Response of Total (DNA) and Metabolically Active (RNA) Microbial Communities in Miscanthus × Giganteus Cultivated Soil to Different Nitrogen Fertilization Rates

Yang, Jihoon; Lee, Jaejin; Choi, Jinlyung; Ma, Lanying; Heaton, Emily A.; Howe, Adina

doi:10.1128/spectrum.02116-21

Response of Total (DNA) and Metabolically Active (RNA) Microbial Communities in Miscanthus × Giganteus Cultivated Soil to Different Nitrogen Fertilization Rates

Journal Article · Wed Feb 16 00:00:00 EST 2022 · Microbiology Spectrum

DOI:https://doi.org/10.1128/spectrum.02116-21· OSTI ID:1860636

^[1]; Lee, Jaejin ^[2]; Choi, Jinlyung ^[3]; Ma, Lanying ^[4]; Heaton, Emily A. ^[5]; ^[2]

Iowa State Univ., Ames, IA (United States); Center for Advanced Bioenergy and Bioproducts Innovation, Urbana, IL (United States); CABBI
Iowa State Univ., Ames, IA (United States); Center for Advanced Bioenergy and Bioproducts Innovation, Urbana, IL (United States)
Iowa State Univ., Ames, IA (United States); Center for Advanced Bioenergy and Bioproducts Innovation, Urbana, IL (United States); Second Genome Inc., Brisbane, CA (United States)
Iowa State Univ., Ames, IA (United States); Center for Advanced Bioenergy and Bioproducts Innovation, Urbana, IL (United States); VastBiome Inc., Millbrae, CA (United States)
Center for Advanced Bioenergy and Bioproducts Innovation, Urbana, IL (United States); Iowa State Univ., Ames, IA (United States)

Miscanthus × giganteus is a promising high-yielding perennial plant to meet growing bioenergy demands; however, the degree to which the soil microbiome affects its nitrogen cycling and subsequently, biomass yield remains unclear. In this study, we hypothesize that contributions of metabolically active soil microbial membership may be underestimated with DNA-based approaches. We assessed the response of the soil microbiome to nitrogen availability in terms of both DNA and RNA soil microbial communities from the Long-term Assessment of Miscanthus Productivity and Sustainability (LAMPS) field trial. DNA and RNA were extracted from 271 samples, and 16S small subunit (SSU) rRNA amplicon sequencing was performed to characterize microbial community structure. Significant differences were observed in the resulting soil microbiomes and were best explained by the sequencing library of origin, either DNA or RNA. Similar numbers of membership were detected in DNA and RNA microbial communities, with more than 90% of membership shared. However, the profile of dominant membership within DNA and RNA differed, with varying proportions of Actinobacteria and Proteobacteria and Firmicutes and Proteobacteria. Only RNA microbial communities showed seasonal responses to nitrogen fertilization, and these differences were associated with nitrogen-cycling bacteria. The relative abundance of bacteria associated with nitrogen cycling was 7-fold higher in RNA than in DNA, and genes associated with denitrifying bacteria were significantly enriched in RNA, suggesting that these bacteria may be underestimated with DNA-only approaches. Our findings indicate that RNA-based SSU characterization can be a significant and complementing resource for understanding the role of soil microbiomes in bioenergy crop production.

View Accepted Manuscript (DOE)

Research Organization:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018420

OSTI ID:: 1860636

Journal Information:: Microbiology Spectrum, Journal Name: Microbiology Spectrum Journal Issue: 1 Vol. 10; ISSN 2165-0497

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Miscanthus : a fast-growing crop for biofuels and chemicals production : A fast-growing crop for biofuels and chemicals production Brosse, Nicolas; Dufour, Anthony; Meng, Xianzhi Biofuels, Bioproducts and Biorefining, Vol. 6, Issue 5 https://doi.org/10.1002/bbb.1353	journal	July 2012
Storage of environmental samples for guaranteeing nucleic acid yields for molecular microbiological studies Rissanen, Antti Juhani; Kurhela, Emilia; Aho, Tommi Applied Microbiology and Biotechnology, Vol. 88, Issue 4 https://doi.org/10.1007/s00253-010-2838-2	journal	August 2010
Patterns of diversity in plant and soil microbial communities along a productivity gradient in a Michigan old-field Broughton, L. C.; Gross, K. L. Oecologia, Vol. 125, Issue 3 https://doi.org/10.1007/s004420000456	journal	November 2000
Comparative Biogeochemical Cycles of Bioenergy Crops Reveal Nitrogen-Fixation and Low Greenhouse Gas Emissions in a Miscanthus × giganteus Agro-Ecosystem Davis, Sarah C.; Parton, William J.; Dohleman, Frank G. Ecosystems, Vol. 13, Issue 1 https://doi.org/10.1007/s10021-009-9306-9	journal	December 2009
Nitrogen fertilization of Miscanthus x giganteus: effects on nitrogen uptake, growth, yield and emissions from biomass combustion Finnan, J.; Burke, B. Nutrient Cycling in Agroecosystems, Vol. 106, Issue 2 https://doi.org/10.1007/s10705-016-9793-y	journal	August 2016
Quality and decomposition in soil of rhizome, root and senescent leaf from Miscanthus x giganteus, as affected by harvest date and N fertilization Amougou, Norbert; Bertrand, Isabelle; Machet, Jean-Marie Plant and Soil, Vol. 338, Issue 1-2 https://doi.org/10.1007/s11104-010-0443-x	journal	June 2010
Culture-independent molecular approaches reveal a mostly unknown high diversity of active nitrogen-fixing bacteria associated with Pennisetum purpureum—a bioenergy crop Videira, Sandy Sampaio; Pereira e. Silva, Michele de Cássia; de Souza Galisa, Péricles Plant and Soil, Vol. 373, Issue 1-2 https://doi.org/10.1007/s11104-013-1828-4	journal	July 2013
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
A Review on Miscanthus Biomass Production and Composition for Bioenergy Use: Genotypic and Environmental Variability and Implications for Breeding Arnoult, Stéphanie; Brancourt-Hulmel, Maryse BioEnergy Research, Vol. 8, Issue 2 https://doi.org/10.1007/s12155-014-9524-7	journal	September 2014
Yield and Nitrogen Removal of Bioenergy Grasses as Influenced by Nitrogen Rate and Harvest Management in the Coastal Plain Region of North Carolina Wang, Zan; Jot Smyth, T.; Crozier, Carl R. BioEnergy Research, Vol. 11, Issue 1 https://doi.org/10.1007/s12155-017-9876-x	journal	September 2017
Multi-year and Multi-site Establishment of the Perennial Biomass Crop Miscanthus × giganteus Using a Staggered Start Design to Elucidate N Response Tejera, Mauricio; Boersma, Nicholas; Vanloocke, Andy BioEnergy Research, Vol. 12, Issue 3 https://doi.org/10.1007/s12155-019-09985-6	journal	May 2019
The effect of fertilization on yield and quality of Miscanthus sinensis ‘Giganteus’ Schwarz, H.; Liebhard, P.; Ehrendorfer, K. Industrial Crops and Products, Vol. 2, Issue 3 https://doi.org/10.1016/0926-6690(94)90031-0	journal	May 1994
Miscanthus: European experience with a novel energy crop Lewandowski, I.; Clifton-Brown, J. C.; Scurlock, J. M. O. Biomass and Bioenergy, Vol. 19, Issue 4 https://doi.org/10.1016/S0961-9534(00)00032-5	journal	October 2000
Delayed harvest of miscanthus—influences on biomass quantity and quality and environmental impacts of energy production Lewandowski, I.; Heinz, A. European Journal of Agronomy, Vol. 19, Issue 1 https://doi.org/10.1016/S1161-0301(02)00018-7	journal	February 2003
Nitrogen Fertilization Management of Switchgrass, Miscanthus and Giant Reed: A Review Monti, Andrea; Zegada-Lizarazu, Walter; Zanetti, Federica Advances in Agronomy https://doi.org/10.1016/bs.agron.2018.08.001	book	September 2018
Nitrogen, energy and land use efficiencies of miscanthus, reed canary grass and triticale as determined by the boundary line approach Lewandowski, I.; Schmidt, U. Agriculture, Ecosystems & Environment, Vol. 112, Issue 4 https://doi.org/10.1016/j.agee.2005.08.003	journal	March 2006
Meta-analysis of the effects of management factors on Miscanthus×giganteus growth and biomass production Miguez, Fernando E.; Villamil, María Bonita; Long, Stephen P. Agricultural and Forest Meteorology, Vol. 148, Issue 8-9 https://doi.org/10.1016/j.agrformet.2008.03.010	journal	July 2008
Comparing annual and perennial energy cropping systems with different management intensities Boehmel, Constanze; Lewandowski, Iris; Claupein, Wilhelm Agricultural Systems, Vol. 96, Issue 1-3 https://doi.org/10.1016/j.agsy.2007.08.004	journal	March 2008
Impacts of surface-applied residues on N-cycling soil microbial communities in miscanthus and switchgrass cropping systems Thompson, Karen A.; Deen, Bill; Dunfield, Kari E. Applied Soil Ecology, Vol. 130 https://doi.org/10.1016/j.apsoil.2018.06.005	journal	September 2018
Development of switchgrass (Panicum virgatum) as a bioenergy feedstock in the United States McLaughlin, Samuel B.; Adams Kszos, Lynn Biomass and Bioenergy, Vol. 28, Issue 6 https://doi.org/10.1016/j.biombioe.2004.05.006	journal	June 2005
Energy crops in Ireland: An economic comparison of willow and Miscanthus production with conventional farming systems Styles, David; Thorne, Fiona; Jones, Michael B. Biomass and Bioenergy, Vol. 32, Issue 5 https://doi.org/10.1016/j.biombioe.2007.10.012	journal	May 2008
Variation on biomass yield and morphological traits of energy grasses from the genus Miscanthus during the first years of crop establishment Jeżowski, S.; Głowacka, K.; Kaczmarek, Z. Biomass and Bioenergy, Vol. 35, Issue 2 https://doi.org/10.1016/j.biombioe.2010.11.013	journal	February 2011
Nutrient requirements of Miscanthus x giganteus: Conclusions from a review of published studies Cadoux, Stéphane; Riche, Andrew B.; Yates, Nicola E. Biomass and Bioenergy, Vol. 38 https://doi.org/10.1016/j.biombioe.2011.01.015	journal	March 2012
The yield and quality response of the energy grass Miscanthus × giganteus to fertiliser applications of nitrogen, potassium and sulphur Shield, Ian F.; Barraclough, Tim J. P.; Riche, Andrew B. Biomass and Bioenergy, Vol. 68 https://doi.org/10.1016/j.biombioe.2014.06.007	journal	September 2014
The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance Wagner, Michael; Horn, Matthias Current Opinion in Biotechnology, Vol. 17, Issue 3 https://doi.org/10.1016/j.copbio.2006.05.005	journal	June 2006
Benefits versus risks of growing biofuel crops: the case of Miscanthus Jørgensen, Uffe Current Opinion in Environmental Sustainability, Vol. 3, Issue 1-2 https://doi.org/10.1016/j.cosust.2010.12.003	journal	March 2011
Modeling long-term yield trends of Miscanthus×giganteus using experimental data from across Europe Lesur, Claire; Jeuffroy, Marie-Hélène; Makowski, David Field Crops Research, Vol. 149 https://doi.org/10.1016/j.fcr.2013.05.004	journal	August 2013
Effects of soil water content and nitrogen supply on the productivity of Miscanthus×giganteus Greef et Deu. in a Mediterranean environment Cosentino, Salvatore L.; Patanè, Cristina; Sanzone, Emanuele Industrial Crops and Products, Vol. 25, Issue 1 https://doi.org/10.1016/j.indcrop.2006.07.006	journal	January 2007
Yield traits of six clones of Miscanthus in the first 3 years following planting in Poland Jeżowski, Stanisław Industrial Crops and Products, Vol. 27, Issue 1 https://doi.org/10.1016/j.indcrop.2007.07.013	journal	January 2008
Growth, yield and mineral content of Miscanthus×giganteus grown as a biofuel for 14 successive harvests Christian, D. G.; Riche, A. B.; Yates, N. E. Industrial Crops and Products, Vol. 28, Issue 3 https://doi.org/10.1016/j.indcrop.2008.02.009	journal	November 2008
Microbial rRNA:rDNA gene ratios may be unexpectedly low due to extracellular DNA preservation in soils Dlott, Glade; Maul, Jude E.; Buyer, Jeffrey Journal of Microbiological Methods, Vol. 115 https://doi.org/10.1016/j.mimet.2015.05.027	journal	August 2015
Economic evaluation of Miscanthus production – A review Witzel, Carl-Philipp; Finger, Robert Renewable and Sustainable Energy Reviews, Vol. 53 https://doi.org/10.1016/j.rser.2015.08.063	journal	January 2016
Differential responses of soil microbial biomass, diversity, and compositions to altitudinal gradients depend on plant and soil characteristics Ren, Chengjie; Zhang, Wei; Zhong, ZeKun Science of The Total Environment, Vol. 610-611 https://doi.org/10.1016/j.scitotenv.2017.08.110	journal	January 2018
Influence of 34-years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China Zhou, Jing; Guan, Dawei; Zhou, Baoku Soil Biology and Biochemistry, Vol. 90 https://doi.org/10.1016/j.soilbio.2015.07.005	journal	November 2015
Differential responses of total and active soil microbial communities to long-term experimental N deposition Freedman, Zachary B.; Romanowicz, Karl J.; Upchurch, Rima A. Soil Biology and Biochemistry, Vol. 90 https://doi.org/10.1016/j.soilbio.2015.08.014	journal	November 2015
Nitrate leaching in temperate agroecosystems: sources, factors and mitigating strategies Di, H. J.; Cameron, K. C. Nutrient Cycling in Agroecosystems, Vol. 64, Issue 3, p. 237-256 https://doi.org/10.1023/A:1021471531188	journal	November 2002
Miscanthus for Renewable Energy Generation: European Union Experience and Projections for Illinois Heaton, Emily A.; Clifton-Brown, John; Voigt, Thomas B. Mitigation and Adaptation Strategies for Global Change, Vol. 9, Issue 4 https://doi.org/10.1023/B:MITI.0000038848.94134.be	journal	October 2004
Active and total microbial communities in forest soil are largely different and highly stratified during decomposition Baldrian, Petr; Kolařík, Miroslav; Štursová, Martina The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.95	journal	July 2011
Microbial seed banks: the ecological and evolutionary implications of dormancy Lennon, Jay T.; Jones, Stuart E. Nature Reviews Microbiology, Vol. 9, Issue 2 https://doi.org/10.1038/nrmicro2504	journal	January 2011
Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes Delmont, Tom O.; Quince, Christopher; Shaiber, Alon Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0176-9	journal	June 2018
Comparison of DNA-, PMA-, and RNA-based 16S rRNA Illumina sequencing for detection of live bacteria in water Li, Ru; Tun, Hein Min; Jahan, Musarrat Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-02516-3	journal	July 2017
Effect of different levels of nitrogen on rhizosphere bacterial community structure in intensive monoculture of greenhouse lettuce Li, Jian-Gang; Shen, Min-Chong; Hou, Jin-Feng Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25305	journal	April 2016
Interactions between the Grasses Phalaris arundinacea, Miscanthus sinensis and Echinochloa crus-galli, and Barley and Cereal Yellow Dwarf Viruses Lamptey, J. N. L.; Plumb, R. T.; Shaw, M. W. Journal of Phytopathology, Vol. 151, Issue 7-8 https://doi.org/10.1046/j.1439-0434.2003.00752.x	journal	August 2003
Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M. Proceedings of the National Academy of Sciences, Vol. 112, Issue 35 https://doi.org/10.1073/pnas.1508382112	journal	August 2015
rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development Stoddard, Steven F.; Smith, Byron J.; Hein, Robert Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1201	journal	November 2014
The Impact of Stand Age and Fertilization on the Soil Microbiome of Miscanthus × giganteus Ma, Lanying; Rocha, Fernando Igne; Lee, Jaejin Phytobiomes Journal, Vol. 5, Issue 1 https://doi.org/10.1094/PBIOMES-01-20-0014-FI	journal	January 2021
Lost in translation: the influence of ribosomes on bacterial mRNA decay Deana, A. Genes & Development, Vol. 19, Issue 21 https://doi.org/10.1101/gad.1348805	journal	November 2005
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Effect of preservation method on the assessment of bacterial community structure in soil and water samples Tatangelo, Valeria; Franzetti, Andrea; Gandolfi, Isabella FEMS Microbiology Letters, Vol. 356, Issue 1 https://doi.org/10.1111/1574-6968.12475	journal	June 2014
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
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
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
Cropland‐to‐ Miscanthus conversion alters soil bacterial and archaeal communities influencing N‐cycle in Northern China Zhao, Chunqiao; Li, Xiaona; Yue, Yuesen GCB Bioenergy, Vol. 13, Issue 9 https://doi.org/10.1111/gcbb.12874	journal	July 2021
Soil net nitrogen mineralization and leaching under Miscanthus × giganteus and Zea mays Studt, Jacob E.; McDaniel, Marshall D.; Tejera, Mauricio D. GCB Bioenergy, Vol. 13, Issue 9 https://doi.org/10.1111/gcbb.12875	journal	July 2021
Meeting US biofuel goals with less land: the potential of Miscanthus Heaton, Emily A.; Dohleman, Frank G.; Long, Stephen P. Global Change Biology, Vol. 14, Issue 9 https://doi.org/10.1111/j.1365-2486.2008.01662.x	journal	September 2008
Impact of different bioenergy crops on N-cycling bacterial and archaeal communities in soil: Impact of bioenergy crops on soil N-cycling archaea and bacteria Mao, Yuejian; Yannarell, Anthony C.; Davis, Sarah C. Environmental Microbiology, Vol. 15, Issue 3 https://doi.org/10.1111/j.1462-2920.2012.02844.x	journal	August 2012
Nitrate leaching losses under Miscanthus grass planted on a silty clay loam soil Christian, D. G.; Riche, A. B. Soil Use and Management, Vol. 14, Issue 3 https://doi.org/10.1111/j.1475-2743.1998.tb00136.x	journal	September 1998
Long-term yield and performance of 15 different Miscanthus genotypes in southwest Germany: Long-term yield and performance of 15 different Miscanthus genotypes Gauder, M.; Graeff-Hönninger, S.; Lewandowski, I. Annals of Applied Biology, Vol. 160, Issue 2 https://doi.org/10.1111/j.1744-7348.2011.00526.x	journal	January 2012
Impact of nitrogen allocation on growth and photosynthesis of Miscanthus ( Miscanthus × giganteus ) Wang, Dan; Maughan, Mathew W.; Sun, Jindong GCB Bioenergy, Vol. 4, Issue 6 https://doi.org/10.1111/j.1757-1707.2012.01167.x	journal	March 2012
Drivers shaping the diversity and biogeography of total and active bacterial communities in the South China Sea Zhang, Yao; Zhao, Zihao; Dai, Minhan Molecular Ecology, Vol. 23, Issue 9 https://doi.org/10.1111/mec.12739	journal	April 2014
Erratum for Smercina et al., “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 22 https://doi.org/10.1128/AEM.02103-19	journal	November 2019
Microbial rRNA Synthesis and Growth Compared through Quantitative Stable Isotope Probing with H ₂ ¹⁸ O Papp, Katerina; Hungate, Bruce A.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 84, Issue 8 https://doi.org/10.1128/AEM.02441-17	journal	February 2018
Composition and Dynamics of Bacterial Communities of a Drinking Water Supply System as Assessed by RNA- and DNA-Based 16S rRNA Gene Fingerprinting Eichler, Stefan; Christen, Richard; Höltje, Claudia Applied and Environmental Microbiology, Vol. 72, Issue 3 https://doi.org/10.1128/AEM.72.3.1858-1872.2006	journal	March 2006
Denitrification Knowles, R. Microbiological Reviews, Vol. 46, Issue 1 https://doi.org/10.1128/mr.46.1.43-70.1982	journal	March 1982
RNA–DNA Ratios as Indicators of Recent Growth Rates of a Fish Bulow, Frank J. Journal of the Fisheries Research Board of Canada, Vol. 27, Issue 12 https://doi.org/10.1139/f70-262	journal	December 1970
CopyRighter: a rapid tool for improving the accuracy of microbial community profiles through lineage-specific gene copy number correction Angly, Florent E.; Dennis, Paul G.; Skarshewski, Adam Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-11	journal	April 2014
The active microbial community more accurately reflects the anaerobic digestion process: 16S rRNA (gene) sequencing as a predictive tool De Vrieze, Jo; Pinto, Ameet J.; Sloan, William T. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0449-9	journal	April 2018
Seasonal dynamics of DNA and RNA viral bioaerosol communities in a daycare center Prussin, Aaron J.; Torres, Pedro J.; Shimashita, John Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0672-z	journal	April 2019
Incorporating 16S Gene Copy Number Information Improves Estimates of Microbial Diversity and Abundance Kembel, Steven W.; Wu, Martin; Eisen, Jonathan A. PLoS Computational Biology, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pcbi.1002743	journal	October 2012
RNA Preservation Agents and Nucleic Acid Extraction Method Bias Perceived Bacterial Community Composition McCarthy, Ann; Chiang, Edna; Schmidt, Marian L. PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0121659	journal	March 2015
Performance of 15 Genotypes at Five Sites in Europe Clifton-Brown, John C.; Lewandowski, Iris; Andersson, Bengt Agronomy Journal, Vol. 93, Issue 5 https://doi.org/10.2134/agronj2001.9351013x	journal	January 2001
and Switchgrass Production in Central Illinois: Impacts on Hydrology and Inorganic Nitrogen Leaching McIsaac, Gregory F.; David, Mark B.; Illinois, Corey A. Mitchell University of Journal of Environment Quality, Vol. 39, Issue 5 https://doi.org/10.2134/jeq2009.0497	journal	January 2010
Prognostic Gene Expression Signatures Can Be Measured in Tissues Collected in RNAlater Preservative Chowdary, Dondapati; Lathrop, Jessica; Skelton, Joanne The Journal of Molecular Diagnostics, Vol. 8, Issue 1 https://doi.org/10.2353/jmoldx.2006.050056	journal	February 2006
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton Apprill, A.; McNally, S.; Parsons, R. Aquatic Microbial Ecology, Vol. 75, Issue 2 https://doi.org/10.3354/ame01753	journal	June 2015
Nitrogen Fertilization Effects on Biomass Production and Yield Components of Miscanthus ×giganteus Lee, Moon-Sub; Wycislo, Andrew; Guo, Jia Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00544	journal	April 2017
Growth and agronomy of Miscanthus x giganteus for biomass production Anderson, Eric; Arundale, Rebecca; Maughan, Matthew Biofuels, Vol. 2, Issue 1 https://doi.org/10.4155/bfs.10.80	journal	January 2011
Soil denitrifier community size changes with land use change to perennial bioenergy cropping systems Thompson, Karen A.; Deen, Bill; Dunfield, Kari E. SOIL, Vol. 2, Issue 4 https://doi.org/10.5194/soil-2-523-2016	journal	January 2016
The active microbial community more accurately reflects the anaerobic digestion process: 16S rRNA (gene) sequencing as a predictive tool Vrieze, Jo De; Pinto, Ameet; Sloan, William figshare https://doi.org/10.6084/m9.figshare.c.4056248	collection	January 2018
Seasonal dynamics of DNA and RNA viral bioaerosol communities in a daycare center Prussin, Aaron; Torres, Pedro; Shimashita, John Figshare https://doi.org/10.6084/m9.figshare.c.4455458	collection	January 2019

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59 BASIC BIOLOGICAL SCIENCES
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activity
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Response of Total (DNA) and Metabolically Active (RNA) Microbial Communities in Miscanthus × Giganteus Cultivated Soil to Different Nitrogen Fertilization Rates

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