Plant–microbe networks in soil are weakened by century-long use of inorganic fertilizers

Huang, Ruilin; McGrath, Steve P.; Hirsch, Penny R.; Clark, Ian M.; Storkey, Jonathan; Wu, Liyou; Zhou, Jizhong; Liang, Yuting

doi:10.1111/1751-7915.13487

Plant–microbe networks in soil are weakened by century-long use of inorganic fertilizers

Journal Article · Thu Sep 19 00:00:00 EDT 2019 · Microbial Biotechnology (Online)

DOI:https://doi.org/10.1111/1751-7915.13487· OSTI ID:1580962

Huang, Ruilin ^[1]; McGrath, Steve P. ^[2]; Hirsch, Penny R. ^[2]; Clark, Ian M. ^[2]; Storkey, Jonathan ^[2]; Wu, Liyou ^[3]; Zhou, Jizhong ^[4]; ^[1]

Chinese Academy of Sciences (CAS), Nanjing (China); Univ. of Chinese Academy of Sciences, Beijing (China)
Rothamsted Research, Hertfordshire (United Kingdom)
Univ. of Oklahoma, Norman, OK (United States)
Univ. of Oklahoma, Norman, OK (United States); Tsinghua Univ., Beijing (China)

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Distinguished Young Scholar Program of the Jiangsu Province; Inst. Strategic Programme‐Soil to Nutrition; Long‐Term Experiments National Capability; National Key R&D Program of China; National Natural Science Foundation of China; UK Biotechnology and Biological Sciences Research Council; USDOE Office of Science (SC); Youth Innovation Promotion Association of Chinese Academy of Sciences

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1580962

Journal Information:: Microbial Biotechnology (Online), Journal Name: Microbial Biotechnology (Online) Journal Issue: 6 Vol. 12; ISSN 1751-7915

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Belowground carbon cycling in a humid tropical forest decreases with fertilization Giardina, Christian P.; Binkley, Dan; Ryan, Michael G. Oecologia, Vol. 139, Issue 4 https://doi.org/10.1007/s00442-004-1552-0	journal	May 2004
Century long fertilization reduces stochasticity controlling grassland microbial community succession Liang, Yuting; Ning, Daliang; Lu, Zhenmei Soil Biology and Biochemistry, Vol. 151 https://doi.org/10.1016/j.soilbio.2020.108023	journal	December 2020
Disentangling Interactions in the Microbiome: A Network Perspective Layeghifard, Mehdi; Hwang, David M.; Guttman, David S. Trends in Microbiology, Vol. 25, Issue 3 https://doi.org/10.1016/j.tim.2016.11.008	journal	March 2017
Long-Term Balanced Fertilization Decreases Arbuscular Mycorrhizal Fungal Diversity in an Arable Soil in North China Revealed by 454 Pyrosequencing Lin, Xiangui; Feng, Youzhi; Zhang, Huayong Environmental Science & Technology, Vol. 46, Issue 11 https://doi.org/10.1021/es3001695	journal	May 2012
Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment Hallin, Sara; Jones, Christopher M.; Schloter, Michael The ISME Journal, Vol. 3, Issue 5 https://doi.org/10.1038/ismej.2008.128	journal	January 2009
GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity He, Zhili; Deng, Ye; Van Nostrand, Joy D. The ISME Journal, Vol. 4, Issue 9 https://doi.org/10.1038/ismej.2010.46	journal	April 2010
Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients Fierer, Noah; Lauber, Christian L.; Ramirez, Kelly S. The ISME Journal, Vol. 6, Issue 5 https://doi.org/10.1038/ismej.2011.159	journal	December 2011
Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships Trivedi, Pankaj; Delgado-Baquerizo, Manuel; Trivedi, Chanda The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.65	journal	May 2016
Grassland species loss resulting from reduced niche dimension Harpole, W. Stanley; Tilman, David Nature, Vol. 446, Issue 7137 https://doi.org/10.1038/nature05684	journal	March 2007
Soil networks become more connected and take up more carbon as nature restoration progresses Morriën, Elly; Hannula, S. Emilia; Snoek, L. Basten Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14349	journal	February 2017
Microbial interactions: from networks to models Faust, Karoline; Raes, Jeroen Nature Reviews Microbiology, Vol. 10, Issue 8 https://doi.org/10.1038/nrmicro2832	journal	July 2012
Structure and function of the global topsoil microbiome Bahram, Mohammad; Hildebrand, Falk; Forslund, Sofia K. Nature, Vol. 560, Issue 7717 https://doi.org/10.1038/s41586-018-0386-6	journal	August 2018
Functional- and abundance-based mechanisms explain diversity loss due to N fertilization Suding, K. N.; Collins, S. L.; Gough, L. Proceedings of the National Academy of Sciences, Vol. 102, Issue 12 https://doi.org/10.1073/pnas.0408648102	journal	March 2005
Spatial scaling of functional gene diversity across various microbial taxa Zhou, J.; Kang, S.; Schadt, C. W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 22 https://doi.org/10.1073/pnas.0709016105	journal	May 2008
Determinants of Species Richness in the Park Grass Experiment Crawley, M. J.; Johnston, A. E.; Silvertown, J. The American Naturalist, Vol. 165, Issue 2 https://doi.org/10.1086/427270	journal	February 2005
Using ecological diversity measures with bacterial communities Hill, Tom C. J.; Walsh, Kerry A.; Harris, James A. FEMS Microbiology Ecology, Vol. 43, Issue 1 https://doi.org/10.1111/j.1574-6941.2003.tb01040.x	journal	February 2003
Small molecules below-ground: the role of specialized metabolites in the rhizosphere Massalha, Hassan; Korenblum, Elisa; Tholl, Dorothea The Plant Journal, Vol. 90, Issue 4 https://doi.org/10.1111/tpj.13543	journal	April 2017
Ecological Linkages Between Aboveground and Belowground Biota Wardle, D. A. Science, Vol. 304, Issue 5677 https://doi.org/10.1126/science.1094875	journal	June 2004
Competition for Light Causes Plant Biodiversity Loss After Eutrophication Hautier, Y.; Niklaus, P. A.; Hector, A. Science, Vol. 324, Issue 5927 https://doi.org/10.1126/science.1169640	journal	April 2009
DNA recovery from soils of diverse composition. Zhou, J.; Bruns, M. A.; Tiedje, J. M. Applied and environmental microbiology, Vol. 62, Issue 2 https://doi.org/10.1128/aem.62.2.316-322.1996	journal	January 1996
Functional Molecular Ecological Networks Zhou, Jizhong; Deng, Ye; Luo, Feng mBio, Vol. 1, Issue 4 https://doi.org/10.1128/mbio.00169-10	journal	October 2010
Chemical Signaling Between Plants and Plant-Pathogenic Bacteria Venturi, Vittorio; Fuqua, Clay Annual Review of Phytopathology, Vol. 51, Issue 1 https://doi.org/10.1146/annurev-phyto-082712-102239	journal	August 2013
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G. Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105159	journal	June 2006
Associations between Pathogens in the Upper Respiratory Tract of Young Children: Interplay between Viruses and Bacteria van den Bergh, Menno R.; Biesbroek, Giske; Rossen, John W. A. PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0047711	journal	October 2012
Soil carbon sequestration in prairie grasslands increased by chronic nitrogen addition Fornara, Dario A.; Tilman, David Ecology, Vol. 93, Issue 9 https://doi.org/10.1890/12-0292.1	journal	September 2012
Cross-biome comparison of microbial association networks Faust, Karoline; Lima-Mendez, Gipsi; Lerat, Jean-Sébastien Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01200	journal	October 2015
Development of a Novel Quantum Dots and Graphene Oxide Based FRET Assay for Rapid Detection of invA Gene of Salmonella Guo, Jiubiao; Chan, Edward W. C.; Chen, Sheng Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00008	journal	January 2017
Plant rhizodeposition — an important source for carbon turnover in soils Hütsch, Birgit W.; Augustin, Jürgen; Merbach, Wolfgang Journal of Plant Nutrition and Soil Science, Vol. 165, Issue 4 https://doi.org/10.1002/1522-2624(200208)165:4<397::AID-JPLN397>3.0.CO;2-C	journal	August 2002
The effect of nitrate-nitrogen supply on bacteria and bacterial-feeding fauna in the rhizosphere of different grass species Griffiths, B. S.; Welschen, R.; van Arendonk, J. J. C. M. Oecologia, Vol. 91, Issue 2 https://doi.org/10.1007/BF00317793	journal	August 1992
Carbon input from plant to soil through root exudation in Digitaria adscendens and Ambrosia artemisiifolia Bekku, Yukiko; Kimura, Makoto; Ikeda, Hiroaki Ecological Research, Vol. 12, Issue 3 https://doi.org/10.1007/BF02529460	journal	December 1997
Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter Geyer, Kevin M.; Kyker-Snowman, Emily; Grandy, A. Stuart Biogeochemistry, Vol. 127, Issue 2-3 https://doi.org/10.1007/s10533-016-0191-y	journal	February 2016
Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective Lambers, Hans; Mougel, Christophe; Jaillard, Benoît Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-009-0042-x	journal	June 2009
Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms Richardson, Alan E.; Barea, José-Miguel; McNeill, Ann M. Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-009-9895-2	journal	February 2009
Changes in soil phosphorus forms through time in perennial versus annual agroecosystems Crews, Timothy E.; Brookes, Philip C. Agriculture, Ecosystems & Environment, Vol. 184 https://doi.org/10.1016/j.agee.2013.11.022	journal	February 2014
Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China Shen, Ju-Pei; Zhang, Li-Mei; Guo, Jun-Fu Applied Soil Ecology, Vol. 46, Issue 1 https://doi.org/10.1016/j.apsoil.2010.06.015	journal	September 2010
Impacts of inorganic and organic fertilization treatments on bacterial and fungal communities in a paddy soil Wang, Jichen; Song, Yang; Ma, Tengfei Applied Soil Ecology, Vol. 112 https://doi.org/10.1016/j.apsoil.2017.01.005	journal	April 2017
Relationship between plants and soil microbial communities in fertilized grasslands Benizri, Emile; Amiaud, Bernard Soil Biology and Biochemistry, Vol. 37, Issue 11 https://doi.org/10.1016/j.soilbio.2005.03.008	journal	November 2005
Reduced dependence of rhizosphere microbiome on plant-derived carbon in 32-year long-term inorganic and organic fertilized soils Ai, Chao; Liang, Guoqing; Sun, Jingwen Soil Biology and Biochemistry, Vol. 80 https://doi.org/10.1016/j.soilbio.2014.09.028	journal	January 2015
Linkages between extracellular enzyme activities and the carbon and nitrogen content of grassland soils Cenini, Valeria L.; Fornara, Dario A.; McMullan, Geoffrey Soil Biology and Biochemistry, Vol. 96 https://doi.org/10.1016/j.soilbio.2016.02.015	journal	May 2016
Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis Ling, Ning; Zhu, Chen; Xue, Chao Soil Biology and Biochemistry, Vol. 99 https://doi.org/10.1016/j.soilbio.2016.05.005	journal	August 2016
Combined use of network inference tools identifies ecologically meaningful bacterial associations in a paddy soil Wang, Honggui; Wei, Zhong; Mei, Lijuan Soil Biology and Biochemistry, Vol. 105 https://doi.org/10.1016/j.soilbio.2016.11.029	journal	February 2017
Biogeographical patterns and mechanisms of microbial community assembly that underlie successional biocrusts across northern China Li, Yuanlong; Hu, Chunxiang npj Biofilms and Microbiomes, Vol. 7, Issue 1 https://doi.org/10.1038/s41522-021-00188-6	journal	February 2021
Root biomass and exudates link plant diversity with soil bacterial and fungal biomass Eisenhauer, Nico; Lanoue, Arnaud; Strecker, Tanja Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep44641	journal	April 2017
Plant species and nitrogen effects on soil biological properties of temperate upland grasslands Bardgett, R. D.; Mawdsley, J. L.; Edwards, S. Functional Ecology, Vol. 13, Issue 5 https://doi.org/10.1046/j.1365-2435.1999.00362.x	journal	October 1999
Environmental and anthropogenic controls over bacterial communities in wetland soils Hartman, W. H.; Richardson, C. J.; Vilgalys, R. Proceedings of the National Academy of Sciences, Vol. 105, Issue 46 https://doi.org/10.1073/pnas.0808254105	journal	November 2008
Long-term nitrogen addition causes the evolution of less-cooperative mutualists: NITROGEN ADDITION DESTABILIZES MUTUALISM Weese, Dylan J.; Heath, Katy D.; Dentinger, Bryn T. M. Evolution, Vol. 69, Issue 3 https://doi.org/10.1111/evo.12594	journal	February 2015
The Park Grass Experiment 1856-2006: its contribution to ecology Silvertown, Jonathan; Poulton, Paul; Johnston, Edward Journal of Ecology, Vol. 94, Issue 4 https://doi.org/10.1111/j.1365-2745.2006.01145.x	journal	May 2006
Shoot, but not root, competition reduces community diversity in experimental mesocosms Lamb, Eric G.; Kembel, Steven W.; Cahill, James F. Journal of Ecology, Vol. 97, Issue 1 https://doi.org/10.1111/j.1365-2745.2008.01454.x	journal	January 2009
Protozoa and plant growth: the microbial loop in soil revisited Bonkowski, Michael New Phytologist, Vol. 162, Issue 3 https://doi.org/10.1111/j.1469-8137.2004.01066.x	journal	June 2004
Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities?: Root exudates and rhizosphere bacteria Dennis, Paul G.; Miller, Anthony J.; Hirsch, Penny R. FEMS Microbiology Ecology, Vol. 72, Issue 3 https://doi.org/10.1111/j.1574-6941.2010.00860.x	journal	March 2010
Fungal and bacterial growth responses to N fertilization and pH in the 150-year ‘Park Grass’ UK grassland experiment: N and pH influence on microbial growth in grassland soils Rousk, Johannes; Brookes, Philip C.; Bååth, Erland FEMS Microbiology Ecology, Vol. 76, Issue 1 https://doi.org/10.1111/j.1574-6941.2010.01032.x	journal	January 2011
DNA recovery from soils of diverse composition. Zhou, J.; Bruns, M. A.; Tiedje, J. M. Applied and environmental microbiology, Vol. 62, Issue 2 https://doi.org/10.1128/AEM.62.2.316-322.1996	journal	January 1996
Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2 Zhou, Jizhong; Deng, Ye; Luo, Feng mBio, Vol. 2, Issue 4 https://doi.org/10.1128/mBio.00122-11	journal	July 2011
Functional Molecular Ecological Networks Zhou, Jizhong; Deng, Ye; Luo, Feng mBio, Vol. 1, Issue 4 https://doi.org/10.1128/mBio.00169-10	journal	October 2010
Over 150 Years of Long-Term Fertilization Alters Spatial Scaling of Microbial Biodiversity Liang, Yuting; Wu, Liyou; Clark, Ian M. mBio, Vol. 6, Issue 2 https://doi.org/10.1128/mBio.00240-15	journal	April 2015
Toward an Ecological Classification of soil Bacteria Fierer, Noah; Bradford, Mark A.; Jackson, Robert B. Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/05-1839	journal	June 2007
Mycorrhizal Community Dynamics Following Nitrogen Fertilization: a Cross-Site test in five Grasslands Egerton-Warburton, Louise M.; Johnson, Nancy Collins; Allen, Edith B. Ecological Monographs, Vol. 77, Issue 4 https://doi.org/10.1890/06-1772.1	journal	November 2007
Effects of Long-Term Fertilization on Soil Carbon and Nitrogen in Chinese Mollisols Jiao, Xiaoguang; Gao, Chongsheng; Sui, Yueyu Agronomy Journal, Vol. 106, Issue 3 https://doi.org/10.2134/agronj13.0233	journal	May 2014
The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions Jacoby, Richard; Peukert, Manuela; Succurro, Antonella Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01617	journal	September 2017
Competition for light causes plant biodiversity loss after eutrophication Hautier, Y.; Niklaus, P. A.; Hector, A. American Association for the Advancement of Science (AAAS) https://doi.org/10.5167/uzh-18666	text	January 2009
Geochip functional genes Zhang, Na figshare https://doi.org/10.6084/m9.figshare.7418501	dataset	January 2018
Geochip functional genes Zhang, Na figshare https://doi.org/10.6084/m9.figshare.7806848.v1	dataset	January 2019
Soil carbon sequestration in prairie grasslands increased by chronic nitrogen addition Fornara, Dario A.; Tilman, David Figshare https://doi.org/10.6084/m9.figshare.c.3304968	collection	January 2016

Cited By (2)

Towards Better Understanding of the Interactions and Efficient Application of Plant Beneficial Prebiotics, Probiotics, Postbiotics and Synbiotics Vassileva, Maria; Flor-Peregrin, Elena; Malusá, Eligio Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.01068	journal	July 2020
Chemical fertilization: a short‐term solution for plant productivity? Molina‐Santiago, Carlos; Matilla, Miguel A. Microbial Biotechnology, Vol. 13, Issue 5 https://doi.org/10.1111/1751-7915.13515	journal	November 2019

Similar Records

Over 150 years of long-term fertilization alters spatial scaling of microbial biodiversity

Journal Article · Mon Apr 06 20:00:00 EDT 2015 · mBio (Online) · OSTI ID:1215660

Taxa-area Relationship (TAR) of Microbial Functional Genes with Long-TGerm Fertilization

Technical Report · Mon May 17 00:00:00 EDT 2010 · OSTI ID:985942

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Plant–microbe networks in soil are weakened by century-long use of inorganic fertilizers

Citation Formats

References (63)

Cited By (2)

Similar Records

Related Subjects