Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development

Sieradzki, Ella T.; Nuccio, Erin E.; Pett-Ridge, Jennifer; Firestone, Mary K.

doi:10.1128/msystems.00315-23

Title: Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development

Journal Article · 26 September 2023 · mSystems

DOI: https://doi.org/10.1128/msystems.00315-23 · OSTI ID:2203352

^[1]; Nuccio, Erin E. ^[2];

^[3];

^[4]

University of California, Berkeley, CA (United States); École Centrale de Lyon (France)
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); University of California, Merced, CA (United States); University of California, Berkeley, CA (United States)
University of California, Berkeley, CA (United States)

Interactions between plant roots and rhizosphere bacteria modulate nitrogen (N)-cycling processes and create habitats rich in low molecular weight compounds (exudates) and complex organic molecules (decaying root litter) compared to those of bulk soil. Microbial N-cycling is regulated by edaphic conditions and genes from many interconnected metabolic pathways, but most studies of soil N-cycling gene expression have focused on single pathways. Currently, we lack a comprehensive understanding of the interplay between soil N-cycling gene regulation, spatial habitat, and time. We present results from a replicated time series of soil metatranscriptomes; we followed gene expression of multiple N transformations in four soil habitats (rhizosphere, detritusphere, rhizo-detritusphere, and bulk soil) during active root growth for the annual grass, Avena fatua. The presence of root litter and living roots significantly altered the trajectories of N-cycling gene expression. Upregulation of assimilatory nitrate reduction in the rhizosphere suggests that rhizosphere bacteria were actively competing with roots for nitrate. Simultaneously, ammonium assimilatory pathways were upregulated in both rhizosphere and detritusphere soil, which could have limited N availability to plants. The detritusphere supported dissimilatory processes DNRA and denitrification. Expression of nitrification genes was dominated by three phylotypes of Thaumarch aeota and was upregulated in bulk soil. Unidirectional ammonium assimilation and its regulatory genes (GS/GOGAT) were upregulated near relatively young roots and highly decayed root litter, suggesting N may have been limiting in these habitats (GS/GOGAT is typically activated under N limitation). In conclusion, our comprehensive analysis indicates that differences in carbon and inorganic N availability control contemporaneous transcription of N-cycling pathways in soil habitats.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER); Joint Genome Institute (JGI)

Grant/Contract Number:: AC52-07NA27344; SC0020163; SC0016247

OSTI ID:: 2203352

Report Number(s):: LLNL--JRNL-854336; 1082217

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 5 Vol. 8; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (90)

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
Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter: Seasonal dynamics of a soil microbial community Žifčáková, Lucia; Větrovský, Tomáš; Howe, Adina Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.13026	journal	October 2015
Litter amendment rather than phosphorus can dramatically change inorganic nitrogen pools in a degraded grassland soil by affecting nitrogen-cycling microbes Che, Rongxiao; Qin, Jinling; Tahmasbian, Iman Soil Biology and Biochemistry, Vol. 120 https://doi.org/10.1016/j.soilbio.2018.02.006	journal	May 2018
Relic DNA is abundant in soil and obscures estimates of soil microbial diversity Carini, Paul; Marsden, Patrick J.; Leff, Jonathan W. Nature Microbiology, Vol. 2, Issue 3 https://doi.org/10.1038/nmicrobiol.2016.242	journal	December 2016
Nitrate reduction and assimilation by a moderately halophilic, halotolerant bacterium Ba1 Hochman, Ayala; Nissany, Aliza; Amizur, Michal Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 965, Issue 1 https://doi.org/10.1016/0304-4165(88)90154-7	journal	April 1988
Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition Coskun, Devrim; Britto, Dev T.; Shi, Weiming Nature Plants, Vol. 3, Issue 6 https://doi.org/10.1038/nplants.2017.74	journal	June 2017
Community RNA-Seq: multi-kingdom responses to living versus decaying roots in soil Nuccio, Erin E.; Nguyen, Nhu H.; Nunes da Rocha, Ulisses ISME Communications, Vol. 1, Issue 1 https://doi.org/10.1038/s43705-021-00059-3	journal	December 2021
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference Kozlov, Alexey M.; Darriba, Diego; Flouri, Tomáš Bioinformatics, Vol. 35, Issue 21 https://doi.org/10.1093/bioinformatics/btz305	journal	May 2019
Biological nitrification inhibition (BNI)—is it a widespread phenomenon? Subbarao, G. V.; Rondon, M.; Ito, O. Plant and Soil, Vol. 294, Issue 1-2 https://doi.org/10.1007/s11104-006-9159-3	journal	December 2006
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Plant traits related to nitrogen uptake influence plant-microbe competition Moreau, Delphine; Pivato, Barbara; Bru, David Ecology, Vol. 96, Issue 8 https://doi.org/10.1890/14-1761.1	journal	August 2015
Phylogeny.fr: robust phylogenetic analysis for the non-specialist Dereeper, A.; Guignon, V.; Blanc, G. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn180	journal	May 2008
Nitrogen Regulation in Bacteria and Archaea Leigh, John A.; Dodsworth, Jeremy A. Annual Review of Microbiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093409	journal	October 2007
Review of mechanisms and quantification of priming effects Kuzyakov, Y.; Friedel, J. K.; Stahr, K. Soil Biology and Biochemistry, Vol. 32, Issue 11-12 https://doi.org/10.1016/S0038-0717(00)00084-5	journal	October 2000
Microbial expression profiles in the rhizosphere of willows depend on soil contamination Yergeau, Etienne; Sanschagrin, Sylvie; Maynard, Christine The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.163	journal	September 2013
Bridging Microbial Functional Traits With Localized Process Rates at Soil Interfaces Blagodatskaya, Evgenia; Tarkka, Mika; Knief, Claudia Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.625697	journal	October 2021
Metabolomics‐driven quantitative analysis of ammonia assimilation in E. coli Yuan, Jie; Doucette, Christopher D.; Fowler, William U. Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.60	journal	January 2009
Life and death in the soil microbiome: how ecological processes influence biogeochemistry Sokol, Noah W.; Slessarev, Eric; Marschmann, Gianna L. Nature Reviews Microbiology, Vol. 20, Issue 7 https://doi.org/10.1038/s41579-022-00695-z	journal	February 2022
Rapid Response of Nitrogen Cycling Gene Transcription to Labile Carbon Amendments in a Soil Microbial Community Chuckran, Peter F.; Fofanov, Viacheslav; Hungate, Bruce A. mSystems, Vol. 6, Issue 3 https://doi.org/10.1128/mSystems.00161-21	journal	June 2021
Biological nitrification inhibition by weeds: wild radish, brome grass, wild oats and annual ryegrass decrease nitrification rates in their rhizospheres O'Sullivan, Cathryn A.; Whisson, Kelley; Treble, Karen Crop and Pasture Science, Vol. 68, Issue 8 https://doi.org/10.1071/CP17243	journal	January 2017
Biological nitrification inhibition in the rhizosphere: determining interactions and impact on microbially mediated processes and potential applications Nardi, Pierfrancesco; Laanbroek, Hendrikus J.; Nicol, Graeme W. FEMS Microbiology Reviews, Vol. 44, Issue 6 https://doi.org/10.1093/femsre/fuaa037	journal	August 2020
Transformations of nitrogen Myrold, David D. Principles and Applications of Soil Microbiology https://doi.org/10.1016/B978-0-12-820202-9.00015-0	book	January 2021
Kinetic and mutagenic studies of the role of the active site residues Asp-50 and Glu-327 of Escherichia coli glutamine synthetase Alibhai, Murtaza; Villafranca, Joseph J. Biochemistry, Vol. 33, Issue 3 https://doi.org/10.1021/bi00169a008	journal	January 1994
Bacterial and archaeal amoA gene distribution covaries with soil nitrification properties across a range of land uses: Landscape distribution of soil ammonia oxidizers Zeglin, Lydia H.; Taylor, Anne E.; Myrold, David D. Environmental Microbiology Reports, Vol. 3, Issue 6 https://doi.org/10.1111/j.1758-2229.2011.00290.x	journal	September 2011
Spatial and temporal effects on plant-microbial competition for inorganic nitrogen in a california annual grassland Schimel, Joshua P.; Jackson, Louise E.; Firestone, Mary K. Soil Biology and Biochemistry, Vol. 21, Issue 8 https://doi.org/10.1016/0038-0717(89)90044-8	journal	January 1989
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
Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review Blagodatskaya, Е.; Kuzyakov, Y. Biology and Fertility of Soils, Vol. 45, Issue 2 https://doi.org/10.1007/s00374-008-0334-y	journal	October 2008
Author Correction: Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria Matheus Carnevali, Paula B.; Schulz, Frederik; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09423-3	journal	March 2019
Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland Jackson, Louise E.; Schimel, Joshua P.; Firestone, Mary K. Soil Biology and Biochemistry, Vol. 21, Issue 3 https://doi.org/10.1016/0038-0717(89)90152-1	journal	January 1989
Identifying multiple stressor controls on phytoplankton dynamics in the River Thames (UK) using high-frequency water quality data Bowes, M. J.; Loewenthal, M.; Read, D. S. Science of The Total Environment, Vol. 569-570 https://doi.org/10.1016/j.scitotenv.2016.06.239	journal	November 2016
Rhizosphere priming effects on soil carbon and nitrogen mineralization Zhu, Biao; Gutknecht, Jessica L. M.; Herman, Donald J. Soil Biology and Biochemistry, Vol. 76 https://doi.org/10.1016/j.soilbio.2014.04.033	journal	September 2014
Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors Rawlings, Neil D.; Barrett, Alan J.; Finn, Robert Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1118	journal	November 2015
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
A plant perspective on nitrogen cycling in the rhizosphere Moreau, Delphine; Bardgett, Richard D.; Finlay, Roger D. Functional Ecology, Vol. 33, Issue 4 https://doi.org/10.1111/1365-2435.13303	journal	March 2019
Rates of rhizodeposition and ammonium depletion in the rhizosphere of axenic oat roots Trofymow, J. A.; Coleman, D. C.; Cambardella, C. Plant and Soil, Vol. 97, Issue 3 https://doi.org/10.1007/BF02383223	journal	October 1987
Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms Tourna, Maria; Freitag, Thomas E.; Nicol, Graeme W. Environmental Microbiology, Vol. 10, Issue 5, p. 1357-1364 https://doi.org/10.1111/j.1462-2920.2007.01563.x	journal	May 2008
Niche specialization of terrestrial archaeal ammonia oxidizers Gubry-Rangin, C.; Hai, B.; Quince, C. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1109000108	journal	December 2011
Archaea predominate among ammonia-oxidizing prokaryotes in soils Leininger, S.; Urich, T.; Schloter, M. Nature, Vol. 442, Issue 7104 https://doi.org/10.1038/nature04983	journal	August 2006
Plant roots alter microbial functional genes supporting root litter decomposition Shi, Shengjing; Herman, Donald J.; He, Zhili Soil Biology and Biochemistry, Vol. 127 https://doi.org/10.1016/j.soilbio.2018.09.013	journal	December 2018
Nitrogen limitation of microbial decomposition in a grassland under elevated CO2 Hu, S.; Chapin, F. S.; Firestone, M. K. Nature, Vol. 409, Issue 6817 https://doi.org/10.1038/35051576	journal	January 2001
Soil metatranscriptome demonstrates a shift in C, N, and S metabolisms of a grassland ecosystem in response to elevated atmospheric CO2 Rosado-Porto, David; Ratering, Stefan; Moser, Gerald Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.937021	journal	August 2022
Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH: Gene transcription, gas kinetics as affected by soil pH Liu, Binbin; Mørkved, Pål Tore; Frostegård, Åsa FEMS Microbiology Ecology, Vol. 72, Issue 3 https://doi.org/10.1111/j.1574-6941.2010.00856.x	journal	February 2010
Comparing DNA, RNA and protein levels for measuring microbial dynamics in soil microcosms amended with nitrogen fertilizer Orellana, Luis H.; Hatt, Janet K.; Iyer, Ramsunder Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-53679-0	journal	November 2019
Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota Kozlowski, Jessica A.; Stieglmeier, Michaela; Schleper, Christa The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2016.2	journal	February 2016
Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen Clarholm, Marianne Soil Biology and Biochemistry, Vol. 17, Issue 2 https://doi.org/10.1016/0038-0717(85)90113-0	journal	January 1985
Species strategy and N fluxes in grassland soil Personeni, E.; Loiseau, P. European Journal of Agronomy, Vol. 22, Issue 2 https://doi.org/10.1016/j.eja.2004.02.007	journal	February 2005
Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene: Archaeal ammonia oxidation in soil Offre, Pierre; Prosser, James I.; Nicol, Graeme W. FEMS Microbiology Ecology, Vol. 70, Issue 1 https://doi.org/10.1111/j.1574-6941.2009.00725.x	journal	October 2009
Interactive Tree Of Life (iTOL) v4: recent updates and new developments Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz239	journal	April 2019
Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies Prosser, James I.; Hink, Linda; Gubry‐Rangin, Cécile Global Change Biology, Vol. 26, Issue 1 https://doi.org/10.1111/gcb.14877	journal	November 2019
Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen Levičnik-Höfferle, Špela; Nicol, Graeme W.; Ausec, Luka FEMS Microbiology Ecology, Vol. 80, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01275.x	journal	January 2012
Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea: Structural biology insights into key AOA enzymes Tolar, Bradley B.; Herrmann, Jonathan; Bargar, John R. Environmental Microbiology Reports, Vol. 9, Issue 5 https://doi.org/10.1111/1758-2229.12567	journal	July 2017
Increased microbial expression of organic nitrogen cycling genes in long-term warmed grassland soils Séneca, Joana; Söllinger, Andrea; Herbold, Craig W. ISME Communications, Vol. 1, Issue 1 https://doi.org/10.1038/s43705-021-00073-5	journal	November 2021
Short-term response of soil N-cycling genes and transcripts to fertilization with nitrification and urease inhibitors, and relationship with field-scale N2O emissions Tosi, Micaela; Brown, Shannon; Ferrari Machado, Pedro Vitor Soil Biology and Biochemistry, Vol. 142 https://doi.org/10.1016/j.soilbio.2019.107703	journal	March 2020
Welcome to the Tidyverse Wickham, Hadley; Averick, Mara; Bryan, Jennifer Journal of Open Source Software, Vol. 4, Issue 43 https://doi.org/10.21105/joss.01686	journal	November 2019
Arabidopsis mutant analysis and gene regulation define a nonredundant role for glutamate dehydrogenase in nitrogen assimilation. Melo-Oliveira, R.; Oliveira, I. C.; Coruzzi, G. M. Proceedings of the National Academy of Sciences, Vol. 93, Issue 10 https://doi.org/10.1073/pnas.93.10.4718	journal	May 1996
A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI) Subbarao, G. V.; Sahrawat, K. L.; Nakahara, K. Annals of Botany, Vol. 112, Issue 2 https://doi.org/10.1093/aob/mcs230	journal	October 2012
CD-HIT Suite: a web server for clustering and comparing biological sequences Huang, Ying; Niu, Beifang; Gao, Ying Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btq003	journal	January 2010
The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria Nicol, Graeme W.; Leininger, Sven; Schleper, Christa Environmental Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-2920.2008.01701.x	journal	November 2008
Short-Term Nitrogen Fertilization Affects Microbial Community Composition and Nitrogen Mineralization Functions in an Agricultural Soil Ouyang, Yang; Norton, Jeanette M. Applied and Environmental Microbiology, Vol. 86, Issue 5 https://doi.org/10.1128/AEM.02278-19	journal	December 2019
Nitrogen Dynamics in an Annual Grassland: oak Canopy, Climate, and Microbial Population Effects Herman, Donald J.; Halverson, Larry J.; Firestone, Mary K. Ecological Applications, Vol. 13, Issue 3 https://doi.org/10.1890/1051-0761(2003)013[0593:NDIAAG]2.0.CO;2	journal	June 2003
Soil contamination alters the willow root and rhizosphere metatranscriptome and the root–rhizosphere interactome Yergeau, Etienne; Tremblay, Julien; Joly, Simon The ISME Journal, Vol. 12, Issue 3 https://doi.org/10.1038/s41396-017-0018-4	journal	January 2018
Root Influence on Nitrogen Mineralization and Nitrification in Rhizosphere Soil Herman, D. J.; Johnson, K. K.; Jaeger, C. H. Soil Science Society of America Journal, Vol. 70, Issue 5 https://doi.org/10.2136/sssaj2005.0113	journal	January 2006
Transcriptional Response of Nitrifying Communities to Wetting of Dry Soil Placella, Sarah A.; Firestone, Mary K. Applied and Environmental Microbiology, Vol. 79, Issue 10 https://doi.org/10.1128/AEM.00404-13	journal	March 2013
The products of glnL and glnG are bifunctional regulatory proteins MacNeil, Tanya; Roberts, Gary P.; MacNeil, Douglas Molecular and General Genetics MGG, Vol. 188, Issue 2 https://doi.org/10.1007/BF00332696	journal	December 1982
Global Patterns and Drivers of Soil Dissimilatory Nitrate Reduction to Ammonium Cheng, Yi; Elrys, Ahmed S.; Merwad, Abdel-Rahman M. Environmental Science & Technology, Vol. 56, Issue 6 https://doi.org/10.1021/acs.est.1c07997	journal	February 2022
Protozoa stimulate N uptake and growth of arbuscular mycorrhizal plants Koller, Robert; Scheu, Stefan; Bonkowski, Michael Soil Biology and Biochemistry, Vol. 65 https://doi.org/10.1016/j.soilbio.2013.05.020	journal	October 2013
Correction to: Expression of macromolecular organic nitrogen degrading enzymes identifies potential mediators of soil organic N availability to an annual grass Sieradzki, Ella T.; Nuccio, Erin E.; Pett-Ridge, Jennifer The ISME Journal, Vol. 17, Issue 7 https://doi.org/10.1038/s41396-023-01441-w	journal	May 2023
Patterns of thaumarchaeal gene expression in culture and diverse marine environments Carini, Paul; Dupont, Christopher L.; Santoro, Alyson E. Environmental Microbiology, Vol. 20, Issue 6 https://doi.org/10.1111/1462-2920.14107	journal	April 2018
Distributions of Extracellular Peptidases Across Prokaryotic Genomes Reflect Phylogeny and Habitat Nguyen, Trang T. H.; Myrold, David D.; Mueller, Ryan S. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00413	journal	March 2019
Plant and soil nitrogen dynamics in California annual grassland Jackson, L. E.; Strauss, R. B.; Firestone, M. K. Plant and Soil, Vol. 110, Issue 1 https://doi.org/10.1007/BF02143533	journal	August 1988
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features Liao, Y.; Smyth, G. K.; Shi, W. Bioinformatics, Vol. 30, Issue 7 https://doi.org/10.1093/bioinformatics/btt656	journal	November 2013
Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation Bayer, Barbara; Vojvoda, Jana; Offre, Pierre The ISME Journal, Vol. 10, Issue 5 https://doi.org/10.1038/ismej.2015.200	journal	November 2015
Niche differentiation is spatially and temporally regulated in the rhizosphere Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0582-x	journal	January 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
Niche construction by the invasive Asian knotweeds (species complex Fallopia): impact on activity, abundance and community structure of denitrifiers and nitrifiers Dassonville, Nicolas; Guillaumaud, Nadine; Piola, Florence Biological Invasions, Vol. 13, Issue 5 https://doi.org/10.1007/s10530-011-9954-5	journal	February 2011
Autotrophic ammonia oxidation by soil thaumarchaea Zhang, L. -M.; Offre, P. R.; He, J. -Z. Proceedings of the National Academy of Sciences, Vol. 107, Issue 40 https://doi.org/10.1073/pnas.1004947107	journal	September 2010
Annual grassland resource pools and fluxes: sensitivity to precipitation and dry periods on two contrasting soils Sudderth, Erika A.; St. Clair, Samuel B.; Placella, Sarah A. Ecosphere, Vol. 3, Issue 8 https://doi.org/10.1890/ES12-00004.1	journal	August 2012
Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli Bueno, R.; Pahel, G.; Magasanik, B. Journal of Bacteriology, Vol. 164, Issue 2 https://doi.org/10.1128/jb.164.2.816-822.1985	journal	November 1985
Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil Pratscher, J.; Dumont, M. G.; Conrad, R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 10 https://doi.org/10.1073/pnas.1010981108	journal	February 2011
Depth distributions of nitrite reductase ( nirK ) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay Reji, Linta; Tolar, Bradley B.; Smith, Jason M. Environmental Microbiology, Vol. 21, Issue 11 https://doi.org/10.1111/1462-2920.14753	journal	August 2019
Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil Pepe-Ranney, Charles; Campbell, Ashley N.; Koechli, Chantal N. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00703	journal	May 2016
P _II signal transduction proteins: nitrogen regulation and beyond Huergo, Luciano F.; Chandra, Govind; Merrick, Mike FEMS Microbiology Reviews, Vol. 37, Issue 2 https://doi.org/10.1111/j.1574-6976.2012.00351.x	journal	March 2013
Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates Henry, S.; Texier, S.; Hallet, S. Environmental Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-2920.2008.01599.x	journal	November 2008
A Mesophilic, Autotrophic, Ammonia-Oxidizing Archaeon of Thaumarchaeal Group I.1a Cultivated from a Deep Oligotrophic Soil Horizon Jung, Man-Young; Park, Soo-Je; Kim, So-Jeong Applied and Environmental Microbiology, Vol. 80, Issue 12 https://doi.org/10.1128/AEM.03730-13	journal	April 2014
Insights into the physiology of ammonia-oxidizing microorganisms Stein, Lisa Y. Current Opinion in Chemical Biology, Vol. 49 https://doi.org/10.1016/j.cbpa.2018.09.003	journal	April 2019
Glutamate dehydrogenase from Escherichia coli: purification and properties Sakamoto, N.; Kotre, A. M.; Savageau, M. A. Journal of Bacteriology, Vol. 124, Issue 2 https://doi.org/10.1128/jb.124.2.775-783.1975	journal	November 1975
Rhizosphere bacteriome structure and functions Ling, Ning; Wang, Tingting; Kuzyakov, Yakov Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28448-9	journal	February 2022
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Microbial Nitrogen Limitation Increases Decomposition Craine, Joseph M.; Morrow, Carl; Fierer, Noah Ecology, Vol. 88, Issue 8 https://doi.org/10.1890/06-1847.1	journal	August 2007

Similar Records

Community RNA-Seq: multi-kingdom responses to living versus decaying roots in soil

Journal Article · 2021 · ISME Communications · OSTI ID:1834274

Nuccio, Erin E.; Nguyen, Nhu H.; Nunes da Rocha, Ulisses; +6 more

Expression of macromolecular organic nitrogen degrading enzymes identifies potential mediators of soil organic N availability to an annual grass

Journal Article · 2023 · The ISME Journal · OSTI ID:1970056

Sieradzki, Ella T.; Nuccio, Erin E.; Pett-Ridge, Jennifer; +1 more

Niche differentiation is spatially and temporally regulated in the rhizosphere

Journal Article · 2020 · The ISME Journal · OSTI ID:1597728

Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas; +8 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
Agriculture and botany
Environmental sciences
soil microbiome
soil nitrogen
rhizosphere
gene expression
metatranscriptomics
nitrification
plant litter
detritusph

Title: Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development

Citation Formats

References (90)

Similar Records

Related Subjects