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Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology

IncP-1 plasmids, first isolated from clinical specimens (R751, RP4), are recognized as important vectors spreading antibiotic resistance genes. The abundance of IncP-1 plasmids in the environment, previously reported, suggested a correlation with anthropogenic pollution. Unexpectedly, qPCR-based det...

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Autores principales: Shintani, Masaki, Nour, Eman, Elsayed, Tarek, Blau, Khald, Wall, Inessa, Jechalke, Sven, Spröer, Cathrin, Bunk, Boyke, Overmann, Jörg, Smalla, Kornelia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7728920/
https://www.ncbi.nlm.nih.gov/pubmed/33329469
http://dx.doi.org/10.3389/fmicb.2020.590776
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author Shintani, Masaki
Nour, Eman
Elsayed, Tarek
Blau, Khald
Wall, Inessa
Jechalke, Sven
Spröer, Cathrin
Bunk, Boyke
Overmann, Jörg
Smalla, Kornelia
author_facet Shintani, Masaki
Nour, Eman
Elsayed, Tarek
Blau, Khald
Wall, Inessa
Jechalke, Sven
Spröer, Cathrin
Bunk, Boyke
Overmann, Jörg
Smalla, Kornelia
author_sort Shintani, Masaki
collection PubMed
description IncP-1 plasmids, first isolated from clinical specimens (R751, RP4), are recognized as important vectors spreading antibiotic resistance genes. The abundance of IncP-1 plasmids in the environment, previously reported, suggested a correlation with anthropogenic pollution. Unexpectedly, qPCR-based detection of IncP-1 plasmids revealed also an increased relative abundance of IncP-1 plasmids in total community DNA from the rhizosphere of lettuce and tomato plants grown in non-polluted soil along with plant age. Here we report the successful isolation of IncP-1 plasmids by exploiting their ability to mobilize plasmid pSM1890. IncP-1 plasmids were captured from the rhizosphere but not from bulk soil, and a high diversity was revealed by sequencing 14 different plasmids that were assigned to IncP-1β, δ, and ε subgroups. Although backbone genes were highly conserved and mobile elements or remnants as Tn501, IS1071, Tn402, or class 1 integron were carried by 13 of the sequenced IncP-1 plasmids, no antibiotic resistance genes were found. Instead, seven plasmids had a mer operon with Tn501-like transposon and five plasmids contained putative metabolic gene clusters linked to these mobile elements. In-depth sequence comparisons with previously known plasmids indicate that the IncP-1 plasmids captured from the rhizosphere are archetypes of those found in clinical isolates. Our findings that IncP-1 plasmids do not always carry accessory genes in unpolluted rhizospheres are important to understand the ecology and role of the IncP-1 plasmids in the natural environment.
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spelling pubmed-77289202020-12-15 Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology Shintani, Masaki Nour, Eman Elsayed, Tarek Blau, Khald Wall, Inessa Jechalke, Sven Spröer, Cathrin Bunk, Boyke Overmann, Jörg Smalla, Kornelia Front Microbiol Microbiology IncP-1 plasmids, first isolated from clinical specimens (R751, RP4), are recognized as important vectors spreading antibiotic resistance genes. The abundance of IncP-1 plasmids in the environment, previously reported, suggested a correlation with anthropogenic pollution. Unexpectedly, qPCR-based detection of IncP-1 plasmids revealed also an increased relative abundance of IncP-1 plasmids in total community DNA from the rhizosphere of lettuce and tomato plants grown in non-polluted soil along with plant age. Here we report the successful isolation of IncP-1 plasmids by exploiting their ability to mobilize plasmid pSM1890. IncP-1 plasmids were captured from the rhizosphere but not from bulk soil, and a high diversity was revealed by sequencing 14 different plasmids that were assigned to IncP-1β, δ, and ε subgroups. Although backbone genes were highly conserved and mobile elements or remnants as Tn501, IS1071, Tn402, or class 1 integron were carried by 13 of the sequenced IncP-1 plasmids, no antibiotic resistance genes were found. Instead, seven plasmids had a mer operon with Tn501-like transposon and five plasmids contained putative metabolic gene clusters linked to these mobile elements. In-depth sequence comparisons with previously known plasmids indicate that the IncP-1 plasmids captured from the rhizosphere are archetypes of those found in clinical isolates. Our findings that IncP-1 plasmids do not always carry accessory genes in unpolluted rhizospheres are important to understand the ecology and role of the IncP-1 plasmids in the natural environment. Frontiers Media S.A. 2020-11-27 /pmc/articles/PMC7728920/ /pubmed/33329469 http://dx.doi.org/10.3389/fmicb.2020.590776 Text en Copyright © 2020 Shintani, Nour, Elsayed, Blau, Wall, Jechalke, Spröer, Bunk, Overmann and Smalla. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Shintani, Masaki
Nour, Eman
Elsayed, Tarek
Blau, Khald
Wall, Inessa
Jechalke, Sven
Spröer, Cathrin
Bunk, Boyke
Overmann, Jörg
Smalla, Kornelia
Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology
title Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology
title_full Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology
title_fullStr Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology
title_full_unstemmed Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology
title_short Plant Species-Dependent Increased Abundance and Diversity of IncP-1 Plasmids in the Rhizosphere: New Insights Into Their Role and Ecology
title_sort plant species-dependent increased abundance and diversity of incp-1 plasmids in the rhizosphere: new insights into their role and ecology
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7728920/
https://www.ncbi.nlm.nih.gov/pubmed/33329469
http://dx.doi.org/10.3389/fmicb.2020.590776
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