Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.)
Abstract
Perennial grasses can assimilate nitrogen (N) fixed by non-nodulating bacteria living in the rhizosphere and the plant's own tissues, but many details of associative N fixation (ANF) remain unknown, including ANF's contribution to grass N nutrition, the exact location of fixation, and composition of the associated microbial community. We examined ANF in switchgrass (Panicum virgatum L.), a North American perennial grass, using 15N-enriched N2 isotopic tracer additions in a combination of in vitro, greenhouse, and field experiments to estimate how much N is assimilated, where fixation takes place, and the likely N-fixing taxa present. Using in vitro incubations, we documented fixation in root-free rhizosphere soil and on root surfaces, with average rates of 3.8 μg N g root-1 d-1 on roots and 0.81 μg N g soil-1 d-1 in soil. In greenhouse transplants, N fixation occurred only in the early growing season, but in the field, fixation was irregularly detectable throughout the 3-month growing season. Soil, leaves, stems, and roots all contained diazotrophs and incorporated fixed N2. Metagenomic analysis suggested that microbial communities were distinct among tissue types and influenced by N fertilizer application. A diverse array of microbes inhabiting the rhizosphere, and possibly aboveground tissues, appear to be episodicallymore »
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1482430
- Alternate Identifier(s):
- OSTI ID: 1506679
- Grant/Contract Number:
- SC0018409; FC02-07ER64494; DEB 1637653
- Resource Type:
- Published Article
- Journal Name:
- Soil Biology and Biochemistry
- Additional Journal Information:
- Journal Name: Soil Biology and Biochemistry Journal Volume: 129 Journal Issue: C; Journal ID: ISSN 0038-0717
- Publisher:
- Elsevier
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Associative nitrogen fixation; Diazotroph; Rhizosphere; Stable isotopes; Switchgrass
Citation Formats
Roley, Sarah S., Xue, Chao, Hamilton, Stephen K., Tiedje, James M., and Robertson, G. Philip. Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.). United Kingdom: N. p., 2019.
Web. doi:10.1016/j.soilbio.2018.11.006.
Roley, Sarah S., Xue, Chao, Hamilton, Stephen K., Tiedje, James M., & Robertson, G. Philip. Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.). United Kingdom. https://doi.org/10.1016/j.soilbio.2018.11.006
Roley, Sarah S., Xue, Chao, Hamilton, Stephen K., Tiedje, James M., and Robertson, G. Philip. Fri .
"Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.)". United Kingdom. https://doi.org/10.1016/j.soilbio.2018.11.006.
@article{osti_1482430,
title = {Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.)},
author = {Roley, Sarah S. and Xue, Chao and Hamilton, Stephen K. and Tiedje, James M. and Robertson, G. Philip},
abstractNote = {Perennial grasses can assimilate nitrogen (N) fixed by non-nodulating bacteria living in the rhizosphere and the plant's own tissues, but many details of associative N fixation (ANF) remain unknown, including ANF's contribution to grass N nutrition, the exact location of fixation, and composition of the associated microbial community. We examined ANF in switchgrass (Panicum virgatum L.), a North American perennial grass, using 15N-enriched N2 isotopic tracer additions in a combination of in vitro, greenhouse, and field experiments to estimate how much N is assimilated, where fixation takes place, and the likely N-fixing taxa present. Using in vitro incubations, we documented fixation in root-free rhizosphere soil and on root surfaces, with average rates of 3.8 μg N g root-1 d-1 on roots and 0.81 μg N g soil-1 d-1 in soil. In greenhouse transplants, N fixation occurred only in the early growing season, but in the field, fixation was irregularly detectable throughout the 3-month growing season. Soil, leaves, stems, and roots all contained diazotrophs and incorporated fixed N2. Metagenomic analysis suggested that microbial communities were distinct among tissue types and influenced by N fertilizer application. A diverse array of microbes inhabiting the rhizosphere, and possibly aboveground tissues, appear to be episodically contributing fixed N to switchgrass.},
doi = {10.1016/j.soilbio.2018.11.006},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 129,
place = {United Kingdom},
year = {Fri Feb 01 00:00:00 EST 2019},
month = {Fri Feb 01 00:00:00 EST 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.soilbio.2018.11.006
https://doi.org/10.1016/j.soilbio.2018.11.006
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 36 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States
journal, August 2018
- Mackelprang, Rachel; Grube, Alyssa M.; Lamendella, Regina
- Frontiers in Microbiology, Vol. 9
Isolation and characterization of N 2 -fixing bacteria from giant reed and switchgrass for plant growth promotion and nutrient uptake
journal, February 2018
- Xu, Jia; Kloepper, Joseph W.; Huang, Ping
- Journal of Basic Microbiology, Vol. 58, Issue 5
Variations in the 15N natural abundance of plant-available N with soil depth: Their influence on estimates of contributions of biological N2 fixation to sugar cane
journal, January 2014
- Baptista, Rafael Butke; de Morais, Rafael Fiusa; Leite, José Marcos
- Applied Soil Ecology, Vol. 73
Evidence for enhanced N availability during switchgrass establishment and seeding year production following inoculation with rhizosphere endophytes
journal, March 2014
- Ker, Keomany; Seguin, Philippe; Driscoll, Brian T.
- Archives of Agronomy and Soil Science, Vol. 60, Issue 11
A lysimeter investigation of nitrogen gains and losses under various systems of covercropping and fertilization, and a discussion of error sources
journal, April 1949
- Chapman, H. D.; Liebig, G. F.; Rayner, D. S.
- Hilgardia, Vol. 19, Issue 3
Endophytic nitrogen fixation in sugarcane: present knowledge and future applications
journal, May 2003
- Boddey, Robert M.; Urquiaga, Segundo; Alves, Bruno J. R.
- Plant and Soil, Vol. 252, Issue 1
Soil Organic Matter, crop Yields, and land use in the Texas Blackland
journal, January 1954
- Smith, R. M.; Thompson, D. O.; Collier, J. W.
- Soil Science, Vol. 77, Issue 5
Soil Organic Carbon Sequestration Rates by Tillage and Crop Rotation
journal, January 2002
- West, Tristram O.; Post, Wilfred M.
- Soil Science Society of America Journal, Vol. 66, Issue 6, p. 1930-1946
Comparative Biogeochemical Cycles of Bioenergy Crops Reveal Nitrogen-Fixation and Low Greenhouse Gas Emissions in a Miscanthus × giganteus Agro-Ecosystem
journal, December 2009
- Davis, Sarah C.; Parton, William J.; Dohleman, Frank G.
- Ecosystems, Vol. 13, Issue 1
Evaluation of the Ion Torrent Personal Genome Machine for Gene-Targeted Studies Using Amplicons of the Nitrogenase Gene nifH
journal, April 2015
- Zhang, Bangzhou; Penton, C. Ryan; Xue, Chao
- Applied and Environmental Microbiology, Vol. 81, Issue 13
Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil
journal, January 2001
- Poly, Franck; Monrozier, Lucile Jocteur; Bally, René
- Research in Microbiology, Vol. 152, Issue 1
Control Points in Ecosystems: Moving Beyond the Hot Spot Hot Moment Concept
journal, January 2017
- Bernhardt, Emily S.; Blaszczak, Joanna R.; Ficken, Cari D.
- Ecosystems, Vol. 20, Issue 4
Methods for quantification of nitrogen fixation associated with gramineae
journal, January 1987
- Boddey, Robert M.; Knowles, Roger
- Critical Reviews in Plant Sciences, Vol. 6, Issue 3
Endophytic nitrogen fixation in dune grasses (Ammophila arenaria and Elymus mollis) from Oregon
journal, September 2004
- Dalton, David A.; Kramer, Sasha; Azios, Nico
- FEMS Microbiology Ecology, Vol. 49, Issue 3
Cellulosic biofuel contributions to a sustainable energy future: Choices and outcomes
journal, June 2017
- Robertson, G. Philip; Hamilton, Stephen K.; Barham, Bradford L.
- Science, Vol. 356, Issue 6345
Biological nitrogen fixation in non-legume plants
journal, March 2013
- Santi, Carole; Bogusz, Didier; Franche, Claudine
- Annals of Botany, Vol. 111, Issue 5
Bioenergy cropping systems that incorporate native grasses stimulate growth of plant-associated soil microbes in the absence of nitrogen fertilization
journal, October 2016
- Oates, Lawrence G.; Duncan, David S.; Sanford, Gregg R.
- Agriculture, Ecosystems & Environment, Vol. 233
Global inputs of biological nitrogen fixation in agricultural systems
journal, July 2008
- Herridge, David F.; Peoples, Mark B.; Boddey, Robert M.
- Plant and Soil, Vol. 311, Issue 1-2
Novel Endophytic Nitrogen-Fixing Clostridia from the Grass Miscanthus sinensis as Revealed by Terminal Restriction Fragment Length Polymorphism Analysis
journal, November 2004
- Miyamoto, T.; Kawahara, M.; Minamisawa, K.
- Applied and Environmental Microbiology, Vol. 70, Issue 11
Nitrogen cycling in summer active perennial grass systems in South Australia: non-symbiotic nitrogen fixation
journal, January 2014
- Gupta, V. V. S. R.; Kroker, S. J.; Hicks, M.
- Crop and Pasture Science, Vol. 65, Issue 10
Nitrogen fixation in endophytic and associative symbiosis
journal, March 2000
- James, E. K.
- Field Crops Research, Vol. 65, Issue 2-3
Biogeochemical Hot Spots and Hot Moments at the Interface of Terrestrial and Aquatic Ecosystems
journal, June 2003
- McClain, Michael E.; Boyer, Elizabeth W.; Dent, C. Lisa
- Ecosystems, Vol. 6, Issue 4
The feasibility of switchgrass for biofuel production
journal, January 2012
- Mitchell, Rob; Vogel, Kenneth P.; Uden, Daniel R.
- Biofuels, Vol. 3, Issue 1
Rapid N^2 Fixation in Pines, Alder, and Locust: Evidence From the Sandbox Ecosystems Study
journal, March 1993
- Bormann, Bernard T.; Bormann, F. Herbert; Bowden, William B.
- Ecology, Vol. 74, Issue 2
Morphological Development of Switchgrass and Kleingrass
journal, January 1992
- Sanderson, Matt A.
- Agronomy Journal, Vol. 84, Issue 3
Effects of soil rewetting and thawing on soil gas fluxes: a review of current literature and suggestions for future research
journal, January 2012
- Kim, D. -G.; Vargas, R.; Bond-Lamberty, B.
- Biogeosciences, Vol. 9, Issue 7
Do Forests Receive Occult Inputs of Nitrogen?
journal, July 2000
- Binkley, Dan; Son, Yowhan; Valentine, David W.
- Ecosystems, Vol. 3, Issue 4
Confirmation of nitrogen fixation in two tropical grasses by 15N2 incorporation
journal, January 1977
- De-Polli, Helvécio; Matsui, Eiichi; Döbereiner*, Johanna
- Soil Biology and Biochemistry, Vol. 9, Issue 2
FunGene: the functional gene pipeline and repository
journal, January 2013
- Fish, Jordan A.; Chai, Benli; Wang, Qiong
- Frontiers in Microbiology, Vol. 4
Influence of corn, switchgrass, and prairie cropping systems on soil microbial communities in the upper Midwest of the United States
journal, December 2015
- Jesus, Ederson da C.; Liang, Chao; Quensen, John F.
- GCB Bioenergy, Vol. 8, Issue 2
Switchgrass nitrogen response and estimated production costs on diverse sites
journal, April 2017
- Fike, John H.; Pease, James W.; Owens, Vance N.
- GCB Bioenergy, Vol. 9, Issue 10
Dependence of 3 Nebraska Sandhills Warm-Season Grasses on Vesicular-Arbuscular Mycorrhizae
journal, January 1993
- Brejda, J. J.; Yocom, D. H.; Moser, L. E.
- Journal of Range Management, Vol. 46, Issue 1
The Contamination of Commercial 15N2 Gas Stocks with 15N–Labeled Nitrate and Ammonium and Consequences for Nitrogen Fixation Measurements
journal, October 2014
- Dabundo, Richard; Lehmann, Moritz F.; Treibergs, Lija
- PLoS ONE, Vol. 9, Issue 10
Nitrogen fertilization challenges the climate benefit of cellulosic biofuels
journal, June 2016
- Ruan, Leilei; Bhardwaj, Ajay K.; Hamilton, Stephen K.
- Environmental Research Letters, Vol. 11, Issue 6
Enhancing Non-symbiotic N2 Fixation in Agriculture
journal, May 2016
- Roper, M. M.; Gupta, V. V. S. R.
- The Open Agriculture Journal, Vol. 10, Issue 1
Ecological Patterns of nifH Genes in Four Terrestrial Climatic Zones Explored with Targeted Metagenomics Using FrameBot, a New Informatics Tool
journal, September 2013
- Wang, Qiong; Quensen, John F.; Fish, Jordan A.
- mBio, Vol. 4, Issue 5
Heterotrophic 15 N 2 Fixation and Distribution of Newly Fixed Nitrogen in a Rice-Flooded Soil System
journal, July 1981
- Eskew, David L.; Eaglesham, Allan R. J.; App, A. A.
- Plant Physiology, Vol. 68, Issue 1
Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient
journal, June 2018
- Roley, Sarah S.; Duncan, David S.; Liang, Di
- PLOS ONE, Vol. 13, Issue 6
Comparative productivity of alternative cellulosic bioenergy cropping systems in the North Central USA
journal, January 2016
- Sanford, Gregg R.; Oates, Lawrence G.; Jasrotia, Poonam
- Agriculture, Ecosystems & Environment, Vol. 216
Measuring Simultaneous Fluxes from Soil of N 2 O and N 2 in the Field Using the 15 N-Gas “Nonequilibrium” Technique
journal, November 2001
- Bergsma, Timothy T.; Ostrom, Nathaniel E.; Emmons, Matt
- Environmental Science & Technology, Vol. 35, Issue 21
Nitrogen fixation by intact grass-soil cores using 15N2 and acetylene reduction
journal, January 1985
- Morris, D. R.; Zuberer, D. A.; Weaver, R. W.
- Soil Biology and Biochemistry, Vol. 17, Issue 1
Recent advances in BNF with non-legume plants
journal, May 1997
- Baldani, JoséI.; Caruso, Leonardo; Baldani, Vera L. D.
- Soil Biology and Biochemistry, Vol. 29, Issue 5-6
Diversity of Nitrogen-Fixing Bacteria Associated with Switchgrass in the Native Tallgrass Prairie of Northern Oklahoma
journal, July 2014
- Bahulikar, Rahul A.; Torres-Jerez, Ivone; Worley, Eric
- Applied and Environmental Microbiology, Vol. 80, Issue 18
Evidence from field nitrogen balance and 15N natural abundance data for the contribution of biological N2 fixation to Brazilian sugarcane varieties
journal, October 2011
- Urquiaga, Segundo; Xavier, Rogério P.; de Morais, Rafael F.
- Plant and Soil, Vol. 356, Issue 1-2
Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA
journal, March 2016
- Liang, Chao; Jesus, Ederson da C.; Duncan, David S.
- Soil Biology and Biochemistry, Vol. 94
Nitrogenase activity associated with some wisconsin prairie grasses
journal, August 1976
- Tjepkema, J. D.; Burris, R. H.
- Plant and Soil, Vol. 45, Issue 1
Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer
journal, February 2016
- Moyes, Andrew B.; Kueppers, Lara M.; Pett-Ridge, Jennifer
- New Phytologist, Vol. 210, Issue 2
Soil Carbon and Nitrogen Responses to Nitrogen Fertilizer and Harvesting Rates in Switchgrass Cropping Systems
journal, January 2017
- Valdez, Zachary P.; Hockaday, William C.; Masiello, Caroline A.
- BioEnergy Research, Vol. 10, Issue 2
The Biology and Agronomy of Switchgrass for Biofuels
journal, September 2005
- Parrish, David J.; Fike, John H.
- Critical Reviews in Plant Sciences, Vol. 24, Issue 5-6
Nitrogen-fixing bacteria of the genusBeijerinckia Derx in the rhizosphere of sugar cane
journal, November 1961
- Dobereiner, Johanna
- Plant and Soil, Vol. 15, Issue 3