Over 150 years of long-term fertilization alters spatial scaling of microbial biodiversity
Abstract
Spatial scaling is a critical issue in ecology, but how anthropogenic activities like fertilization affect spatial scaling is poorly understood, especially for microbial communities. Here, we determined the effects of long-term fertilization on the spatial scaling of microbial functional diversity and its relationships to plant diversity in the 150-year-old Park Grass Experiment, the oldest continuous grassland experiment in the world. Nested samples were taken from plots with contrasting inorganic fertilization regimes, and community DNAs were analyzed using the GeoChip-based functional gene array. The slopes of microbial gene-area relationships (GARs) and plant species-area relationships (SARs) were estimated in a plot receiving nitrogen (N), phosphorus (P), and potassium (K) and a control plot without fertilization. Our results indicated that long-term inorganic fertilization significantly increased both microbial GARs and plant SARs. Microbial spatial turnover rates (i.e., z values) were less than 0.1 and were significantly higher in the fertilized plot (0.0583) than in the control plot (0.0449) (P < 0.0001). The z values also varied significantly with different functional genes involved in carbon (C), N, P, and sulfur (S) cycling and with various phylogenetic groups (archaea, bacteria, and fungi). Similarly, the plant SARs increased significantly (P < 0.0001), from 0.225 in the controlmore »
- Authors:
-
- Chinese Academy of Sciences, Nanjing (China); Tsinghua Univ., Beijing (China); Univ. of Oklahoma, Norman, OK (United States)
- Univ. of Oklahoma, Norman, OK (United States)
- Rothamsted Research, Harpenden, Herts (United Kingdom)
- Tsinghua Univ., Beijing (China)
- Chinese Academy of Sciences, Nanjing (China)
- Tsinghua Univ., Beijing (China);Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab., Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1215660
- Alternate Identifier(s):
- OSTI ID: 1215661
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 6; Journal Issue: 2; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES
Citation Formats
Liang, Yuting, Wu, Liyou, Clark, Ian M., Xue, Kai, Yang, Yunfeng, Van Nostrand, Joy D., Deng, Ye, He, Zhili, McGrath, Steve, Storkey, Jonathan, Hirsch, Penny R., Sun, Bo, and Zhou, Jizhong. Over 150 years of long-term fertilization alters spatial scaling of microbial biodiversity. United States: N. p., 2015.
Web. doi:10.1128/mBio.00240-15.
Liang, Yuting, Wu, Liyou, Clark, Ian M., Xue, Kai, Yang, Yunfeng, Van Nostrand, Joy D., Deng, Ye, He, Zhili, McGrath, Steve, Storkey, Jonathan, Hirsch, Penny R., Sun, Bo, & Zhou, Jizhong. Over 150 years of long-term fertilization alters spatial scaling of microbial biodiversity. United States. https://doi.org/10.1128/mBio.00240-15
Liang, Yuting, Wu, Liyou, Clark, Ian M., Xue, Kai, Yang, Yunfeng, Van Nostrand, Joy D., Deng, Ye, He, Zhili, McGrath, Steve, Storkey, Jonathan, Hirsch, Penny R., Sun, Bo, and Zhou, Jizhong. Tue .
"Over 150 years of long-term fertilization alters spatial scaling of microbial biodiversity". United States. https://doi.org/10.1128/mBio.00240-15. https://www.osti.gov/servlets/purl/1215660.
@article{osti_1215660,
title = {Over 150 years of long-term fertilization alters spatial scaling of microbial biodiversity},
author = {Liang, Yuting and Wu, Liyou and Clark, Ian M. and Xue, Kai and Yang, Yunfeng and Van Nostrand, Joy D. and Deng, Ye and He, Zhili and McGrath, Steve and Storkey, Jonathan and Hirsch, Penny R. and Sun, Bo and Zhou, Jizhong},
abstractNote = {Spatial scaling is a critical issue in ecology, but how anthropogenic activities like fertilization affect spatial scaling is poorly understood, especially for microbial communities. Here, we determined the effects of long-term fertilization on the spatial scaling of microbial functional diversity and its relationships to plant diversity in the 150-year-old Park Grass Experiment, the oldest continuous grassland experiment in the world. Nested samples were taken from plots with contrasting inorganic fertilization regimes, and community DNAs were analyzed using the GeoChip-based functional gene array. The slopes of microbial gene-area relationships (GARs) and plant species-area relationships (SARs) were estimated in a plot receiving nitrogen (N), phosphorus (P), and potassium (K) and a control plot without fertilization. Our results indicated that long-term inorganic fertilization significantly increased both microbial GARs and plant SARs. Microbial spatial turnover rates (i.e., z values) were less than 0.1 and were significantly higher in the fertilized plot (0.0583) than in the control plot (0.0449) (P < 0.0001). The z values also varied significantly with different functional genes involved in carbon (C), N, P, and sulfur (S) cycling and with various phylogenetic groups (archaea, bacteria, and fungi). Similarly, the plant SARs increased significantly (P < 0.0001), from 0.225 in the control plot to 0.419 in the fertilized plot. Soil fertilization, plant diversity, and spatial distance had roughly equal contributions in shaping the microbial functional community structure, while soil geochemical variables contributed less. These results indicated that long-term agricultural practice could alter the spatial scaling of microbial biodiversity. Determining the spatial scaling of microbial biodiversity and its response to human activities is important but challenging in microbial ecology. Most studies to date are based on different sites that may not be truly comparable or on short-term perturbations, and hence, the results observed could represent transient responses. This study examined the spatial patterns of microbial communities in response to different fertilization regimes at the Rothamsted Research Experimental Station, which has become an invaluable resource for ecologists, environmentalists, and soil scientists. The current study is the first showing that long-term fertilization has dramatic impacts on the spatial scaling of microbial communities. By identifying the spatial patterns in response to long-term fertilization and their underlying mechanisms, this study makes fundamental contributions to predictive understanding of microbial biogeography.},
doi = {10.1128/mBio.00240-15},
journal = {mBio (Online)},
number = 2,
volume = 6,
place = {United States},
year = {Tue Apr 07 00:00:00 EDT 2015},
month = {Tue Apr 07 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Stochastic Assembly Leads to Alternative Communities with Distinct Functions in a Bioreactor Microbial Community
journal, March 2013
- Zhou, Jizhong; Liu, Wenzong; Deng, Ye
- mBio, Vol. 4, Issue 2
Beyond biogeographic patterns: processes shaping the microbial landscape
journal, May 2012
- Hanson, China A.; Fuhrman, Jed A.; Horner-Devine, M. Claire
- Nature Reviews Microbiology, Vol. 10, Issue 7
Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices
journal, September 2007
- He, Ji-zheng; Shen, Ju-pei; Zhang, Li-mei
- Environmental Microbiology, Vol. 9, Issue 9
DNA recovery from soils of diverse composition.
journal, January 1996
- Zhou, J.; Bruns, M. A.; Tiedje, J. M.
- Applied and environmental microbiology, Vol. 62, Issue 2
Microbial biogeography: putting microorganisms on the map
journal, February 2006
- Martiny, Jennifer B. Hughes; Bohannan, Brendan J. M.; Brown, James H.
- Nature Reviews Microbiology, Vol. 4, Issue 2
Spatial scaling of arbuscular mycorrhizal fungal diversity is affected by farming practice: Spatial scaling of arbuscular mycorrhizal fungi
journal, September 2010
- van der Gast, Christopher J.; Gosling, Paul; Tiwari, Bela
- Environmental Microbiology, Vol. 13, Issue 1
Grassland diversity under changing productivity and the underlying mechanisms - results of a 10-yr experiment
journal, March 2012
- Liira, Jaan; Ingerpuu, Nele; Kalamees, Rein
- Journal of Vegetation Science, Vol. 23, Issue 5
Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies
journal, October 2008
- Treseder, Kathleen K.
- Ecology Letters, Vol. 11, Issue 10
The imprint of the geographical, evolutionary and ecological context on species-area relationships: Imprint on species-area relationships
journal, November 2005
- Drakare, Stina; Lennon, Jack J.; Hillebrand, Helmut
- Ecology Letters, Vol. 9, Issue 2
Direct effect of fertilization on microbial carbon transformation in grassland soils in dependence on the substrate quality
journal, February 2010
- Kaštovská, Eva; Šantrůčková, Hana; Picek, Tomáš
- Journal of Plant Nutrition and Soil Science, Vol. 173, Issue 5
Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2
journal, July 2011
- Zhou, Jizhong; Deng, Ye; Luo, Feng
- mBio, Vol. 2, Issue 4
Patterns of elevational beta diversity in micro- and macroorganisms: Species turnover along elevational gradients
journal, April 2012
- Wang, Jianjun; Soininen, Janne; Zhang, Yong
- Global Ecology and Biogeography, Vol. 21, Issue 7
Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes
journal, February 2013
- Wang, Jianjun; Shen, Ji; Wu, Yucheng
- The ISME Journal, Vol. 7, Issue 7
Grassland management influences spatial patterns of soil microbial communities
journal, June 2013
- Sayer, Emma J.; Wagner, Markus; Oliver, Anna E.
- Soil Biology and Biochemistry, Vol. 61
A global perspective on belowground carbon dynamics under nitrogen enrichment: Belowground C dynamics under N enrichment
journal, May 2010
- Liu, Lingli; Greaver, Tara L.
- Ecology Letters, Vol. 13, Issue 7
Plant species and nitrogen effects on soil biological properties of temperate upland grasslands
journal, October 1999
- Bardgett, R. D.; Mawdsley, J. L.; Edwards, S.
- Functional Ecology, Vol. 13, Issue 5
Effects of elevated CO2 and nitrogen fertilization pretreatments on decomposition on tallgrass prairie leaf litter
journal, March 1994
- Kemp, Paul R.; Waldecker, Deborah G.; Owensby, Clenton E.
- Plant and Soil, Vol. 165, Issue 1
Arbuscular mycorrhizal fungal community structure and diversity in response to long-term fertilization: a field case from China
journal, May 2010
- Wang, Fa Yuan; Hu, Jun Li; Lin, Xian Gui
- World Journal of Microbiology and Biotechnology, Vol. 27, Issue 1
Community genetics: resource addition has opposing effects on genetic and species diversity in a 150-year experiment
journal, February 2009
- Silvertown, Jonathan; Biss, Pamela M.; Freeland, Joanna
- Ecology Letters, Vol. 12, Issue 2
Perturbations Alter Community Convergence, Divergence, and Formation of Multiple Community States
journal, August 2008
- Houseman, Gregory R.; Mittelbach, Gary G.; Reynolds, Heather L.
- Ecology, Vol. 89, Issue 8
A melange of curves - further dialogue about species-area relationships
journal, November 2004
- Scheiner, Samuel M.
- Global Ecology and Biogeography, Vol. 13, Issue 6
Size and activity of soil microbial communities in long-term experimental grassland plots treated with manure and inorganic fertilizers
journal, April 1996
- Hopkins, D. W.; Shiel, R. S.
- Biology and Fertility of Soils, Vol. 22, Issue 1-2
Long-term effects of nitrogen fertilization on methane oxidation in soil of the broadbalk wheat experiment
journal, October 1993
- Hütsch, Birgit W.; Webster, Colin P.; Powlson, David S.
- Soil Biology and Biochemistry, Vol. 25, Issue 10
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
journal, January 2011
- Rousk, Johannes; Brookes, Philip C.; Bååth, Erland
- FEMS Microbiology Ecology, Vol. 76, Issue 1
Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems
journal, August 2007
- Allison, Steven D.; Hanson, China A.; Treseder, Kathleen K.
- Soil Biology and Biochemistry, Vol. 39, Issue 8
The Park Grass Experiment 1856-2006: its contribution to ecology
journal, May 2006
- Silvertown, Jonathan; Poulton, Paul; Johnston, Edward
- Journal of Ecology, Vol. 94, Issue 4
Bacterial taxa-area and distance-decay relationships in marine environments
journal, January 2014
- Zinger, L.; Boetius, A.; Ramette, A.
- Molecular Ecology, Vol. 23, Issue 4
Biogeography: An Emerging Cornerstone for Understanding Prokaryotic Diversity, Ecology, and Evolution
journal, November 2006
- Ramette, Alban; Tiedje, James M.
- Microbial Ecology, Vol. 53, Issue 2
Stochasticity, succession, and environmental perturbations in a fluidic ecosystem
journal, February 2014
- Zhou, Jizhong; Deng, Ye; Zhang, Ping
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
Activity and Composition of the Denitrifying Bacterial Community Respond Differently to Long-Term Fertilization
journal, December 2005
- Enwall, K.; Philippot, L.; Hallin, S.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
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
Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks
journal, January 1999
- Aerts, R.
- Journal of Experimental Botany, Vol. 50, Issue 330
Human impacts on the species?area relationship in reef fish assemblages
journal, September 2007
- Tittensor, Derek P.; Micheli, Fiorenza; Nyström, Magnus
- Ecology Letters, Vol. 10, Issue 9
Environmental and plant community determinants of species loss following nitrogen enrichment
journal, July 2007
- Clark, Chris M.; Cleland, Elsa E.; Collins, Scott L.
- Ecology Letters, Vol. 10, Issue 7
Seasonal controls on grassland microbial biogeography: Are they governed by plants, abiotic properties or both?
journal, April 2014
- Regan, Kathleen M.; Nunan, Naoise; Boeddinghaus, Runa S.
- Soil Biology and Biochemistry, Vol. 71
A taxa–area relationship for bacteria
journal, December 2004
- Horner-Devine, M. Claire; Lage, Melissa; Hughes, Jennifer B.
- Nature, Vol. 432, Issue 7018
Consequences of changing biodiversity
journal, May 2000
- Chapin III, F. Stuart; Zavaleta, Erika S.; Eviner, Valerie T.
- Nature, Vol. 405, Issue 6783
Scale-Dependent Responses of Plant Biodiversity to Nitrogen Enrichment
journal, August 2008
- Chalcraft, David R.; Cox, Stephen B.; Clark, Christopher
- Ecology, Vol. 89, Issue 8
The power of species sorting: Local factors drive bacterial community composition over a wide range of spatial scales
journal, December 2007
- Van der Gucht, K.; Cottenie, K.; Muylaert, K.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 51
Changes in soil phosphorus forms through time in perennial versus annual agroecosystems
journal, February 2014
- Crews, Timothy E.; Brookes, Philip C.
- Agriculture, Ecosystems & Environment, Vol. 184
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
Community assembly: when should history matter?
journal, August 2003
- Chase, Jonathan M.
- Oecologia, Vol. 136, Issue 4
Competition Among Grasses Along a Nitrogen Gradient: Initial Conditions and Mechanisms of Competition
journal, February 1993
- Wedin, David; Tilman, David
- Ecological Monographs, Vol. 63, Issue 2
Microbial macroecology: highly structured prokaryotic soil assemblages in a tropical deciduous forest: Prokaryotic macroecology
journal, May 2005
- Noguez, Ana M.; Arita, Héctor T.; Escalante, Ana E.
- Global Ecology and Biogeography, Vol. 14, Issue 3
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
Development of a Common Oligonucleotide Reference Standard for Microarray Data Normalization and Comparison across Different Microbial Communities
journal, December 2009
- Liang, Y.; He, Z.; Wu, L.
- Applied and Environmental Microbiology, Vol. 76, Issue 4
Changes in species diversity following habitat disturbance are dependent on spatial scale: theoretical and empirical evidence
journal, October 2008
- Dumbrell, Alex J.; Clark, Ewen J.; Frost, Gillian A.
- Journal of Applied Ecology, Vol. 45, Issue 5
Community Structure of Ammonia-Oxidizing Bacteria under Long-Term Application of Mineral Fertilizer and Organic Manure in a Sandy Loam Soil
journal, November 2006
- Chu, H.; Fujii, T.; Morimoto, S.
- Applied and Environmental Microbiology, Vol. 73, Issue 2
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
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
Ecological Linkages Between Aboveground and Belowground Biota
journal, June 2004
- Wardle, D. A.
- Science, Vol. 304, Issue 5677
Spatial scaling of microbial biodiversity
journal, September 2006
- Green, Jessica; Bohannan, Brendan J. M.
- Trends in Ecology & Evolution, Vol. 21, Issue 9
Impact of Nitrogen Deposition on the Species Richness of Grasslands
journal, March 2004
- Stevens, C. J.
- Science, Vol. 303, Issue 5665
Structure of functional ecological networks of soil microbial communities for nitrogen transformations and their response to cropping in major soils in eastern China
journal, January 2014
- Sun, Bo; Wang, Feng; Zhou, JiZhong
- Chinese Science Bulletin, Vol. 59, Issue 4-5
Microarray-Based Analysis of Subnanogram Quantities of Microbial Community DNAs by Using Whole-Community Genome Amplification
journal, July 2006
- Wu, L.; Liu, X.; Schadt, C. W.
- Applied and Environmental Microbiology, Vol. 72, Issue 7
Drivers of bacterial -diversity depend on spatial scale
journal, April 2011
- Martiny, J. B. H.; Eisen, J. A.; Penn, K.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 19
Does Ecosystem size Determine Aquatic Bacterial Richness?
journal, July 2005
- Reche, Isabel; Pulido-Villena, Elvira; Morales-Baquero, Rafael
- Ecology, Vol. 86, Issue 7
Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems
journal, December 2010
- Ramirez, Kelly S.; Lauber, Christian L.; Knight, Rob
- Ecology, Vol. 91, Issue 12
Scale Dependence in Plant Biodiversity
journal, February 2001
- Crawley, M. J.
- Science, Vol. 291, Issue 5505
Toward an Ecological Classification of soil Bacteria
journal, June 2007
- Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
- Ecology, Vol. 88, Issue 6
Functional Molecular Ecological Networks
journal, October 2010
- Zhou, Jizhong; Deng, Ye; Luo, Feng
- mBio, Vol. 1, Issue 4
Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity
journal, February 2013
- Ranjard, L.; Dequiedt, S.; Chemidlin Prévost-Bouré, N.
- Nature Communications, Vol. 4, Issue 1
Works referencing / citing this record:
Plant–microbe networks in soil are weakened by century‐long use of inorganic fertilizers
journal, July 2019
- Huang, Ruilin; McGrath, Steve P.; Hirsch, Penny R.
- Microbial Biotechnology, Vol. 12, Issue 6
Mineral vs. Organic Amendments: Microbial Community Structure, Activity and Abundance of Agriculturally Relevant Microbes Are Driven by Long-Term Fertilization Strategies
journal, September 2016
- Francioli, Davide; Schulz, Elke; Lentendu, Guillaume
- Frontiers in Microbiology, Vol. 7
Spatial scaling of forest soil microbial communities across a temperature gradient: Temperature altered microbial spatial scaling
journal, September 2018
- Deng, Ye; Ning, Daliang; Qin, Yujia
- Environmental Microbiology, Vol. 20, Issue 10
Microbiomes of China’s Space Station During Assembly, Integration, and Test Operations
journal, February 2019
- Zhang, Ying; Zhang, Lan-tao; Li, Zhi-dong
- Microbial Ecology, Vol. 78, Issue 3