Rainfall events stimulate episodic associative nitrogen fixation in switchgrass

Vizza, Carmella; Belanger, Matthew A.; Jones, Jabarius; Murphy, Sean J.; Buckley, Daniel H.; Robertson, G. Philip; Roley, Sarah S.

doi:10.1007/s10533-024-01180-w

Rainfall events stimulate episodic associative nitrogen fixation in switchgrass

Journal Article · Thu Oct 03 00:00:00 EDT 2024 · Biogeochemistry (Online)

DOI:https://doi.org/10.1007/s10533-024-01180-w· OSTI ID:2455048

; Belanger, Matthew A.; Jones, Jabarius; Murphy, Sean J.; Buckley, Daniel H.; Robertson, G. Philip; Roley, Sarah S.

Abstract

Associative N ₂ fixation (ANF) is widespread but poorly characterized, limiting our ability to estimate global inputs from N ₂ fixation. In some places, ANF rates are at or below detection most of the time but occasionally and unpredictably spiking to very high rates. Here we test the hypothesis that plant phenology and rainfall events stimulate ANF episodes. We measured ANF in intact soil cores in switchgrass ( Panicum virgatum L.) in Michigan, USA. We used rain exclusion shelters to impose three rainfall treatments with each receiving 60 mm of water over a 20-day period but at different frequencies. We concurrently established a treatment that received ambient rainfall, and all four treatments were replicated four times. To assess the effects of plant phenology, we measured ANF at key phenological stages in the ambient treatment. To assess the effects of rainfall, we measured ANF immediately before and immediately after each wetting event in each treatment involving rainfall manipulation. We found that the previous day’s rainfall could explain 29% of the variation in ANF rates within the ambient treatment alone, and that bulk soil C:N ratio was also positively correlated with ANF, explaining 18% of the variation alone. Wetting events increased ANF and the magnitude of response to wetting increased with the amount of water added and decreased with the amount of inorganic N added in water. ANF episodes thus appear to be driven primarily by wetting events. Wetting events likely increase C availability, promote microbial growth, and make rhizosphere conditions conducive to ANF.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0018409

OSTI ID:: 2455048

Journal Information:: Biogeochemistry (Online), Journal Name: Biogeochemistry (Online) Journal Issue: 11 Vol. 167; ISSN 1573-515X

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (61)

Stoichiometry controls asymbiotic nitrogen fixation and its response to nitrogen inputs in a nitrogen-saturated forest Zheng, Mianhai; Zhang, Wei; Luo, Yiqi Ecology, Vol. 99, Issue 9 https://doi.org/10.1002/ecy.2416	journal	July 2018
Effects of altered dry season length and plant inputs on soluble soil carbon Homyak, Peter M.; Blankinship, Joseph C.; Slessarev, Eric W. Ecology, Vol. 99, Issue 10 https://doi.org/10.1002/ecy.2473	journal	August 2018
Nitrogen fixation and denitrification in a floodplain forest near Manaus, Brazil Kreibich, Heidi; Kern, J�rgen Hydrological Processes, Vol. 17, Issue 7 https://doi.org/10.1002/hyp.1294	journal	January 2003
Denitrification and the challenge of scaling microsite knowledge to the globe Robertson, G. Philip mLife, Vol. 2, Issue 3 https://doi.org/10.1002/mlf2.12080	journal	September 2023
Mixed effects models and extensions in ecology with R Zuur, Alain F.; Ieno, Elena N.; Walker, Neil Statistics for Biology and Health https://doi.org/10.1007/978-0-387-87458-6	book	January 2009
Nitrogenase activity associated with some wisconsin prairie grasses Tjepkema, J. D.; Burris, R. H. Plant and Soil, Vol. 45, Issue 1 https://doi.org/10.1007/BF00011131	journal	August 1976
The effect of soil drying on humus decomposition and nitrogen availability Birch, H. F. Plant and Soil, Vol. 10, Issue 1 https://doi.org/10.1007/BF01343734	journal	September 1958
Microbial community shifts influence patterns in tropical forest nitrogen fixation Reed, Sasha C.; Townsend, Alan R.; Cleveland, Cory C. Oecologia, Vol. 164, Issue 2 https://doi.org/10.1007/s00442-010-1649-6	journal	May 2010
Biogeochemical Hot Spots and Hot Moments at the Interface of Terrestrial and Aquatic Ecosystems McClain, Michael E.; Boyer, Elizabeth W.; Dent, C. Lisa Ecosystems, Vol. 6, Issue 4 https://doi.org/10.1007/s10021-003-0161-9	journal	June 2003
Carbon and Nitrogen Decoupling Under an 11-Year Drought in the Shortgrass Steppe Evans, Sarah E.; Burke, Ingrid C. Ecosystems, Vol. 16, Issue 1 https://doi.org/10.1007/s10021-012-9593-4	journal	September 2012
Control Points in Ecosystems: Moving Beyond the Hot Spot Hot Moment Concept Bernhardt, Emily S.; Blaszczak, Joanna R.; Ficken, Cari D. Ecosystems, Vol. 20, Issue 4 https://doi.org/10.1007/s10021-016-0103-y	journal	January 2017
Exploring the Role of Cryptic Nitrogen Fixers in Terrestrial Ecosystems: A Frontier in Nitrogen Cycling Research Cleveland, Cory C.; Reis, Carla R. G.; Perakis, Steven S. Ecosystems, Vol. 25, Issue 8 https://doi.org/10.1007/s10021-022-00804-2	journal	November 2022
Global inputs of biological nitrogen fixation in agricultural systems Herridge, David F.; Peoples, Mark B.; Boddey, Robert M. Plant and Soil, Vol. 311, Issue 1-2 https://doi.org/10.1007/s11104-008-9668-3	journal	July 2008
Optimization of the 15N2 incorporation and acetylene reduction methods for free-living nitrogen fixation Smercina, Darian N.; Evans, Sarah E.; Friesen, Maren L. Plant and Soil, Vol. 445, Issue 1-2 https://doi.org/10.1007/s11104-019-04307-3	journal	October 2019
Nitrogen transformations Robertson, G. P.; Groffman, P. M. Soil Microbiology, Ecology and Biochemistry https://doi.org/10.1016/B978-0-12-822941-5.00014-4	book	November 2023
Influence of dry–wet cycles on the interrelationship between aggregate, particulate organic matter, and microbial community dynamics Denef, Karolien; Six, Johan; Bossuyt, Heleen Soil Biology and Biochemistry, Vol. 33, Issue 12-13 https://doi.org/10.1016/S0038-0717(01)00076-1	journal	October 2001
Rainfall intensification increases nitrate leaching from tilled but not no-till cropping systems in the U.S. Midwest Hess, Laura J. T.; Hinckley, Eve-Lyn S.; Robertson, G. Philip Agriculture, Ecosystems & Environment, Vol. 290 https://doi.org/10.1016/j.agee.2019.106747	journal	March 2020
The intensity of water stress dictates whether the N status of temperate-type perennial grass swards is affected by drought Errecart, Pedro Manuel; Marino, María Alejandra; Agnusdei, Mónica Graciela Field Crops Research, Vol. 257 https://doi.org/10.1016/j.fcr.2020.107928	journal	October 2020
Early accumulation of active fraction soil carbon in newly established cellulosic biofuel systems Sprunger, Christine D.; Philip Robertson, G. Geoderma, Vol. 318 https://doi.org/10.1016/j.geoderma.2017.11.040	journal	May 2018
Soil redox dynamics under dynamic hydrologic regimes - A review Zhang, Zengyu; Furman, Alex Science of The Total Environment, Vol. 763 https://doi.org/10.1016/j.scitotenv.2020.143026	journal	April 2021
Synergistic effects of diffusion and microbial physiology reproduce the Birch effect in a micro-scale model Evans, Sarah; Dieckmann, Ulf; Franklin, Oskar Soil Biology and Biochemistry, Vol. 93 https://doi.org/10.1016/j.soilbio.2015.10.020	journal	February 2016
Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA Liang, Chao; Jesus, Ederson da C.; Duncan, David S. Soil Biology and Biochemistry, Vol. 94 https://doi.org/10.1016/j.soilbio.2015.11.020	journal	March 2016
Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.) Roley, Sarah S.; Xue, Chao; Hamilton, Stephen K. Soil Biology and Biochemistry, Vol. 129 https://doi.org/10.1016/j.soilbio.2018.11.006	journal	February 2019
Global patterns of terrestrial biological nitrogen (N ₂ ) fixation in natural ecosystems Cleveland, Cory C.; Townsend, Alan R.; Schimel, David S. Global Biogeochemical Cycles, Vol. 13, Issue 2 https://doi.org/10.1029/1999GB900014	journal	June 1999
Evidence for the functional significance of diazotroph community structure in soil Hsu, Shi-Fang; Buckley, Daniel H. The ISME Journal, Vol. 3, Issue 1 https://doi.org/10.1038/ismej.2008.82	journal	September 2008
Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil Blazewicz, Steven J.; Hungate, Bruce A.; Koch, Benjamin J. The ISME Journal, Vol. 14, Issue 6 https://doi.org/10.1038/s41396-020-0617-3	journal	March 2020
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Global nitrogen budgets in cereals: A 50-year assessment for maize, rice and wheat production systems Ladha, J. K.; Tirol-Padre, A.; Reddy, C. K. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19355	journal	January 2016
Characterization of Root Exudates at Different Growth Stages of Ten Rice (Oryza sativa L.) Cultivars Aulakh, M. S.; Wassmann, R.; Bueno, C. Plant Biology, Vol. 3, Issue 2 https://doi.org/10.1055/s-2001-12905	journal	March 2001
Field measurements of nitrogenase activity in soils amended with wheat straw Roper, Mm Australian Journal of Agricultural Research, Vol. 34, Issue 6 https://doi.org/10.1071/AR9830725	journal	January 1983
Nitrogen cycling in summer active perennial grass systems in South Australia: non-symbiotic nitrogen fixation Gupta, V. V. S. R.; Kroker, S. J.; Hicks, M. Crop and Pasture Science, Vol. 65, Issue 10 https://doi.org/10.1071/CP14109	journal	January 2014
Dormancy contributes to the maintenance of microbial diversity Jones, S. E.; Lennon, J. T. Proceedings of the National Academy of Sciences, Vol. 107, Issue 13 https://doi.org/10.1073/pnas.0912765107	journal	March 2010
Human influence has intensified extreme precipitation in North America Kirchmeier-Young, Megan C.; Zhang, Xuebin Proceedings of the National Academy of Sciences, Vol. 117, Issue 24 https://doi.org/10.1073/pnas.1921628117	journal	June 2020
Beyond Cohen'sd: Alternative Effect Size Measures for Between-Subject Designs Peng, Chao-Ying Joanne; Chen, Li-Ting The Journal of Experimental Education, Vol. 82, Issue 1 https://doi.org/10.1080/00220973.2012.745471	journal	August 2013
Senescence and nitrogen use efficiency in perennial grasses for forage and biofuel production Yang, Jiading; Udvardi, Michael Journal of Experimental Botany, Vol. 69, Issue 4 https://doi.org/10.1093/jxb/erx241	journal	August 2017
Influence of corn, switchgrass, and prairie cropping systems on soil microbial communities in the upper Midwest of the United States Jesus, Ederson da C.; Liang, Chao; Quensen, John F. GCB Bioenergy, Vol. 8, Issue 2 https://doi.org/10.1111/gcbb.12289	journal	December 2015
Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils Borken, Werner; Matzner, Egbert Global Change Biology, Vol. 15, Issue 4 https://doi.org/10.1111/j.1365-2486.2008.01681.x	journal	April 2009
Regulation and function of root exudates Badri, Dayakar V.; Vivanco, Jorge M. Plant, Cell & Environment, Vol. 32, Issue 6 https://doi.org/10.1111/j.1365-3040.2009.01926.x	journal	June 2009
To Fix or Not To Fix: Controls on Free-Living Nitrogen Fixation in the Rhizosphere Smercina, Darian N.; Evans, Sarah E.; Friesen, Maren L. Applied and Environmental Microbiology, Vol. 85, Issue 6 https://doi.org/10.1128/AEM.02546-18	journal	January 2019
Evaluation of nitrogen fixation by bacteria in association with roots of tropical grasses van Berkum, P.; Bohlool, B. B. Microbiological Reviews, Vol. 44, Issue 3 https://doi.org/10.1128/mr.44.3.491-517.1980	journal	September 1980
Non-Symbiotic Nitrogen Fixation in some Quebec Soils Chang, P-C.; Knowles, R. Canadian Journal of Microbiology, Vol. 11, Issue 1 https://doi.org/10.1139/m65-005	journal	February 1965
The effect of organic amendment, water content, and oxygen on the incorporation of ¹⁵ N ₂ by some agricultural and forest soils Brouzes, R.; Lasik, J.; Knowles, R. Canadian Journal of Microbiology, Vol. 15, Issue 8 https://doi.org/10.1139/m69-160	journal	August 1969
Functional Ecology of Free-Living Nitrogen Fixation: A Contemporary Perspective Reed, Sasha C.; Cleveland, Cory C.; Townsend, Alan R. Annual Review of Ecology, Evolution, and Systematics, Vol. 42, Issue 1 https://doi.org/10.1146/annurev-ecolsys-102710-145034	journal	December 2011
Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes Schimel, Joshua P. Annual Review of Ecology, Evolution, and Systematics, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110617-062614	journal	November 2018
Oxygen and Hydrogen in Biological Nitrogen Fixation Robson, R. L.; Postgate, J. R. Annual Review of Microbiology, Vol. 34, Issue 1 https://doi.org/10.1146/annurev.mi.34.100180.001151	journal	October 1980
The Contamination of Commercial 15N2 Gas Stocks with 15N–Labeled Nitrate and Ammonium and Consequences for Nitrogen Fixation Measurements Dabundo, Richard; Lehmann, Moritz F.; Treibergs, Lija PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0110335	journal	October 2014
Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient Roley, Sarah S.; Duncan, David S.; Liang, Di PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0197320	journal	June 2018
Heterotrophic Nitrogen Fixation in Decomposing Litter: Patterns and Regulation Vitousek, Peter M.; Hobbie, Sarah Ecology, Vol. 81, Issue 9 https://doi.org/10.1890/0012-9658(2000)081[2366:HNFIDL]2.0.CO;2	journal	September 2000
Microbial Stress-Response Physiology and its Implications for Ecosystem Function Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/06-0219	journal	June 2007
Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil Blazewicz, Steven J.; Schwartz, Egbert; Firestone, Mary K. Ecology, Vol. 95, Issue 5 https://doi.org/10.1890/13-1031.1	journal	May 2014
Morphological Development of Switchgrass and Kleingrass Sanderson, Matt A. Agronomy Journal, Vol. 84, Issue 3 https://doi.org/10.2134/agronj1992.00021962008400030013x	journal	January 1992
Nitrogen Fixation in a Gulf Coast Salt Marsh1 Casselman, Mieke E.; Patrick, W. H.; DeLaune, R. D. Soil Science Society of America Journal, Vol. 45, Issue 1 https://doi.org/10.2136/sssaj1981.03615995004500010012x	journal	January 1981
Contribution of Nitrogen Fixation to Sugar Cane: Nitrogen‐15 and Nitrogen‐Balance Estimates Urquiaga, Segundo; Cruz, Kátia H. S.; Boddey, Robert M. Soil Science Society of America Journal, Vol. 56, Issue 1 https://doi.org/10.2136/sssaj1992.03615995005600010017x	journal	January 1992
Flush of Carbon Dioxide Following Rewetting of Dried Soil Relates to Active Organic Pools Franzluebbers, A. J.; Haney, R. L.; Honeycutt, C. W. Soil Science Society of America Journal, Vol. 64, Issue 2 https://doi.org/10.2136/sssaj2000.642613x	journal	January 2000
Release of Intracellular Solutes by Four Soil Bacteria Exposed to Dilution Stress Halverson, Larry J.; Jones, Thomas M.; Firestone, Mary K. Soil Science Society of America Journal, Vol. 64, Issue 5 https://doi.org/10.2136/sssaj2000.6451630x	journal	January 2000
Drought-Induced Nitrogen Retranslocation in Perennial C4 Grasses of Tallgrass Prairie Heckathorn, Scott A.; DeLucia, Evan H. Ecology, Vol. 75, Issue 7 https://doi.org/10.2307/1941592	journal	October 1994
A Critique and Improvement of the CL Common Language Effect Size Statistics of McGraw and Wong Vargha, András; Delaney, Harold D. Journal of Educational and Behavioral Statistics, Vol. 25, Issue 2 https://doi.org/10.3102/10769986025002101	journal	June 2000
Plant growth and phenolic compounds in the rhizosphere soil of wild oat (Avena fatua L.) Iannucci, Anna; Fragasso, Mariagiovanna; Platani, Cristiano Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00509	journal	January 2013
Quantifying and correcting for pre-assay CO₂ loss in short-term carbon mineralization assays Belanger, Matthew A.; Vizza, Carmella; Robertson, G. Philip SOIL, Vol. 7, Issue 1 https://doi.org/10.5194/soil-7-47-2021	journal	January 2021
KBS Soils Crum, J. R.; Collins, H. P. Zenodo https://doi.org/10.5281/ZENODO.2581504	text	January 1995
Seasonal Changes in N2 Fixation Activity and N Enrichment in Paddy Soils as Affected by Soil Management in the Northern Area of Japan Kondo, Motohiko; Yasuda, Michio Japan Agricultural Research Quarterly: JARQ, Vol. 37, Issue 2 https://doi.org/10.6090/jarq.37.105	journal	January 2003

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