Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture

Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and e...

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Published inThe ISME Journal Vol. 11; no. 10; pp. 2294 - 2304
Main Authors Hannula, S Emilia, Morriën, Elly, de Hollander, Mattias, van der Putten, Wim H, van Veen, Johannes A, de Boer, Wietse
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.10.2017
Oxford University Press
Nature Publishing Group
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Abstract Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13 CO 2 . The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13 C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13 C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
AbstractList Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13 CO 2 . The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13 C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13 C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with CO . The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived C was taken up by bacteria but that in long-term abandoned fields most of the root-derived C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13CO2. The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13 CO 2. The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13 C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13 C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13 CO2 . The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13 C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13 C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13CO2. The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13CO2. The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
Author de Boer, Wietse
van der Putten, Wim H
Hannula, S Emilia
Morriën, Elly
de Hollander, Mattias
van Veen, Johannes A
Author_xml – sequence: 1
  givenname: S Emilia
  surname: Hannula
  fullname: Hannula, S Emilia
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  givenname: Elly
  surname: Morriën
  fullname: Morriën, Elly
  organization: Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Department of Ecosytem and Landscape Dynamics (IBED-ELD), Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam
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  givenname: Mattias
  surname: de Hollander
  fullname: de Hollander, Mattias
  organization: Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW)
– sequence: 4
  givenname: Wim H
  surname: van der Putten
  fullname: van der Putten, Wim H
  organization: Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Department of Nematology, Wageningen University & Research
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  givenname: Wietse
  surname: de Boer
  fullname: de Boer, Wietse
  organization: Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Department of Soil Quality, Wageningen University & Research
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28585935$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright International Society for Microbial Ecology 2017
Copyright Nature Publishing Group Oct 2017
Copyright © 2017 International Society for Microbial Ecology 2017 International Society for Microbial Ecology
Wageningen University & Research
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Snippet Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root...
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StartPage 2294
SubjectTerms 45/22
45/77
631/158/670
704/158/2466
704/158/855
Abandoned land
Agriculture
Arable land
Bacteria
Bacteria - classification
Bacteria - genetics
Bacteria - isolation & purification
Biomass
Biomedical and Life Sciences
Bodembiologie
Bodembiologie en biologische bodemkwaliteit
Carbon - metabolism
Carbon dioxide
Chair Soil Biology and Biological Soil Quality
Communities
Cores
Deoxyribonucleic acid
DNA
DNA sequencing
Ecological succession
Ecology
Ecosystem
Endophytes
EPS
Evolutionary Biology
Exudates
Food chains
Food plants
Food webs
Fungi
Fungi - classification
Fungi - genetics
Fungi - isolation & purification
Laboratorium voor Nematologie
Laboratory of Nematology
Leerstoelgroep Bodembiologie en biologische Bodemkwaliteit
Life Sciences
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Mycorrhizae - classification
Mycorrhizae - genetics
Mycorrhizae - isolation & purification
Netherlands
Nutrient cycles
Original
original-article
PE&RC
Phospholipids
Plant Roots - microbiology
Plants
Plants - microbiology
Rhizosphere
Soil - chemistry
Soil Biology
Soil Biology and Biological Soil Quality
Soil Microbiology
Stable isotopes
Terrestrial ecosystems
Title Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture
URI https://link.springer.com/article/10.1038/ismej.2017.90
https://www.ncbi.nlm.nih.gov/pubmed/28585935
https://www.proquest.com/docview/1940179085
https://www.proquest.com/docview/1906466164
https://pubmed.ncbi.nlm.nih.gov/PMC5607372
http://www.narcis.nl/publication/RecordID/oai:library.wur.nl:wurpubs%2F527543
Volume 11
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