Soil mycorrhizal and nematode diversity vary in response to bioenergy crop identity and fertilization

Emery, Sarah M.; Reid, Matthew L.; Bell-Dereske, Lukas; Gross, Katherine L.

doi:10.1111/gcbb.12460

Title: Soil mycorrhizal and nematode diversity vary in response to bioenergy crop identity and fertilization

Journal Article · Tue Jun 20 00:00:00 EDT 2017 · Global Change Biology. Bioenergy

DOI:https://doi.org/10.1111/gcbb.12460· OSTI ID:1364458

^[1]; Reid, Matthew L. ^[1]; Bell-Dereske, Lukas ^[2]; Gross, Katherine L. ^[3]

University of Louisville, Louisville KY USA
University of New Mexico, Albuquerque NM USA
W.K. Kellogg Biological Station, Hickory Corners MI USA

Abstract The mandate by the Energy Independence and Security Act of 2007 to increase renewable fuel production in the USA has resulted in extensive research into the sustainability of perennial bioenergy crops such as switchgrass ( Panicum virgatum ) and miscanthus ( Miscanthus× giganteus ). Perennial grassland crops have been shown to support greater aboveground biodiversity and ecosystem function than annual crops. However, management considerations, such as what crop to plant or whether to use fertilizer, may alter belowground diversity and ecosystem functioning associated with these grasslands as well. In this study, we compared crop type (switchgrass or miscanthus) and nitrogen fertilization effects on arbuscular mycorrhizal fungal ( AMF ) and soil nematode abundance, activity, and diversity in a long‐term experiment. We quantified AMF root colonization, AMF extra‐radical hyphal length, soil glomalin concentrations, AMF richness and diversity, plant‐parasitic nematode abundance, and nematode family richness and diversity in each treatment. Mycorrhizal activity and diversity were higher with switchgrass than with miscanthus, leading to higher potential soil carbon contributions via increased hyphal growth and glomalin production. Plant‐parasitic nematode ( PPN ) abundance was 2.3 × higher in miscanthus plots compared to switchgrass, mostly due to increases in dagger nematodes ( Xiphinema) . The higher PPN abundance in miscanthus may be a consequence of lower AMF in this species, as AMF can provide protection against PPN through a variety of mechanisms. Nitrogen fertilization had minor negative effects on AMF and nematode diversity associated with these crops. Overall, we found that crop type and fertilizer application associated with perennial bioenergy cropping systems can have detectable effects on the diversity and composition of soil communities, which may have important consequences for the ecosystem services provided by these systems.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE)

Grant/Contract Number:: ACO5-76RL01830; FC02-07ER64494; DEB 1637653; 2015-67020-23184

OSTI ID:: 1364458

Alternate ID(s):: OSTI ID: 1364459

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

Publisher:: WileyCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 25 works

Citation information provided by
Web of Science

References (69)

Agroenergy Crops Influence the Diversity, Biomass, and Guild Structure of Terrestrial Arthropod Communities Robertson, Bruce A.; Porter, Cody; Landis, Douglas A. BioEnergy Research, Vol. 5, Issue 1 https://doi.org/10.1007/s12155-011-9161-3	journal	November 2011
Spatial scaling of arbuscular mycorrhizal fungal diversity is affected by farming practice: Spatial scaling of arbuscular mycorrhizal fungi van der Gast, Christopher J.; Gosling, Paul; Tiwari, Bela Environmental Microbiology, Vol. 13, Issue 1 https://doi.org/10.1111/j.1462-2920.2010.02326.x	journal	September 2010
Ecology of Plant and Free-Living Nematodes in Natural and Agricultural Soil Neher, Deborah A. Annual Review of Phytopathology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev-phyto-073009-114439	journal	July 2010
Distribution, morphological description, and molecular characterization of Xiphinema and Longidorous spp. associated with plants ( Miscanthus spp. and Panicum virgatum ) used for biofuels Mekete, Tesfamariam; Gray, Michael E.; Niblack, Terry L. GCB Bioenergy, Vol. 1, Issue 4 https://doi.org/10.1111/j.1757-1707.2009.01020.x	journal	August 2009
Behavior of Bradford-reactive substances is consistent with predictions for glomalin Koide, Roger T.; Peoples, Matthew S. Applied Soil Ecology, Vol. 63 https://doi.org/10.1016/j.apsoil.2012.09.015	journal	January 2013
A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies Treseder, Kathleen K. New Phytologist, Vol. 164, Issue 2 https://doi.org/10.1111/j.1469-8137.2004.01159.x	journal	July 2004
A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY Anderson, Marti J. Austral Ecology, Vol. 26, Issue 1 https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x	journal	February 2001
Arbuscular mycorrhizal fungi and organic farming Gosling, P.; Hodge, A.; Goodlass, G. Agriculture, Ecosystems & Environment, Vol. 113, Issue 1-4 https://doi.org/10.1016/j.agee.2005.09.009	journal	April 2006
Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible McMurdie, Paul J.; Holmes, Susan PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003531	journal	April 2014
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
The Ethanol Decade: An Expansion of U.S. Corn Production, 2000-09 Wallander, Steve; Claassen, Roger; Nickerson, Cynthia SSRN Electronic Journal https://doi.org/10.2139/ssrn.2131399	journal	January 2011
Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration Cornejo, Pablo; Meier, Sebastián; Borie, Gilda Science of The Total Environment, Vol. 406, Issue 1-2 https://doi.org/10.1016/j.scitotenv.2008.07.045	journal	November 2008
Seasonality of arbuscular mycorrhizal hyphae and glomalin in a western Montana grassland Lutgen, Emily R.; Muir-Clairmont, Deborah; Graham, Jon Plant and Soil, Vol. 257, Issue 1 https://doi.org/10.1023/A:1026224209597	journal	November 2003
A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi McGONIGLE, T. P.; Miller, M. H.; Evans, D. G. New Phytologist, Vol. 115, Issue 3 https://doi.org/10.1111/j.1469-8137.1990.tb00476.x	journal	July 1990
Comparative water use by maize, perennial crops, restored prairie, and poplar trees in the US Midwest Hamilton, S. K.; Hussain, M. Z.; Bhardwaj, A. K. Environmental Research Letters, Vol. 10, Issue 6 https://doi.org/10.1088/1748-9326/10/6/064015	journal	June 2015
Transmission of Viruses by Plant Nematodes Brown, D. J. F.; Robertson, W. M.; Trudgill, D. L. Annual Review of Phytopathology, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.py.33.090195.001255	journal	September 1995
Nitrogen Fertilization Effects on Productivity and Nitrogen Loss in Three Grass-Based Perennial Bioenergy Cropping Systems Duran, Brianna E. L.; Duncan, David S.; Oates, Lawrence G. PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0151919	journal	March 2016
Yields of Miscanthus × giganteus and Panicum virgatum decline with stand age in the Midwestern USA Arundale, Rebecca A.; Dohleman, Frank G.; Heaton, Emily A. GCB Bioenergy, Vol. 6, Issue 1 https://doi.org/10.1111/gcbb.12077	journal	September 2013
Nitrogen enrichment causes minimal changes in arbuscular mycorrhizal colonization but shifts community composition?evidence from rDNA data Jumpponen, Ari; Trowbridge, Justin; Mandyam, Keerthi Biology and Fertility of Soils, Vol. 41, Issue 4 https://doi.org/10.1007/s00374-005-0845-8	journal	March 2005
Fungal symbionts alter plant responses to global change Kivlin, Stephanie N.; Emery, Sarah M.; Rudgers, Jennifer A. American Journal of Botany, Vol. 100, Issue 7 https://doi.org/10.3732/ajb.1200558	journal	July 2013
Ribosomal Database Project: data and tools for high throughput rRNA analysis Cole, James R.; Wang, Qiong; Fish, Jordan A. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1244	journal	November 2013
Nematodes as soil indicators: functional and biodiversity aspects Yeates, Gregor W. Biology and Fertility of Soils, Vol. 37, Issue 4 https://doi.org/10.1007/s00374-003-0586-5	journal	February 2003
Carbon-rich organic fertilizers to increase soil biodiversity: Evidence from a meta-analysis of nematode communities Liu, Ting; Chen, Xiaoyun; Hu, Feng Agriculture, Ecosystems & Environment, Vol. 232 https://doi.org/10.1016/j.agee.2016.07.015	journal	September 2016
The ecology and agronomy of Miscanthus sinensis , a species important to bioenergy crop development, in its native range in Japan: a review Stewart, J. Ryan; Toma, Yo; FernÁNdez, FabiÁN G. GCB Bioenergy, Vol. 1, Issue 2 https://doi.org/10.1111/j.1757-1707.2009.01010.x	journal	April 2009
Bioenergy cropping systems that incorporate native grasses stimulate growth of plant-associated soil microbes in the absence of nitrogen fertilization Oates, Lawrence G.; Duncan, David S.; Sanford, Gregg R. Agriculture, Ecosystems & Environment, Vol. 233 https://doi.org/10.1016/j.agee.2016.09.008	journal	October 2016
Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes Werling, B. P.; Dickson, T. L.; Isaacs, R. Proceedings of the National Academy of Sciences, Vol. 111, Issue 4 https://doi.org/10.1073/pnas.1309492111	journal	January 2014
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
Form of inorganic nitrogen influences mycorrhizal colonisation and photosynthesis of cucumber Valentine, A. J.; Osborne, B. A.; Mitchell, D. T. Scientia Horticulturae, Vol. 92, Issue 3-4 https://doi.org/10.1016/S0304-4238(01)00302-8	journal	February 2002
Glomalin extraction and measurement Janos, David P.; Garamszegi, Sara; Beltran, Bray Soil Biology and Biochemistry, Vol. 40, Issue 3 https://doi.org/10.1016/j.soilbio.2007.10.007	journal	March 2008
Plant-Parasitic Nematodes Are Potential Pathogens of Miscanthus × giganteus and Panicum virgatum Used for Biofuels Mekete, Tesfamariam; Reynolds, Kimberly; Lopez-Nicora, Horacio D. Plant Disease, Vol. 95, Issue 4 https://doi.org/10.1094/PDIS-05-10-0335	journal	April 2011
A trait-based framework to understand life history of mycorrhizal fungi Chagnon, Pierre-Luc; Bradley, Robert L.; Maherali, Hafiz Trends in Plant Science, Vol. 18, Issue 9 https://doi.org/10.1016/j.tplants.2013.05.001	journal	September 2013
Ink and Vinegar, a Simple Staining Technique for Arbuscular-Mycorrhizal Fungi Vierheilig, Horst; Coughlan, Andrew P.; Wyss, Urs Applied and Environmental Microbiology, Vol. 64, Issue 12 https://doi.org/10.1128/AEM.64.12.5004-5007.1998	journal	January 1998
Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie Wilson, Gail W. T.; Hartnett, David C. American Journal of Botany, Vol. 85, Issue 12 https://doi.org/10.2307/2446507	journal	December 1998
Arbuscular Mycorrhizal Fungi for the Biocontrol of Plant-Parasitic Nematodes: A Review of the Mechanisms Involved Schouteden, Nele; De Waele, Dirk; Panis, Bart Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01280	journal	November 2015
Response of switchgrass yield to future climate change Tulbure, Mirela G.; Wimberly, Michael C.; Owens, Vance N. Environmental Research Letters, Vol. 7, Issue 4 https://doi.org/10.1088/1748-9326/7/4/045903	journal	November 2012
Extraction of an Abundant and Unusual Protein from soil and Comparison with Hyphal Protein of Arbuscular Mycorrhizal Fungi Wright, Sara F.; Upadhyaya, Abha Soil Science, Vol. 161, Issue 9 https://doi.org/10.1097/00010694-199609000-00003	journal	January 1996
Effect of elevated atmospheric CO2 on mycorrhizal colonization, external mycorrhizal hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal fungus Glomus mosseae Staddon, Philip L.; Fitter, Alastair H.; Graves, Jonathan D. Global Change Biology, Vol. 5, Issue 3 https://doi.org/10.1046/j.1365-2486.1999.00230.x	journal	March 1999
Biochar in bioenergy cropping systems: impacts on soil faunal communities and linked ecosystem processes McCormack, Sarah A.; Ostle, Nick; Bardgett, Richard D. GCB Bioenergy, Vol. 5, Issue 2 https://doi.org/10.1111/gcbb.12046	journal	January 2013
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
Glomalin in Ecosystems Treseder, Kathleen K.; Turner, Katie M. Soil Science Society of America Journal, Vol. 71, Issue 4 https://doi.org/10.2136/sssaj2006.0377	journal	January 2007
Nitrogen Fertilization Does Significantly Increase Yields of Stands of Miscanthus × giganteus and Panicum virgatum in Multiyear Trials in Illinois Arundale, Rebecca A.; Dohleman, Frank G.; Voigt, Thomas B. BioEnergy Research, Vol. 7, Issue 1 https://doi.org/10.1007/s12155-013-9385-5	journal	October 2013
Mechanisms of soil carbon accrual and storage in bioenergy cropping systems Tiemann, Lisa K.; Grandy, A. Stuart GCB Bioenergy, Vol. 7, Issue 2 https://doi.org/10.1111/gcbb.12126	journal	March 2014
UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing Edgar, Robert C. BioRxiv https://doi.org/10.1101/081257	posted_content	October 2016
Enrichment of specific bacterial and eukaryotic microbes in the rhizosphere of switchgrass ( P anicum virgatum L.) through root exudates : Root exudate-utilizing microbes in switchgrass rhizosphere Mao, Yuejian; Li, Xiangzhen; Smyth, Eoghan M. Environmental Microbiology Reports, Vol. 6, Issue 3 https://doi.org/10.1111/1758-2229.12152	journal	March 2014
Nitrogen fertilization challenges the climate benefit of cellulosic biofuels Ruan, Leilei; Bhardwaj, Ajay K.; Hamilton, Stephen K. Environmental Research Letters, Vol. 11, Issue 6 https://doi.org/10.1088/1748-9326/11/6/064007	journal	June 2016
Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity Eisenhauer, Nico; Cesarz, Simone; Koller, Robert Global Change Biology, Vol. 18, Issue 2 https://doi.org/10.1111/j.1365-2486.2011.02555.x	journal	October 2011
NINJA: An automated calculation system for nematode-based biological monitoring Sieriebriennikov, Bogdan; Ferris, Howard; de Goede, Ron G. M. European Journal of Soil Biology, Vol. 61 https://doi.org/10.1016/j.ejsobi.2014.02.004	journal	March 2014
Linking soil biodiversity and agricultural soil management Thiele-Bruhn, Sören; Bloem, Jaap; de Vries, Franciska T. Current Opinion in Environmental Sustainability, Vol. 4, Issue 5 https://doi.org/10.1016/j.cosust.2012.06.004	journal	November 2012
A framework for soil food web diagnostics: extension of the nematode faunal analysis concept Ferris, H.; Bongers, T.; de Goede, R. G. M. Applied Soil Ecology, Vol. 18, Issue 1 https://doi.org/10.1016/S0929-1393(01)00152-4	journal	September 2001
Comparative productivity of alternative cellulosic bioenergy cropping systems in the North Central USA Sanford, Gregg R.; Oates, Lawrence G.; Jasrotia, Poonam Agriculture, Ecosystems & Environment, Vol. 216 https://doi.org/10.1016/j.agee.2015.10.018	journal	January 2016
A quantitative review comparing the yields of two candidate C4 perennial biomass crops in relation to nitrogen, temperature and water Heaton, E. Biomass and Bioenergy, Vol. 27, Issue 1 https://doi.org/10.1016/j.biombioe.2003.10.005	journal	July 2004
Nematode diversity in agroecosystems Yeates, G. W.; Bongers, T. Agriculture, Ecosystems & Environment, Vol. 74, Issue 1-3 https://doi.org/10.1016/S0167-8809(99)00033-X	journal	June 1999
Functioning of mycorrhizal associations along the mutualism-parasitism continuum Johnson, N. C.; Graham, J. H.; Smith, F. A. New Phytologist, Vol. 135, Issue 4 https://doi.org/10.1046/j.1469-8137.1997.00729.x	journal	April 1997
Long-term mineral fertilization impact on chemical and microbiological properties of soil and Miscanthus × giganteus yield [Long-term mineral fertilization impact on chemical and microbiological properties of soil and Miscanthus × giganteus yield] Stępień, W.; Eb, Górska; Pietkiewicz, S. Plant, Soil and Environment, Vol. 60, Issue No. 3 https://doi.org/10.17221/890/2013-PSE	journal	March 2014
Biodiversity of arbuscular mycorrhizal fungi in agroecosystems Douds, David D.; Millner, Patricia D. Agriculture, Ecosystems & Environment, Vol. 74, Issue 1-3 https://doi.org/10.1016/S0167-8809(99)00031-6	journal	June 1999
The biogeochemistry of bioenergy landscapes: carbon, nitrogen, and water considerations Robertson, G. Philip; Hamilton, Stephen K.; Del Grosso, Stephen J. Ecological Applications, Vol. 21, Issue 4 https://doi.org/10.1890/09-0456.1	journal	June 2011
Effects of tillage systems on soil characteristics, glomalin and mycorrhizal propagules in a Chilean Ultisol Borie, F.; Rubio, R.; Rouanet, J. L. Soil and Tillage Research, Vol. 88, Issue 1-2 https://doi.org/10.1016/j.still.2005.06.004	journal	July 2006
Yield, biomass composition, and N use efficiency during establishment of four Miscanthus × giganteus genotypes as influenced by N management Dierking, R. M.; Allen, D. J.; Brouder, S. M. Biomass and Bioenergy, Vol. 91 https://doi.org/10.1016/j.biombioe.2016.05.005	journal	August 2016
Sustainable bioenergy production from marginal lands in the US Midwest Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong Nature, Vol. 493, Issue 7433 https://doi.org/10.1038/nature11811	journal	January 2013
Comparative economic analysis of perennial, annual, and intercrops for biomass production Hallam, A.; Anderson, I. C.; Buxton, D. R. Biomass and Bioenergy, Vol. 21, Issue 6 https://doi.org/10.1016/S0961-9534(01)00051-4	journal	December 2001
Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie Eom, A. -H.; Hartnett, D. C.; Wilson, G. W. T. Oecologia, Vol. 122, Issue 3 https://doi.org/10.1007/s004420050050	journal	February 2000
Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment Gollotte, Armelle; van Tuinen, Diederik; Atkinson, David Mycorrhiza, Vol. 14, Issue 2 https://doi.org/10.1007/s00572-003-0244-7	journal	May 2003
A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi Hoeksema, Jason D.; Chaudhary, V. Bala; Gehring, Catherine A. Ecology Letters, Vol. 13, Issue 3 https://doi.org/10.1111/j.1461-0248.2009.01430.x	journal	March 2010
Nitrogen Enrichment Alters Mycorrhizal Allocation at five Mesic to Semiarid Grasslands Johnson, Nancy Collins; Rowland, Diane L.; Corkidi, Lea Ecology, Vol. 84, Issue 7 https://doi.org/10.1890/0012-9658(2003)084[1895:NEAMAA]2.0.CO;2	journal	July 2003
Bioenergy crop productivity and potential climate change mitigation from marginal lands in the United States: An ecosystem modeling perspective Qin, Zhangcai; Zhuang, Qianlai; Cai, Ximing GCB Bioenergy, Vol. 7, Issue 6 https://doi.org/10.1111/gcbb.12212	journal	July 2014
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
Shifts in Arbuscular Mycorrhizal Communities Along an Anthropogenic Nitrogen Deposition Gradient Egerton-Warburton, Louise M.; Allen, Edith B. Ecological Applications, Vol. 10, Issue 2 https://doi.org/10.1890/1051-0761(2000)010[0484:SIAMCA]2.0.CO;2	journal	April 2000
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
The Biology and Agronomy of Switchgrass for Biofuels Parrish, David J.; Fike, John H. Critical Reviews in Plant Sciences, Vol. 24, Issue 5-6 https://doi.org/10.1080/07352680500316433	journal	September 2005

Similar Records

Nitrogen Fertilizer, Arbuscular Mycorrhizal Fungi, and Soil Nematodes Affect Lignin Quality and Quantity in Switchgrass (Panicum virgatum L.)

Journal Article · Sat Apr 24 00:00:00 EDT 2021 · BioEnergy Research · OSTI ID:1364458

Basyal, Binod; Foster, Cliff; Gross, Katherine L.; +1 more

Influence of Bioenergy Crop Production and Climate Change on Ecosystem Services

Journal Article · Tue Oct 24 00:00:00 EDT 2017 · Journal of the American Water Resources Association · OSTI ID:1364458

Cibin, Raj; Chaubey, Indrajeet; Muenich, Rebecca L.; +4 more

Perennial biomass production from marginal land in the Upper Mississippi River Basin

Journal Article · Wed May 16 00:00:00 EDT 2018 · Land Degradation and Development · OSTI ID:1364458

Feng, Qingyu; Chaubey, Indrajeet; Cibin, Raj; +4 more

Title: Soil mycorrhizal and nematode diversity vary in response to bioenergy crop identity and fertilization

Citation Formats

References (69)

Similar Records

Related Subjects