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Title: Effect of land use and soil organic matter quality on the structure and function of microbial communities in pastoral soils: Implications for disease suppression

Abstract

Cropping soils vary in extent of natural suppression of soil-borne plant diseases. However, it is unknown whether similar variation occurs across pastoral agricultural systems. We examined soil microbial community properties known to be associated with disease suppression across 50 pastoral fields varying in management intensity. The composition and abundance of the disease-suppressive community were assessed from both taxonomic and functional perspectives. Pseudomonas bacteria were selected as a general taxonomic indicator of disease suppressive potential, while genes associated with the biosynthesis of a suite of secondary metabolites provided functional markers (GeoChip 5.0 microarray analysis). The composition of both the Pseudomonas communities and disease suppressive functional genes were responsive to land use. Underlying soil properties explained 37% of the variation in Pseudomonas community structure and up to 61% of the variation in the abundance of disease suppressive functional genes. Notably, measures of soil organic matter quality, C:P ratio, and aromaticity of the dissolved organic matter content (carbon recalcitrance), influenced both the taxonomic and functional disease suppressive potential of the pasture soils. Our results suggest that key components of the soil microbial community may be managed on-farm to enhance disease suppression and plant productivity.

Authors:
ORCiD logo [1];  [1];  [2];  [3];  [4];  [5];  [6]
  1. Lincoln Univ., Christchurch (New Zealand); AgResearch Ltd, Christchurch (New Zealand)
  2. Lincoln Univ., Christchurch (New Zealand)
  3. Univ. of Utrecht (Netherlands)
  4. Univ. of Oklahoma, Norman, OK (United States)
  5. Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tsinghua Univ., Beijing (China)
  6. Lincoln Univ., Christchurch (New Zealand); AgResearch Ltd, Christchurch (New Zealand); Scion Research Ltd, Christchurch (New Zealand)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1567102
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 13; Journal Issue: 5; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Dignam, Bryony E. A., O’Callaghan, Maureen, Condron, Leo M., Kowalchuk, George A., Van Nostrand, Joy D., Zhou, Jizhong, and Wakelin, Steven A. Effect of land use and soil organic matter quality on the structure and function of microbial communities in pastoral soils: Implications for disease suppression. United States: N. p., 2018. Web. doi:10.1371/journal.pone.0196581.
Dignam, Bryony E. A., O’Callaghan, Maureen, Condron, Leo M., Kowalchuk, George A., Van Nostrand, Joy D., Zhou, Jizhong, & Wakelin, Steven A. Effect of land use and soil organic matter quality on the structure and function of microbial communities in pastoral soils: Implications for disease suppression. United States. https://doi.org/10.1371/journal.pone.0196581
Dignam, Bryony E. A., O’Callaghan, Maureen, Condron, Leo M., Kowalchuk, George A., Van Nostrand, Joy D., Zhou, Jizhong, and Wakelin, Steven A. Mon . "Effect of land use and soil organic matter quality on the structure and function of microbial communities in pastoral soils: Implications for disease suppression". United States. https://doi.org/10.1371/journal.pone.0196581. https://www.osti.gov/servlets/purl/1567102.
@article{osti_1567102,
title = {Effect of land use and soil organic matter quality on the structure and function of microbial communities in pastoral soils: Implications for disease suppression},
author = {Dignam, Bryony E. A. and O’Callaghan, Maureen and Condron, Leo M. and Kowalchuk, George A. and Van Nostrand, Joy D. and Zhou, Jizhong and Wakelin, Steven A.},
abstractNote = {Cropping soils vary in extent of natural suppression of soil-borne plant diseases. However, it is unknown whether similar variation occurs across pastoral agricultural systems. We examined soil microbial community properties known to be associated with disease suppression across 50 pastoral fields varying in management intensity. The composition and abundance of the disease-suppressive community were assessed from both taxonomic and functional perspectives. Pseudomonas bacteria were selected as a general taxonomic indicator of disease suppressive potential, while genes associated with the biosynthesis of a suite of secondary metabolites provided functional markers (GeoChip 5.0 microarray analysis). The composition of both the Pseudomonas communities and disease suppressive functional genes were responsive to land use. Underlying soil properties explained 37% of the variation in Pseudomonas community structure and up to 61% of the variation in the abundance of disease suppressive functional genes. Notably, measures of soil organic matter quality, C:P ratio, and aromaticity of the dissolved organic matter content (carbon recalcitrance), influenced both the taxonomic and functional disease suppressive potential of the pasture soils. Our results suggest that key components of the soil microbial community may be managed on-farm to enhance disease suppression and plant productivity.},
doi = {10.1371/journal.pone.0196581},
journal = {PLoS ONE},
number = 5,
volume = 13,
place = {United States},
year = {Mon May 07 00:00:00 EDT 2018},
month = {Mon May 07 00:00:00 EDT 2018}
}

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Cited by: 25 works
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Works referenced in this record:

Monitoring dissolved organic carbon in surface and drinking waters
journal, January 2002

  • Volk, Christian; Wood, Larry; Johnson, Bruce
  • Journal of Environmental Monitoring, Vol. 4, Issue 1
  • DOI: 10.1039/b107768f

Variation in microbial responses and Rhizoctonia solani AG2-2IIIB growth in soil under different organic amendment regimes
journal, April 2012

  • van Overbeek, Leonard S.; Senechkin, Ilya V.; van Bruggen, Ariena H. C.
  • Canadian Journal of Plant Pathology, Vol. 34, Issue 2
  • DOI: 10.1080/07060661.2012.679622

Soil and plant specific effects on bacterial community composition in the rhizosphere
journal, September 2001


GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
journal, May 2007

  • He, Zhili; Gentry, Terry J.; Schadt, Christopher W.
  • The ISME Journal, Vol. 1, Issue 1
  • DOI: 10.1038/ismej.2007.2

Fungal Community Structure in Disease Suppressive Soils Assessed by 28S LSU Gene Sequencing
journal, April 2014


Microbial and biochemical basis of a Fusarium wilt-suppressive soil
journal, June 2015

  • Cha, Jae-Yul; Han, Sangjo; Hong, Hee-Jeon
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.95

Challenges and opportunities in harnessing soil disease suppressiveness for sustainable pasture production
journal, April 2016


Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria
journal, May 2011


Effects of soil type and farm management on soil ecological functional genes and microbial activities
journal, April 2010

  • Reeve, Jennifer R.; Schadt, Christopher W.; Carpenter-Boggs, Lynne
  • The ISME Journal, Vol. 4, Issue 9
  • DOI: 10.1038/ismej.2010.42

Response of soil microbial communities to contrasted histories of phosphorus fertilisation in pastures
journal, October 2012


Assessment of the specificity of Burkholderia and Pseudomonas qPCR assays for detection of these genera in soil using 454 pyrosequencing
journal, June 2012


The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms
journal, February 2008

  • Raaijmakers, Jos M.; Paulitz, Timothy C.; Steinberg, Christian
  • Plant and Soil, Vol. 321, Issue 1-2
  • DOI: 10.1007/s11104-008-9568-6

Cost of root disease on white clover growth in New Zealand dairy pastures
journal, April 2016


Non-parametric multivariate analyses of changes in community structure
journal, March 1993


Pasture management clearly affects soil microbial community structure and N-cycling bacteria
journal, May 2009


Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland
journal, November 2012

  • Yang, Yunfeng; Wu, Linwei; Lin, Qiaoyan
  • Global Change Biology, Vol. 19, Issue 2
  • DOI: 10.1111/gcb.12065

Molecular ecological network analyses
journal, January 2012


Nutrient use Efficiency in Plants
journal, April 2001

  • Baligar, V. C.; Fageria, N. K.; He, Z. L.
  • Communications in Soil Science and Plant Analysis, Vol. 32, Issue 7-8
  • DOI: 10.1081/CSS-100104098

Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease
journal, June 2009

  • Kyselková, Martina; Kopecký, Jan; Frapolli, Michele
  • The ISME Journal, Vol. 3, Issue 10
  • DOI: 10.1038/ismej.2009.61

Hot-water extractable carbon in soils: a sensitive measurement for determining impacts of fertilisation, grazing and cultivation
journal, September 2003


m Icrobial p Opulations r Esponsible for s Pecific s oil s Uppressiveness to p lant p Athogens
journal, September 2002


Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi
journal, January 2005


Soil immune responses
journal, June 2016


Diversity and Natural Functions of Antibiotics Produced by Beneficial and Plant Pathogenic Bacteria
journal, September 2012


The bacterial biogeography of British soils: Mapping soil bacteria
journal, April 2011


Assessment of Variation in Bacterial Composition among Microhabitats in a Mangrove Environment Using DGGE Fingerprints and Barcoded Pyrosequencing
journal, January 2012


T-REX: software for the processing and analysis of T-RFLP data
journal, June 2009

  • Culman, Steven W.; Bukowski, Robert; Gauch, Hugh G.
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-171

Chitinase genes revealed and compared in bacterial isolates, DNA extracts and a metagenomic library from a phytopathogen-suppressive soil
journal, February 2010


Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils
journal, March 2008


On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages
journal, March 2006

  • Clarke, K. Robert; Somerfield, Paul J.; Chapman, M. Gee
  • Journal of Experimental Marine Biology and Ecology, Vol. 330, Issue 1
  • DOI: 10.1016/j.jembe.2005.12.017

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

Community fingerprinting in a sequencing world
journal, March 2014

  • van Dorst, Josie; Bissett, Andrew; Palmer, Anne S.
  • FEMS Microbiology Ecology, Vol. 89, Issue 2
  • DOI: 10.1111/1574-6941.12308

Recent advances in the biological control of fusarium wilts
journal, January 1993

  • Alabouvette, Claude; Lemanceau, Philippe; Steinberg, Christian
  • Pesticide Science, Vol. 37, Issue 4
  • DOI: 10.1002/ps.2780370409

Analyses of soil microbial community compositions and functional genes reveal potential consequences of natural forest succession
journal, May 2015

  • Cong, Jing; Yang, Yunfeng; Liu, Xueduan
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep10007

Assessment and Management of soil Microbial Community Structure for Disease Suppression
journal, September 2004


Fungal invasion of the rhizosphere microbiome
journal, May 2015

  • Chapelle, Emilie; Mendes, Rodrigo; Bakker, Peter A. HM
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.82

Physicochemical properties of 50 New Zealand pasture soils: a starting point for assessing and managing soil microbial resources
journal, August 2013

  • Wakelin, Sa; van Koten, C.; O'Callaghan, M.
  • New Zealand Journal of Agricultural Research, Vol. 56, Issue 4
  • DOI: 10.1080/00288233.2013.822003

A method of linking multivariate community structure to environmental variables
journal, January 1993

  • Clarke, Kr; Ainsworth, M.
  • Marine Ecology Progress Series, Vol. 92
  • DOI: 10.3354/meps092205

Functional Molecular Ecological Networks
journal, October 2010


Plant diversity improves protection against soil-borne pathogens by fostering antagonistic bacterial communities
journal, January 2012


Genomic appraisal of Klebsiella PGPB isolated from soil to enhance the growth of barley
journal, May 2021


Recent advances in the biological control of fusarium wilts
journal, January 1993

  • Alabouvette, Claude; Lemanceau, Philippe; Steinberg, Christian
  • Pesticide Science, Vol. 37, Issue 4
  • DOI: 10.1002/ps.2780370409

Cost of root disease on white clover growth in New Zealand dairy pastures
journal, April 2016


Challenges and opportunities in harnessing soil disease suppressiveness for sustainable pasture production
journal, April 2016


Assessment of the diversity, and antagonism towards Rhizoctonia solani AG3, of Pseudomonas species in soil from different agricultural regimes
journal, January 2004


In search of biological indicators for soil health and disease suppression
journal, August 2000


GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
journal, May 2007

  • He, Zhili; Gentry, Terry J.; Schadt, Christopher W.
  • The ISME Journal, Vol. 1, Issue 1
  • DOI: 10.1038/ismej.2007.2

Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease
journal, June 2009

  • Kyselková, Martina; Kopecký, Jan; Frapolli, Michele
  • The ISME Journal, Vol. 3, Issue 10
  • DOI: 10.1038/ismej.2009.61

Effects of soil type and farm management on soil ecological functional genes and microbial activities
journal, April 2010

  • Reeve, Jennifer R.; Schadt, Christopher W.; Carpenter-Boggs, Lynne
  • The ISME Journal, Vol. 4, Issue 9
  • DOI: 10.1038/ismej.2010.42

Fungal invasion of the rhizosphere microbiome
journal, May 2015

  • Chapelle, Emilie; Mendes, Rodrigo; Bakker, Peter A. HM
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.82

Microbial and biochemical basis of a Fusarium wilt-suppressive soil
journal, June 2015

  • Cha, Jae-Yul; Han, Sangjo; Hong, Hee-Jeon
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.95

Monitoring dissolved organic carbon in surface and drinking waters
journal, January 2002

  • Volk, Christian; Wood, Larry; Johnson, Bruce
  • Journal of Environmental Monitoring, Vol. 4, Issue 1
  • DOI: 10.1039/b107768f

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

Analysis of soil eDNA functional genes: potential to increase profitability and sustainability of pastoral agriculture
journal, July 2016


Community fingerprinting in a sequencing world
journal, March 2014

  • van Dorst, Josie; Bissett, Andrew; Palmer, Anne S.
  • FEMS Microbiology Ecology, Vol. 89, Issue 2
  • DOI: 10.1111/1574-6941.12308

Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland
journal, November 2012

  • Yang, Yunfeng; Wu, Linwei; Lin, Qiaoyan
  • Global Change Biology, Vol. 19, Issue 2
  • DOI: 10.1111/gcb.12065

Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens
journal, May 2009


Chitinase genes revealed and compared in bacterial isolates, DNA extracts and a metagenomic library from a phytopathogen-suppressive soil
journal, February 2010


Assessment of the specificity of Burkholderia and Pseudomonas qPCR assays for detection of these genera in soil using 454 pyrosequencing
journal, June 2012


Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale
journal, June 2009

  • Lauber, C. L.; Hamady, M.; Knight, R.
  • Applied and Environmental Microbiology, Vol. 75, Issue 15
  • DOI: 10.1128/aem.00335-09

Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47.
journal, January 1992


Characterization of a Chitinase Gene from Stenotrophomonas maltophilia Strain 34S1 and Its Involvement in Biological Control
journal, March 2002


Assessment of Soil Microbial Community Structure by Use of Taxon-Specific Quantitative PCR Assays
journal, July 2005


Diversity and Natural Functions of Antibiotics Produced by Beneficial and Plant Pathogenic Bacteria
journal, September 2012


Assessment and Management of soil Microbial Community Structure for Disease Suppression
journal, September 2004


T-REX: software for the processing and analysis of T-RFLP data
journal, June 2009

  • Culman, Steven W.; Bukowski, Robert; Gauch, Hugh G.
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-171

GuiTope: an application for mapping random-sequence peptides to protein sequences
journal, January 2012

  • Halperin, Rebecca F.; Stafford, Phillip; Emery, Jack S.
  • BMC Bioinformatics, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2105-13-1

Assessment of Variation in Bacterial Composition among Microhabitats in a Mangrove Environment Using DGGE Fingerprints and Barcoded Pyrosequencing
journal, January 2012


Fungal Community Structure in Disease Suppressive Soils Assessed by 28S LSU Gene Sequencing
journal, April 2014


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Plant growth‐promoting archaea trigger induced systemic resistance in Arabidopsis thaliana against Pectobacterium carotovorum and Pseudomonas syringae
journal, January 2019

  • Song, Geun Cheol; Im, Hyunjoo; Jung, Jihye
  • Environmental Microbiology, Vol. 21, Issue 3
  • DOI: 10.1111/1462-2920.14486

Using soil bacterial communities to predict physico-chemical variables and soil quality
journal, June 2020


Applications of the Soil, Plant and Rumen Microbiomes in Pastoral Agriculture
journal, July 2019

  • Attwood, Graeme T.; Wakelin, Steve A.; Leahy, Sinead C.
  • Frontiers in Nutrition, Vol. 6
  • DOI: 10.3389/fnut.2019.00107

Visualizing Microbial Community Dynamics via a Controllable Soil Environment
journal, February 2020