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Title: Plant–microbe networks in soil are weakened by century‐long use of inorganic fertilizers

Abstract

Understanding the changes in plant-microbe interactions is critically important for predicting ecosystem functioning in response to human-induced environmental changes such as nitrogen (N) addition. In this study, the effects of a century-long fertilization treatment (> 150 years) on the networks between plants and soil microbial functional communities, detected by GeoChip, in grassland were determined in the Park Grass Experiment at Rothamsted Research, UK. Our results showed that plants and soil microbes have a consistent response to long-term fertilization-both richness and diversity of plants and soil microbes are significantly decreased, as well as microbial functional genes involved in soil carbon (C), nitrogen (N) and phosphorus (P) cycling. The network-based analyses showed that long-term fertilization decreased the complexity of networks between plant and microbial functional communities in terms of node numbers, connectivity, network density and the clustering coefficient. Similarly, within the soil microbial community, the strength of microbial associations was also weakened in response to long-term fertilization. Mantel path analysis showed that soil C and N contents were the main factors affecting the network between plants and microbes. Our results indicate that century-long fertilization weakens the plant-microbe networks, which is important in improving our understanding of grassland ecosystem functions and stability under long-term agriculturemore » management.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [3];  [4]; ORCiD logo [1]
  1. State Key Laboratory of Soil and Sustainable Agriculture Institute of Soil Science Chinese Academy of Sciences Nanjing 210008 China; University of Chinese Academy of Sciences No. 19A Yuquan Road Beijing 100049 China
  2. Rothamsted Research Harpenden Hertfordshire AL5 2JQ UK
  3. Institute for Environmental Genomics Department of Microbiology &, Plant Biology School of Civil Engineering and Environmental Sciences University of Oklahoma Norman OK 73019 USA
  4. Institute for Environmental Genomics Department of Microbiology &, Plant Biology School of Civil Engineering and Environmental Sciences University of Oklahoma Norman OK 73019 USA; State Key Joint Laboratory of Environment Simulation and Pollution Control School of Environment Tsinghua University Beijing100084China
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1580962
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Microbial Biotechnology (Online)
Additional Journal Information:
Journal Name: Microbial Biotechnology (Online); Journal Volume: 12; Journal Issue: 6; Journal ID: ISSN 1751-7915
Publisher:
Wiley
Country of Publication:
United States
Language:
English

Citation Formats

Huang, Ruilin, McGrath, Steve P., Hirsch, Penny R., Clark, Ian M., Storkey, Jonathan, Wu, Liyou, Zhou, Jizhong, and Liang, Yuting. Plant–microbe networks in soil are weakened by century‐long use of inorganic fertilizers. United States: N. p., 2019. Web. doi:10.1111/1751-7915.13487.
Huang, Ruilin, McGrath, Steve P., Hirsch, Penny R., Clark, Ian M., Storkey, Jonathan, Wu, Liyou, Zhou, Jizhong, & Liang, Yuting. Plant–microbe networks in soil are weakened by century‐long use of inorganic fertilizers. United States. doi:10.1111/1751-7915.13487.
Huang, Ruilin, McGrath, Steve P., Hirsch, Penny R., Clark, Ian M., Storkey, Jonathan, Wu, Liyou, Zhou, Jizhong, and Liang, Yuting. Mon . "Plant–microbe networks in soil are weakened by century‐long use of inorganic fertilizers". United States. doi:10.1111/1751-7915.13487. https://www.osti.gov/servlets/purl/1580962.
@article{osti_1580962,
title = {Plant–microbe networks in soil are weakened by century‐long use of inorganic fertilizers},
author = {Huang, Ruilin and McGrath, Steve P. and Hirsch, Penny R. and Clark, Ian M. and Storkey, Jonathan and Wu, Liyou and Zhou, Jizhong and Liang, Yuting},
abstractNote = {Understanding the changes in plant-microbe interactions is critically important for predicting ecosystem functioning in response to human-induced environmental changes such as nitrogen (N) addition. In this study, the effects of a century-long fertilization treatment (> 150 years) on the networks between plants and soil microbial functional communities, detected by GeoChip, in grassland were determined in the Park Grass Experiment at Rothamsted Research, UK. Our results showed that plants and soil microbes have a consistent response to long-term fertilization-both richness and diversity of plants and soil microbes are significantly decreased, as well as microbial functional genes involved in soil carbon (C), nitrogen (N) and phosphorus (P) cycling. The network-based analyses showed that long-term fertilization decreased the complexity of networks between plant and microbial functional communities in terms of node numbers, connectivity, network density and the clustering coefficient. Similarly, within the soil microbial community, the strength of microbial associations was also weakened in response to long-term fertilization. Mantel path analysis showed that soil C and N contents were the main factors affecting the network between plants and microbes. Our results indicate that century-long fertilization weakens the plant-microbe networks, which is important in improving our understanding of grassland ecosystem functions and stability under long-term agriculture management.},
doi = {10.1111/1751-7915.13487},
journal = {Microbial Biotechnology (Online)},
number = 6,
volume = 12,
place = {United States},
year = {2019},
month = {7}
}

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Works referenced in this record:

Structure and function of the global topsoil microbiome
journal, August 2018


The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms
journal, June 2006


Plant species and nitrogen effects on soil biological properties of temperate upland grasslands
journal, October 1999


Relationship between plants and soil microbial communities in fertilized grasslands
journal, November 2005


Protozoa and plant growth: the microbial loop in soil revisited
journal, June 2004


Determinants of Species Richness in the Park Grass Experiment
journal, February 2005

  • Crawley, M. J.; Johnston, A. E.; Silvertown, J.
  • The American Naturalist, Vol. 165, Issue 2
  • DOI: 10.1086/427270

Changes in soil phosphorus forms through time in perennial versus annual agroecosystems
journal, February 2014


Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities?: Root exudates and rhizosphere bacteria
journal, March 2010


Mycorrhizal Community Dynamics Following Nitrogen Fertilization: a Cross-Site test in five Grasslands
journal, November 2007

  • Egerton-Warburton, Louise M.; Johnson, Nancy Collins; Allen, Edith B.
  • Ecological Monographs, Vol. 77, Issue 4
  • DOI: 10.1890/06-1772.1

Root biomass and exudates link plant diversity with soil bacterial and fungal biomass
journal, April 2017

  • Eisenhauer, Nico; Lanoue, Arnaud; Strecker, Tanja
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep44641

Microbial interactions: from networks to models
journal, July 2012

  • Faust, Karoline; Raes, Jeroen
  • Nature Reviews Microbiology, Vol. 10, Issue 8
  • DOI: 10.1038/nrmicro2832

Toward an Ecological Classification of soil Bacteria
journal, June 2007

  • Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
  • Ecology, Vol. 88, Issue 6
  • DOI: 10.1890/05-1839

Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients
journal, December 2011

  • Fierer, Noah; Lauber, Christian L.; Ramirez, Kelly S.
  • The ISME Journal, Vol. 6, Issue 5
  • DOI: 10.1038/ismej.2011.159

Soil carbon sequestration in prairie grasslands increased by chronic nitrogen addition
journal, September 2012


Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter
journal, February 2016

  • Geyer, Kevin M.; Kyker-Snowman, Emily; Grandy, A. Stuart
  • Biogeochemistry, Vol. 127, Issue 2-3
  • DOI: 10.1007/s10533-016-0191-y

Belowground carbon cycling in a humid tropical forest decreases with fertilization
journal, May 2004


The effect of nitrate-nitrogen supply on bacteria and bacterial-feeding fauna in the rhizosphere of different grass species
journal, August 1992

  • Griffiths, B. S.; Welschen, R.; van Arendonk, J. J. C. M.
  • Oecologia, Vol. 91, Issue 2
  • DOI: 10.1007/BF00317793

Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment
journal, January 2009

  • Hallin, Sara; Jones, Christopher M.; Schloter, Michael
  • The ISME Journal, Vol. 3, Issue 5
  • DOI: 10.1038/ismej.2008.128

Grassland species loss resulting from reduced niche dimension
journal, March 2007


Competition for Light Causes Plant Biodiversity Loss After Eutrophication
journal, April 2009


GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity
journal, April 2010


Using ecological diversity measures with bacterial communities
journal, February 2003


Plant rhizodeposition — an important source for carbon turnover in soils
journal, August 2002


Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective
journal, June 2009


Disentangling Interactions in the Microbiome: A Network Perspective
journal, March 2017

  • Layeghifard, Mehdi; Hwang, David M.; Guttman, David S.
  • Trends in Microbiology, Vol. 25, Issue 3
  • DOI: 10.1016/j.tim.2016.11.008

Over 150 Years of Long-Term Fertilization Alters Spatial Scaling of Microbial Biodiversity
journal, April 2015


Long-Term Balanced Fertilization Decreases Arbuscular Mycorrhizal Fungal Diversity in an Arable Soil in North China Revealed by 454 Pyrosequencing
journal, May 2012

  • Lin, Xiangui; Feng, Youzhi; Zhang, Huayong
  • Environmental Science & Technology, Vol. 46, Issue 11
  • DOI: 10.1021/es3001695

Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms
journal, February 2009

  • Richardson, Alan E.; Barea, José-Miguel; McNeill, Ann M.
  • Plant and Soil, Vol. 321, Issue 1-2
  • DOI: 10.1007/s11104-009-9895-2

The Park Grass Experiment 1856-2006: its contribution to ecology
journal, May 2006


Functional- and abundance-based mechanisms explain diversity loss due to N fertilization
journal, March 2005

  • Suding, K. N.; Collins, S. L.; Gough, L.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 12
  • DOI: 10.1073/pnas.0408648102

Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships
journal, May 2016

  • Trivedi, Pankaj; Delgado-Baquerizo, Manuel; Trivedi, Chanda
  • The ISME Journal, Vol. 10, Issue 11
  • DOI: 10.1038/ismej.2016.65

Chemical Signaling Between Plants and Plant-Pathogenic Bacteria
journal, August 2013


Combined use of network inference tools identifies ecologically meaningful bacterial associations in a paddy soil
journal, February 2017


Ecological Linkages Between Aboveground and Belowground Biota
journal, June 2004


Spatial scaling of functional gene diversity across various microbial taxa
journal, May 2008

  • Zhou, J.; Kang, S.; Schadt, C. W.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 22
  • DOI: 10.1073/pnas.0709016105

Functional Molecular Ecological Networks
journal, October 2010


Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2
journal, July 2011