Associative nitrogen fixation linked with three perennial bioenergy grasses in field and greenhouse experiments

Wewalwela, Jayani J.; Tian, Yuan; Donaldson, Janet R.; Baldwin, Brian S.; Varco, Jac J.; Rushing, Brett; Lu, Haoliang; Williams, Mark A.

doi:10.1111/gcbb.12744

Associative nitrogen fixation linked with three perennial bioenergy grasses in field and greenhouse experiments

Journal Article · Mon Oct 19 00:00:00 EDT 2020 · Global Change Biology. Bioenergy

DOI:https://doi.org/10.1111/gcbb.12744· OSTI ID:1678757

^[1]; Tian, Yuan ^[2]; Donaldson, Janet R. ^[3]; Baldwin, Brian S. ^[4]; ^[4]; Rushing, Brett ^[4]; Lu, Haoliang ^[5]; ^[6]

Department of Biological Sciences Mississippi State University Mississippi MS USA, Department of Agricultural Technology Faculty of Technology University of Colombo Colombo Sri Lanka
Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems College of the Environment and Ecology Xiamen University Xiamen Fujian China
School of Biological, Environmental, and Earth Sciences University of Southern Mississippi Hattiesburg MS USA
Department of Plant and Soil Sciences Mississippi State University Mississippi MS USA
Fujian Key Laboratory of Coastal Pollution Prevention and Control College of the Environment and Ecology Xiamen University Xiamen Fujian China
Rhizosphere‐Soil Microbial Ecology and Biogeochemistry School of Plant and Environmental Sciences Virginia Polytechnic and State University Blacksburg VA USA

Abstract

Associative nitrogen (N ₂ )‐fixation (ANF) by bacteria in the root‐zone of perennial bioenergy grasses has the potential to replace or supplement N fertilizer and support sustainable production of biomass, but its application in marginal ecosystems requires further evaluation. In this study, we first combined both greenhouse and field experiments, to explore the N ₂ fixation effects of three temperate feedstocks Miscanthus × giganteus (giant miscanthus, Freedom), Panicum virgatum (switchgrass, Alamo), and Saccharum sp. (energycane, Ho 02‐147). In field studies across three growing seasons, plant and soil pools of candidate feedstocks were partially composed of N derived from the atmosphere (Ndfa). Energycane, giant miscanthus, and switchgrass were estimated to derive >30%, %Ndfa. Greenhouse studies were also performed to trace isotopically labeled ¹⁵ N ₂ into plant biomass and soil pools. Evidence for Ndfa was detected in all three feedstock grasses (using reference ¹⁵ N of soil, chicory, and sorghum, δ ¹⁵ N~+7.0). Isotopically labeled ¹⁵ N ₂ was traced into biomass (during grass elongation stage) and soil pools. Extrapolation of rates during the 24 hr labeling period to 50 days estimated 30%–55% of plant Ndfa, with the greatest Ndfa for energycane. The findings of the field natural abundance and greenhouse ¹⁵ N ₂ feeding experiments provided complementary evidence that perennial bioenergy grasses have the potential to support relatively high rates of ANF, and accumulate diazotroph‐derived N into biomass when grown on non‐fertilized soil.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: FG36-06GO86025

OSTI ID:: 1678757

Alternate ID(s):: OSTI ID: 1850243
OSTI ID: 1787062

Journal Information:: Global Change Biology. Bioenergy, Journal Name: Global Change Biology. Bioenergy Journal Issue: 12 Vol. 12; ISSN 1757-1693

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (60)

Biological nitrogen fixation associated with sugar cane and rice: Contributions and prospects for improvement Boddey, R. M.; de Oliveira, O. C.; Urquiaga, S. Plant and Soil, Vol. 174, Issue 1-2 https://doi.org/10.1007/BF00032247	journal	July 1995
Nitrogen fixation associated with grasses and cereals: Recent progress and perspectives for the future Boddey, Robert M.; Dobereiner, Johanna Fertilizer Research, Vol. 42, Issue 1-3 https://doi.org/10.1007/BF00750518	journal	January 1995
Non-symbiotic nitrogen fixation in soil Delwiche, C. C.; Wijler, J. Plant and Soil, Vol. 7, Issue 2 https://doi.org/10.1007/BF01343722	journal	January 1956
Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth Wei, Chun-Yan; Lin, Li; Luo, Li-Jing Biology and Fertility of Soils, Vol. 50, Issue 4 https://doi.org/10.1007/s00374-013-0878-3	journal	November 2013
Foliar δ15N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient Kahmen, Ansgar; Wanek, Wolfgang; Buchmann, Nina Oecologia, Vol. 156, Issue 4 https://doi.org/10.1007/s00442-008-1028-8	journal	April 2008
Two Invasive Plants Alter Soil Microbial Community Composition in Serpentine Grasslands Batten, Katharine M.; Scow, Kate M.; Davies, Kendi F. Biological Invasions, Vol. 8, Issue 2 https://doi.org/10.1007/s10530-004-3856-8	journal	March 2006
The invasive Sorghum halepense harbors endophytic N2-fixing bacteria and alters soil biogeochemistry Rout, Marnie E.; Chrzanowski, Thomas H. Plant and Soil, Vol. 315, Issue 1-2 https://doi.org/10.1007/s11104-008-9740-z	journal	August 2008
Prospects and problems of simple linear models for estimating symbiotic N2 fixation by crop and pasture legumes Unkovich, M. J.; Baldock, J.; Peoples, M. B. Plant and Soil, Vol. 329, Issue 1-2 https://doi.org/10.1007/s11104-009-0136-5	journal	August 2009
Evidence from field nitrogen balance and 15N natural abundance data for the contribution of biological N2 fixation to Brazilian sugarcane varieties Urquiaga, Segundo; Xavier, Rogério P.; de Morais, Rafael F. Plant and Soil, Vol. 356, Issue 1-2 https://doi.org/10.1007/s11104-011-1016-3	journal	October 2011
Genetic diversity and plant growth promoting traits of diazotrophic bacteria isolated from two Pennisetum purpureum Schum. genotypes grown in the field Videira, Sandy Sampaio; de Oliveira, Danilo Messias; de Morais, Rafael Fiusa Plant and Soil, Vol. 356, Issue 1-2 https://doi.org/10.1007/s11104-011-1082-6	journal	December 2011
Nitrogen contributions from faba bean (Vicia faba L.) reliant on soil rhizobia or inoculation Denton, Matthew D.; Pearce, David J.; Peoples, Mark B. Plant and Soil, Vol. 365, Issue 1-2 https://doi.org/10.1007/s11104-012-1393-2	journal	August 2012
N2 fixation, N transfer, and yield in grassland communities including a deep-rooted legume or non-legume species Frankow-Lindberg, B. E.; Dahlin, A. S. Plant and Soil, Vol. 370, Issue 1-2 https://doi.org/10.1007/s11104-013-1650-z	journal	March 2013
Appraisal of 15N enrichment and 15N natural abundance methods for estimating N2 fixation by understorey Acacia leiocalyx and A. disparimma in a native forest of subtropical Australia Hosseini Bai, Shahla; Sun, Fangfang; Xu, Zhihong Journal of Soils and Sediments, Vol. 12, Issue 5 https://doi.org/10.1007/s11368-012-0492-2	journal	March 2012
Development and status of dedicated energy crops in the United States Jessup, Russell W. In Vitro Cellular & Developmental Biology - Plant, Vol. 45, Issue 3 https://doi.org/10.1007/s11627-009-9221-y	journal	June 2009
Nitrogen-Use Dynamics in Switchgrass Grown for Biomass Lemus, Rocky; Parrish, David J.; Abaye, Ozzie BioEnergy Research, Vol. 1, Issue 2 https://doi.org/10.1007/s12155-008-9014-x	journal	June 2008
N2-fixing trees and the transfer of fixed-N for sustainable agroforestry: a review Munroe, Jake W.; Isaac, Marney E. Agronomy for Sustainable Development, Vol. 34, Issue 2 https://doi.org/10.1007/s13593-013-0190-5	journal	November 2013
Nitrogen fixation by intact grass-soil cores using 15N2 and acetylene reduction Morris, D. R.; Zuberer, D. A.; Weaver, R. W. Soil Biology and Biochemistry, Vol. 17, Issue 1 https://doi.org/10.1016/0038-0717(85)90094-X	journal	January 1985
The root system of a grain sorghum crop Myers, R. J. K. Field Crops Research, Vol. 3 https://doi.org/10.1016/0378-4290(80)90007-6	journal	January 1980
The contribution of biological nitrogen fixation for sustainable agricultural systems in the tropics Boddey, Robert M.; De Moraes Sá, João Carlos; Alves, Bruno J. R. Soil Biology and Biochemistry, Vol. 29, Issue 5-6 https://doi.org/10.1016/S0038-0717(96)00221-0	journal	May 1997
Quantification of the contribution of biological nitrogen fixation to tropical green manure crops and the residual benefit to a subsequent maize crop using 15N-isotope techniques Ramos, M. Journal of Biotechnology, Vol. 91, Issue 2-3 https://doi.org/10.1016/S0168-1656(01)00335-2	journal	October 2001
δ15N as an integrator of the nitrogen cycle Robinson, David Trends in Ecology & Evolution, Vol. 16, Issue 3 https://doi.org/10.1016/S0169-5347(00)02098-X	journal	March 2001
Intra-annual changes in biomass, carbon, and nitrogen dynamics at 4-year old switchgrass field trials in west Tennessee, USA☆ Garten Jr., C. T.; Smith, J. L.; Tyler, D. D. Agriculture, Ecosystems & Environment, Vol. 136, Issue 1-2 https://doi.org/10.1016/j.agee.2009.12.019	journal	February 2010
Temporal variation of diazotrophic community abundance and structure in surface and subsoil under four fertilization regimes during a wheat growing season Wang, Jichen; Zhang, Dan; Zhang, Li Agriculture, Ecosystems & Environment, Vol. 216 https://doi.org/10.1016/j.agee.2015.09.039	journal	January 2016
Molecular detection and quantification of nifH gene sequences in the rhizosphere of sorghum (Sorghum bicolor) sown with two levels of nitrogen fertilizer Coelho, Marcia R. R.; Marriel, Ivanildo E.; Jenkins, Sasha N. Applied Soil Ecology, Vol. 42, Issue 1 https://doi.org/10.1016/j.apsoil.2009.01.010	journal	May 2009
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 Baptista, Rafael Butke; de Morais, Rafael Fiusa; Leite, José Marcos Applied Soil Ecology, Vol. 73 https://doi.org/10.1016/j.apsoil.2013.08.008	journal	January 2014
Rooting and growth of pre-germinated sugarcane seedlings inoculated with diazotrophic bacteria dos Santos, Silvana Gomes; Chaves, Valfredo Almeida; da Silva Ribeiro, Flaviane Applied Soil Ecology, Vol. 133 https://doi.org/10.1016/j.apsoil.2018.08.015	journal	January 2019
The solubility of neon, nitrogen and argon in distilled water and seawater Hamme, Roberta C.; Emerson, Steven R. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 51, Issue 11 https://doi.org/10.1016/j.dsr.2004.06.009	journal	November 2004
Natural 15N abundances in a tallgrass prairie ecosystem exposed to 8-y of elevated atmospheric CO2 Williams, Mark A.; Rice, Charles W.; Owensby, Clenton E. Soil Biology and Biochemistry, Vol. 38, Issue 2 https://doi.org/10.1016/j.soilbio.2005.06.009	journal	February 2006
Methodologies for estimating nitrogen transfer between legumes and companion species in agro-ecosystems: A review of 15N-enriched techniques Chalk, Phillip M.; Peoples, Mark B.; McNeill, Ann M. Soil Biology and Biochemistry, Vol. 73 https://doi.org/10.1016/j.soilbio.2014.02.005	journal	June 2014
The nitrogen cycle: A review of isotope effects and isotope modeling approaches Denk, Tobias R. A.; Mohn, Joachim; Decock, Charlotte Soil Biology and Biochemistry, Vol. 105 https://doi.org/10.1016/j.soilbio.2016.11.015	journal	February 2017
Nitrogen acquisition strategies during the winter-spring transitional period are divergent at the species level yet convergent at the ecosystem level in temperate grasslands Ma, Linna; Liu, Guofang; Xu, Xiaofeng Soil Biology and Biochemistry, Vol. 122 https://doi.org/10.1016/j.soilbio.2018.04.020	journal	July 2018
Temporal fate of 15N and 14C leaf-fed to red and white clover in pure stand or mixture with grass – Implications for estimation of legume derived N in soil and companion species Rasmussen, Jim; Gylfadóttir, Thórey; Dhalama, Nawa Raj Soil Biology and Biochemistry, Vol. 133 https://doi.org/10.1016/j.soilbio.2019.02.011	journal	June 2019
Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome de Souza, Rafael Soares Correa; Okura, Vagner Katsumi; Armanhi, Jaderson Silveira Leite Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28774	journal	June 2016
Tansley Review No. 95. 15N natural abundance in soil-plant systems Hogberg, Peter New Phytologist, Vol. 137, Issue 2 https://doi.org/10.1046/j.1469-8137.1997.00808.x	journal	October 1997
On the relationship between C and N fixation and amino acid synthesis in nodulated alfalfa (Medicago sativa) Molero, Gemma; Tcherkez, Guillaume; Araus, Jose Luis Functional Plant Biology, Vol. 41, Issue 4 https://doi.org/10.1071/FP13189	journal	January 2014
Associative N ₂ -fixation in pearl millet and sorghum: Levels and response to inoculation Lee, Keuk-Ki; Wani, Suhas Pralhad; Yoneyama, Tadakatsu Soil Science and Plant Nutrition, Vol. 40, Issue 3 https://doi.org/10.1080/00380768.1994.10413325	journal	September 1994
Methods for quantification of nitrogen fixation associated with gramineae Boddey, Robert M.; Knowles, Roger Critical Reviews in Plant Sciences, Vol. 6, Issue 3 https://doi.org/10.1080/07352688709382251	journal	January 1987
Biological Nitrogen Fixation in Sugar Cane: A Key to Energetically Viable Biofuel Production Boddey, R. M. Critical Reviews in Plant Sciences, Vol. 14, Issue 3 https://doi.org/10.1080/713608118	journal	January 1995
Invasion of non-native grasses causes a drop in soil carbon storage in California grasslands Koteen, Laura E.; Baldocchi, Dennis D.; Harte, John Environmental Research Letters, Vol. 6, Issue 4 https://doi.org/10.1088/1748-9326/6/4/044001	journal	October 2011
Contribution of nitrogen fixation to first year Miscanthus × giganteus Keymer, Daniel P.; Kent, Angela D. GCB Bioenergy, Vol. 6, Issue 5 https://doi.org/10.1111/gcbb.12095	journal	July 2013
Morphological and physiological traits for higher biomass production in perennial rhizomatous grasses grown on marginal land Jones, Michael B.; Finnan, John; Hodkinson, Trevor R. GCB Bioenergy, Vol. 7, Issue 2 https://doi.org/10.1111/gcbb.12203	journal	June 2014
Plant and soil effects on bacterial communities associated with Miscanthus × giganteus rhizosphere and rhizomes Li, Dongfang; Voigt, Thomas B.; Kent, Angela D. GCB Bioenergy, Vol. 8, Issue 1 https://doi.org/10.1111/gcbb.12252	journal	April 2015
Perennial species mixtures for multifunctional production of biomass on marginal land Carlsson, Georg; Mårtensson, Linda-Maria; Prade, Thomas GCB Bioenergy, Vol. 9, Issue 1 https://doi.org/10.1111/gcbb.12373	journal	June 2016
Microbial communities and diazotrophic activity differ in the root-zone of Alamo and Dacotah switchgrass feedstocks Rodrigues, Richard R.; Moon, Jinyoung; Zhao, Bingyu GCB Bioenergy, Vol. 9, Issue 6 https://doi.org/10.1111/gcbb.12396	journal	August 2016
Biomass production of herbaceous energy crops in the United States: field trial results and yield potential maps from the multiyear regional feedstock partnership Lee, Do Kyoung; Aberle, Ezra; Anderson, Eric K. GCB Bioenergy, Vol. 10, Issue 10 https://doi.org/10.1111/gcbb.12493	journal	January 2018
Nitrogen‐dependent bacterial community shifts in root, rhizome and rhizosphere of nutrient‐efficient Miscanthus x giganteus from long‐term field trials Liu, Yuan; Ludewig, Uwe GCB Bioenergy, Vol. 11, Issue 11 https://doi.org/10.1111/gcbb.12634	journal	June 2019
Application of n15 to the Study of Biological Nitrogen Fixation Burris, R. H.; Miller, C. E. Science, Vol. 93, Issue 2405 https://doi.org/10.1126/science.93.2405.114	journal	January 1941
Stable Isotope Probing with 15N2 Reveals Novel Noncultivated Diazotrophs in Soil Buckley, D. H.; Huangyutitham, V.; Hsu, S. -F. Applied and Environmental Microbiology, Vol. 73, Issue 10 https://doi.org/10.1128/AEM.02610-06	journal	March 2007
Fixation of Dinitrogen-15 Associated with Rice Plants Ito, Osamu; Cabrera, Delfin; Watanabe, Iwao Applied and Environmental Microbiology, Vol. 39, Issue 3 https://doi.org/10.1128/AEM.39.3.554-558.1980	journal	January 1980
Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota Van Deynze, Allen; Zamora, Pablo; Delaux, Pierre-Marc PLOS Biology, Vol. 16, Issue 8 https://doi.org/10.1371/journal.pbio.2006352	journal	August 2018
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
Describing and Quantifying Growth Stages of Perennial Forage Grasses Moore, K. J.; Moser, L. E.; Vogel, K. P. Agronomy Journal, Vol. 83, Issue 6 https://doi.org/10.2134/agronj1991.00021962008300060027x	journal	January 1991
Biomass and Carbon Partitioning in Switchgrass Frank, A. B.; Berdahl, J. D.; Hanson, J. D. Crop Science, Vol. 44, Issue 4 https://doi.org/10.2135/cropsci2004.1391	journal	January 2004
Evaluation of Sugarcane × Progeny for Biomass Composition and Yield Components Wang, Li-Ping; Jackson, Phillip A.; Lu, Xin Crop Science, Vol. 48, Issue 3 https://doi.org/10.2135/cropsci2007.10.0555	journal	January 2008
Growing Dedicated Energy Crops on Marginal Lands and Ecosystem Services Blanco-Canqui, Humberto Soil Science Society of America Journal, Vol. 80, Issue 4 https://doi.org/10.2136/sssaj2016.03.0080	journal	January 2016
Restranslocation of Shoot Nitrogen to Rhizomes and Roots in Prairie Grasses May Limit Loss of N to Grazing and Fire during Drought Heckathorn, S. A.; Delucia, E. H. Functional Ecology, Vol. 10, Issue 3 https://doi.org/10.2307/2390289	journal	June 1996
Switchgrass Growth and Development: Water, Nitrogen, and Plant Density Effects Sanderson, M. A.; Reed, R. L. Journal of Range Management, Vol. 53, Issue 2 https://doi.org/10.2307/4003287	journal	March 2000
Bioenergy from “surplus” land: environmental and socio-economic implications Dauber, Jens; Brown, Chris; Fernando, Ana Luisa BioRisk, Vol. 7 https://doi.org/10.3897/biorisk.7.3036	journal	October 2012
Assessment of impacts of agricultural and climate change scenarios on watershed water quantity and quality, and crop production Teshager, Awoke D.; Gassman, Philip W.; Schoof, Justin T. Hydrology and Earth System Sciences, Vol. 20, Issue 8 https://doi.org/10.5194/hess-20-3325-2016	journal	January 2016

Associative nitrogen fixation linked with three perennial bioenergy grasses in field and greenhouse experiments

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Associative nitrogen fixation linked with three perennial bioenergy grasses in field and greenhouse experiments

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