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Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations

Hemipteran insects are ubiquitous inhabitants of the phyllosphere. Changes in microbial phyllosphere communities have recently been demonstrated following infestation by Macrosteles quadrilineatus (Aster Leafhopper). Although epiphytic Salmonella enterica populations naturally decline in the phyllos...

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Autores principales: Harrod, Victoria L., Groves, Russell L., Guillemette, Ellie G., Barak, Jeri D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9122940/
https://www.ncbi.nlm.nih.gov/pubmed/35595751
http://dx.doi.org/10.1038/s41598-022-11750-3
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author Harrod, Victoria L.
Groves, Russell L.
Guillemette, Ellie G.
Barak, Jeri D.
author_facet Harrod, Victoria L.
Groves, Russell L.
Guillemette, Ellie G.
Barak, Jeri D.
author_sort Harrod, Victoria L.
collection PubMed
description Hemipteran insects are ubiquitous inhabitants of the phyllosphere. Changes in microbial phyllosphere communities have recently been demonstrated following infestation by Macrosteles quadrilineatus (Aster Leafhopper). Although epiphytic Salmonella enterica populations naturally decline in the phyllosphere of plants, M. quadrilineatus infestation facilitated the growth of the bacterial pathogen populations. Here, we demonstrate that cellular damage by insect stylet penetration results in a localized beneficial niche on the leaf surface, leading to enhanced S. enterica populations. We measured S. enterica populations and colonization patterns on plants infested with Hemipterans with distinct feeding behaviors. M. quadrilineatus infestation resulted in higher solute leakage and significantly greater bacterial populations than plants absent of insects. Following immigration via contaminated irrigation water, the highest populations of S. enterica are naturally found on the tips of tomato leaflets. We discovered M. quadrilineatus feeding preference altered the natural distribution of S. enterica populations, and that the presence of S. enterica altered the distribution of probing attempts. These findings elucidate how cellular damage resulting from insect feeding drives changes in bacterial colonization of the phyllosphere.
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spelling pubmed-91229402022-05-22 Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations Harrod, Victoria L. Groves, Russell L. Guillemette, Ellie G. Barak, Jeri D. Sci Rep Article Hemipteran insects are ubiquitous inhabitants of the phyllosphere. Changes in microbial phyllosphere communities have recently been demonstrated following infestation by Macrosteles quadrilineatus (Aster Leafhopper). Although epiphytic Salmonella enterica populations naturally decline in the phyllosphere of plants, M. quadrilineatus infestation facilitated the growth of the bacterial pathogen populations. Here, we demonstrate that cellular damage by insect stylet penetration results in a localized beneficial niche on the leaf surface, leading to enhanced S. enterica populations. We measured S. enterica populations and colonization patterns on plants infested with Hemipterans with distinct feeding behaviors. M. quadrilineatus infestation resulted in higher solute leakage and significantly greater bacterial populations than plants absent of insects. Following immigration via contaminated irrigation water, the highest populations of S. enterica are naturally found on the tips of tomato leaflets. We discovered M. quadrilineatus feeding preference altered the natural distribution of S. enterica populations, and that the presence of S. enterica altered the distribution of probing attempts. These findings elucidate how cellular damage resulting from insect feeding drives changes in bacterial colonization of the phyllosphere. Nature Publishing Group UK 2022-05-20 /pmc/articles/PMC9122940/ /pubmed/35595751 http://dx.doi.org/10.1038/s41598-022-11750-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Harrod, Victoria L.
Groves, Russell L.
Guillemette, Ellie G.
Barak, Jeri D.
Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations
title Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations
title_full Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations
title_fullStr Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations
title_full_unstemmed Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations
title_short Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations
title_sort salmonella enterica changes macrosteles quadrilineatus feeding behaviors resulting in altered s. enterica distribution on leaves and increased populations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9122940/
https://www.ncbi.nlm.nih.gov/pubmed/35595751
http://dx.doi.org/10.1038/s41598-022-11750-3
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