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Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management
Plants manipulate their rhizosphere community in a species and even a plant life stage-dependent manner. In essence plants select, promote and (de)activate directly the local bacterial and fungal community, and indirectly representatives of the next trophic level, protists and nematodes. By doing so...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6965313/ https://www.ncbi.nlm.nih.gov/pubmed/31998352 http://dx.doi.org/10.3389/fpls.2019.01697 |
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author | Harkes, Paula van Steenbrugge, Joris Johannes Matheus van den Elsen, Sven Johannes Josephus Suleiman, Afnan Khalil Ahmad de Haan, Johannes Jan Holterman, Martijn Hermanus Maria Helder, Johannes |
author_facet | Harkes, Paula van Steenbrugge, Joris Johannes Matheus van den Elsen, Sven Johannes Josephus Suleiman, Afnan Khalil Ahmad de Haan, Johannes Jan Holterman, Martijn Hermanus Maria Helder, Johannes |
author_sort | Harkes, Paula |
collection | PubMed |
description | Plants manipulate their rhizosphere community in a species and even a plant life stage-dependent manner. In essence plants select, promote and (de)activate directly the local bacterial and fungal community, and indirectly representatives of the next trophic level, protists and nematodes. By doing so, plants enlarge the pool of bioavailable nutrients and maximize local disease suppressiveness within the boundaries set by the nature of the local microbial community. MiSeq sequencing of specific variable regions of the 16S or 18S ribosomal DNA (rDNA) is widely used to map microbial shifts. As current RNA extraction procedures are time-consuming and expensive, the rRNA-based characterization of the active microbial community is taken along less frequently. Recently, we developed a relatively fast and affordable protocol for the simultaneous extraction of rDNA and rRNA from soil. Here, we investigated the long-term impact of three type of soil management, two conventional and an organic regime, on soil biota in fields naturally infested with the Columbian root-knot nematode Meloidogyne chitwoodi with pea (Pisum sativum) as the main crop. For all soil samples, large differences were observed between resident (rDNA) and active (rRNA) microbial communities. Among the four organismal group under investigation, the bacterial community was most affected by the main crop, and unweighted and weighted UniFrac analyses (explaining respectively 16.4% and 51.3% of the observed variation) pointed at a quantitative rather than a qualitative shift. LEfSe analyses were employed for each of the four organismal groups to taxonomically pinpoint the effects of soil management. Concentrating on the bacterial community in the pea rhizosphere, organic soil management resulted in a remarkable activation of members of the Burkholderiaceae, Enterobacteriaceae, and Pseudomonadaceae. Prolonged organic soil management was also accompanied by significantly higher densities of bacterivorous nematodes, whereas levels of M. chitwoodi had dropped drastically. Though present and active in the fields under investigation Orbiliaceae, a family harboring numerous nematophagous fungi, was not associated with the M. chitwoodi decline. A closer look revealed that a local accumulation and activation of Pseudomonas, a genus that includes a number of nematode-suppressive species, paralleled the lower M. chitwoodi densities. This study underlines the relevance of taking along both resident and active fractions of multiple organismal groups while mapping the impact of e.g. crops and soil management regimes. |
format | Online Article Text |
id | pubmed-6965313 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-69653132020-01-29 Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management Harkes, Paula van Steenbrugge, Joris Johannes Matheus van den Elsen, Sven Johannes Josephus Suleiman, Afnan Khalil Ahmad de Haan, Johannes Jan Holterman, Martijn Hermanus Maria Helder, Johannes Front Plant Sci Plant Science Plants manipulate their rhizosphere community in a species and even a plant life stage-dependent manner. In essence plants select, promote and (de)activate directly the local bacterial and fungal community, and indirectly representatives of the next trophic level, protists and nematodes. By doing so, plants enlarge the pool of bioavailable nutrients and maximize local disease suppressiveness within the boundaries set by the nature of the local microbial community. MiSeq sequencing of specific variable regions of the 16S or 18S ribosomal DNA (rDNA) is widely used to map microbial shifts. As current RNA extraction procedures are time-consuming and expensive, the rRNA-based characterization of the active microbial community is taken along less frequently. Recently, we developed a relatively fast and affordable protocol for the simultaneous extraction of rDNA and rRNA from soil. Here, we investigated the long-term impact of three type of soil management, two conventional and an organic regime, on soil biota in fields naturally infested with the Columbian root-knot nematode Meloidogyne chitwoodi with pea (Pisum sativum) as the main crop. For all soil samples, large differences were observed between resident (rDNA) and active (rRNA) microbial communities. Among the four organismal group under investigation, the bacterial community was most affected by the main crop, and unweighted and weighted UniFrac analyses (explaining respectively 16.4% and 51.3% of the observed variation) pointed at a quantitative rather than a qualitative shift. LEfSe analyses were employed for each of the four organismal groups to taxonomically pinpoint the effects of soil management. Concentrating on the bacterial community in the pea rhizosphere, organic soil management resulted in a remarkable activation of members of the Burkholderiaceae, Enterobacteriaceae, and Pseudomonadaceae. Prolonged organic soil management was also accompanied by significantly higher densities of bacterivorous nematodes, whereas levels of M. chitwoodi had dropped drastically. Though present and active in the fields under investigation Orbiliaceae, a family harboring numerous nematophagous fungi, was not associated with the M. chitwoodi decline. A closer look revealed that a local accumulation and activation of Pseudomonas, a genus that includes a number of nematode-suppressive species, paralleled the lower M. chitwoodi densities. This study underlines the relevance of taking along both resident and active fractions of multiple organismal groups while mapping the impact of e.g. crops and soil management regimes. Frontiers Media S.A. 2020-01-10 /pmc/articles/PMC6965313/ /pubmed/31998352 http://dx.doi.org/10.3389/fpls.2019.01697 Text en Copyright © 2020 Harkes, van Steenbrugge, van den Elsen, Suleiman, de Haan, Holterman and Helder 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 | Plant Science Harkes, Paula van Steenbrugge, Joris Johannes Matheus van den Elsen, Sven Johannes Josephus Suleiman, Afnan Khalil Ahmad de Haan, Johannes Jan Holterman, Martijn Hermanus Maria Helder, Johannes Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management |
title | Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management |
title_full | Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management |
title_fullStr | Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management |
title_full_unstemmed | Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management |
title_short | Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management |
title_sort | shifts in the active rhizobiome paralleling low meloidogyne chitwoodi densities in fields under prolonged organic soil management |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6965313/ https://www.ncbi.nlm.nih.gov/pubmed/31998352 http://dx.doi.org/10.3389/fpls.2019.01697 |
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