of the parameters that affect L. monocytogenes plant root colonization, knowledge that may enable us to deter its association with and, thus, downstream contamination of, food crops. IMPORTANCE Listeria monocytogenes is ubiquitous in the environment, being found in or on soil, water, plants, and wildlife. However, little is known about the requirements for L. monocytogenes’ existence in these settings. Recent L. monocytogenes outbreaks have been associated with contaminated produce; thus, we used a plant colonization model to investigate factors that alter L. monocytogenes’ ability to colonize plant roots. We show that L. monocytogenes colonization of roots was enhanced when grown at higher temperatures prior to inoculation but did not require a known regulator of virulence and biofilm formation. Additionally, we identified several rhizobacteria that altered the ability of 11 different strains of L. monocytogenes to colonize plant roots. Understanding the factors that impact L. monocytogenes physiology and growth will be crucial for finding mechanisms (whether chemical or microbial) that enable its removal from plant surfaces to reduce L. monocytogenes contamination of produce and eliminate foodborne illness.
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spelling pubmed-85799802021-11-18 Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots Schoenborn, Alexi A. Clapper, Haley Eckshtain-Levi, Noam Shank, Elizabeth A. Appl Environ Microbiol Environmental Microbiology In spite of its relevance as a foodborne pathogen, we have limited knowledge about Listeria monocytogenes in the environment. L. monocytogenes outbreaks have been linked to fruits and vegetables; thus, a better understanding of the factors influencing its ability to colonize plants is important. We tested how environmental factors and other soil- and plant-associated bacteria influenced L. monocytogenes’ ability to colonize plant roots using Arabidopsis thaliana seedlings in a hydroponic growth system. We determined that the successful root colonization of L. monocytogenes 10403S was modestly but significantly enhanced by the bacterium being pregrown at higher temperatures, and this effect was independent of the biofilm and virulence regulator PrfA. We tested 14 rhizosphere-derived bacteria for their impact on L. monocytogenes 10403S, identifying one that enhanced and 10 that inhibited the association of 10403S with plant roots. We also characterized the outcomes of these interactions under both coinoculation and invasion conditions. We characterized the physical requirements of five of these rhizobacteria to impact the association of L. monocytogenes 10403S with roots, visualizing one of these interactions by microscopy. Furthermore, we determined that two rhizobacteria (one an inhibitor, the other an enhancer of 10403S root association) were able to similarly impact 10 different L. monocytogenes strains, indicating that the effects of these rhizobacteria on L. monocytogenes are not strain specific. Taken together, our results advance our understanding of the parameters that affect L. monocytogenes plant root colonization, knowledge that may enable us to deter its association with and, thus, downstream contamination of, food crops. IMPORTANCE Listeria monocytogenes is ubiquitous in the environment, being found in or on soil, water, plants, and wildlife. However, little is known about the requirements for L. monocytogenes’ existence in these settings. Recent L. monocytogenes outbreaks have been associated with contaminated produce; thus, we used a plant colonization model to investigate factors that alter L. monocytogenes’ ability to colonize plant roots. We show that L. monocytogenes colonization of roots was enhanced when grown at higher temperatures prior to inoculation but did not require a known regulator of virulence and biofilm formation. Additionally, we identified several rhizobacteria that altered the ability of 11 different strains of L. monocytogenes to colonize plant roots. Understanding the factors that impact L. monocytogenes physiology and growth will be crucial for finding mechanisms (whether chemical or microbial) that enable its removal from plant surfaces to reduce L. monocytogenes contamination of produce and eliminate foodborne illness. American Society for Microbiology 2021-11-10 /pmc/articles/PMC8579980/ /pubmed/34550783 http://dx.doi.org/10.1128/AEM.01411-21 Text en Copyright © 2021 Schoenborn et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Environmental Microbiology
Schoenborn, Alexi A.
Clapper, Haley
Eckshtain-Levi, Noam
Shank, Elizabeth A.
Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots
title Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots
title_full Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots
title_fullStr Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots
title_full_unstemmed Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots
title_short Rhizobacteria Impact Colonization of Listeria monocytogenes on Arabidopsis thaliana Roots
title_sort rhizobacteria impact colonization of listeria monocytogenes on arabidopsis thaliana roots
topic Environmental Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579980/
https://www.ncbi.nlm.nih.gov/pubmed/34550783
http://dx.doi.org/10.1128/AEM.01411-21
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