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...
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Language: | English |
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Frontiers Media S.A.
2020-01-01
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Series: | Frontiers in Plant Science |
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Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.01697/full |
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doaj-91aff8fe1af644b5876c6466b5147cc2 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Paula Harkes Joris Johannes Matheus van Steenbrugge Sven Johannes Josephus van den Elsen Afnan Khalil Ahmad Suleiman Afnan Khalil Ahmad Suleiman Johannes Jan de Haan Martijn Hermanus Maria Holterman Johannes Helder |
spellingShingle |
Paula Harkes Joris Johannes Matheus van Steenbrugge Sven Johannes Josephus van den Elsen Afnan Khalil Ahmad Suleiman Afnan Khalil Ahmad Suleiman Johannes Jan de Haan Martijn Hermanus Maria Holterman Johannes Helder Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil Management Frontiers in Plant Science organic soil management active microbiome rhizosphere disease suppressiveness Meloidogyne chitwoodi |
author_facet |
Paula Harkes Joris Johannes Matheus van Steenbrugge Sven Johannes Josephus van den Elsen Afnan Khalil Ahmad Suleiman Afnan Khalil Ahmad Suleiman Johannes Jan de Haan Martijn Hermanus Maria Holterman Johannes Helder |
author_sort |
Paula Harkes |
title |
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_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_sort |
shifts in the active rhizobiome paralleling low meloidogyne chitwoodi densities in fields under prolonged organic soil management |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Plant Science |
issn |
1664-462X |
publishDate |
2020-01-01 |
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. |
topic |
organic soil management active microbiome rhizosphere disease suppressiveness Meloidogyne chitwoodi |
url |
https://www.frontiersin.org/article/10.3389/fpls.2019.01697/full |
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doaj-91aff8fe1af644b5876c6466b5147cc22020-11-25T01:41:45ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-01-011010.3389/fpls.2019.01697499942Shifts in the Active Rhizobiome Paralleling Low Meloidogyne chitwoodi Densities in Fields Under Prolonged Organic Soil ManagementPaula Harkes0Joris Johannes Matheus van Steenbrugge1Sven Johannes Josephus van den Elsen2Afnan Khalil Ahmad Suleiman3Afnan Khalil Ahmad Suleiman4Johannes Jan de Haan5Martijn Hermanus Maria Holterman6Johannes Helder7Laboratory of Nematology, Department of Plant Sciences, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Nematology, Department of Plant Sciences, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Nematology, Department of Plant Sciences, Wageningen University & Research, Wageningen, NetherlandsDepartment of Microbial Ecology, NIOO-KNAW, Wageningen, NetherlandsDepartment of Microbiological Water Quality and Health, KWR Watercycle Research Institute, PE Nieuwegein, NetherlandsOpen Teelten, Department of Wageningen Plant Research, Wageningen University & Research, Lelystad, NetherlandsLaboratory of Nematology, Department of Plant Sciences, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Nematology, Department of Plant Sciences, Wageningen University & Research, Wageningen, NetherlandsPlants 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.https://www.frontiersin.org/article/10.3389/fpls.2019.01697/fullorganic soil managementactive microbiomerhizospheredisease suppressivenessMeloidogyne chitwoodi |