Niche differentiation is spatially and temporally regulated in the rhizosphere

Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas; Brodie, Eoin L.; Zhou, Jizhong; Tringe, Susannah G.; Malmstrom, Rex R.; Woyke, Tanja; Banfield, Jillian F.; Firestone, Mary K.; Pett-Ridge, Jennifer

doi:10.1038/s41396-019-0582-x

Niche differentiation is spatially and temporally regulated in the rhizosphere

Journal Article · Fri Jan 17 00:00:00 EST 2020 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-019-0582-x· OSTI ID:2281290

; Starr, Evan; ; ; ; ; Malmstrom, Rex R.; ; ; Firestone, Mary K.;

Abstract

The rhizosphere is a hotspot for microbial carbon transformations, and is the entry point for root polysaccharides and polymeric carbohydrates that are important precursors to soil organic matter (SOM). However, the ecological mechanisms that underpin rhizosphere carbohydrate depolymerization are poorly understood. Using Avena fatua, a common annual grass, we analyzed time-resolved metatranscriptomes to compare microbial functions in rhizosphere, detritusphere, and combined rhizosphere–detritusphere habitats. Transcripts were binned using a unique reference database generated from soil isolate genomes, single-cell amplified genomes, metagenomes, and stable isotope probing metagenomes. While soil habitat significantly affected both community composition and overall gene expression, the succession of microbial functions occurred at a faster time scale than compositional changes. Using hierarchical clustering of upregulated decomposition genes, we identified four distinct microbial guilds populated by taxa whose functional succession patterns suggest specialization for substrates provided by fresh growing roots, decaying root detritus, the combination of live and decaying root biomass, or aging root material. Carbohydrate depolymerization genes were consistently upregulated in the rhizosphere, and both taxonomic and functional diversity were highest in the combined rhizosphere–detritusphere, suggesting coexistence of rhizosphere guilds is facilitated by niche differentiation. Metatranscriptome-defined guilds provide a framework to model rhizosphere succession and its consequences for soil carbon cycling.

View Journal Article

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231; AC52-07NA27344; SC0010570; SC0016247

OSTI ID:: 2281290

Alternate ID(s):: OSTI ID: 1623334
OSTI ID: 1597728

Report Number(s):: LLNL-JRNL--772364

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 4 Vol. 14; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (101)

Modeling Global Soil Carbon and Soil Microbial Carbon by Integrating Microbial Processes into the Ecosystem Process Model TRIPLEX-GHG: GLOBAL SOIL CARBON AND MICROBIAL CARBON Wang, Kefeng; Peng, Changhui; Zhu, Qiuan Journal of Advances in Modeling Earth Systems, Vol. 9, Issue 6 https://doi.org/10.1002/2017MS000920	journal	October 2017
Litter chemistry influences decomposition through activity of specific microbial functional guilds Bhatnagar, Jennifer M.; Peay, Kabir G.; Treseder, Kathleen K. Ecological Monographs, Vol. 88, Issue 3 https://doi.org/10.1002/ecm.1303	journal	May 2018
Manipulating the soil microbiome to increase soil health and plant fertility Chaparro, Jacqueline M.; Sheflin, Amy M.; Manter, Daniel K. Biology and Fertility of Soils, Vol. 48, Issue 5 https://doi.org/10.1007/s00374-012-0691-4	journal	May 2012
Stimulation of Different Functional Groups of Bacteria by Various Plant Residues as a Driver of Soil Priming Effect Pascault, Noémie; Ranjard, Lionel; Kaisermann, Aurore Ecosystems, Vol. 16, Issue 5 https://doi.org/10.1007/s10021-013-9650-7	journal	February 2013
Bacterial reference genes for gene expression studies by RT-qPCR: survey and analysis Rocha, Danilo J. P.; Santos, Carolina S.; Pacheco, Luis G. C. Antonie van Leeuwenhoek, Vol. 108, Issue 3 https://doi.org/10.1007/s10482-015-0524-1	journal	July 2015
Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation Rasse, Daniel P.; Rumpel, Cornelia; Dignac, Marie-France Plant and Soil, Vol. 269, Issue 1-2 https://doi.org/10.1007/s11104-004-0907-y	journal	February 2005
Spatial and temporal dynamics of hotspots of enzyme activity in soil as affected by living and dead roots—a soil zymography analysis Spohn, Marie; Kuzyakov, Yakov Plant and Soil, Vol. 379, Issue 1-2 https://doi.org/10.1007/s11104-014-2041-9	journal	February 2014
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
The priming effect of organic matter: a question of microbial competition? Fontaine, Sébastien; Mariotti, André; Abbadie, Luc Soil Biology and Biochemistry, Vol. 35, Issue 6 https://doi.org/10.1016/S0038-0717(03)00123-8	journal	June 2003
Using stable isotopes to explore root-microbe-mineral interactions in soil Pett-Ridge, Jennifer; Firestone, Mary K. Rhizosphere, Vol. 3 https://doi.org/10.1016/j.rhisph.2017.04.016	journal	June 2017
Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil Bird, Jeffrey A.; Herman, Donald J.; Firestone, Mary K. Soil Biology and Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1016/j.soilbio.2010.08.010	journal	April 2011
Microbial hotspots and hot moments in soil: Concept & review Kuzyakov, Yakov; Blagodatskaya, Evgenia Soil Biology and Biochemistry, Vol. 83 https://doi.org/10.1016/j.soilbio.2015.01.025	journal	April 2015
Disentangling carbon flow across microbial kingdoms in the rhizosphere of maize Hünninghaus, Maike; Dibbern, Dörte; Kramer, Susanne Soil Biology and Biochemistry, Vol. 134 https://doi.org/10.1016/j.soilbio.2019.03.007	journal	July 2019
Plant coexistence and the niche Silvertown, J. Trends in Ecology & Evolution, Vol. 19, Issue 11 https://doi.org/10.1016/j.tree.2004.09.003	journal	November 2004
Rebuilding community ecology from functional traits Mcgill, B.; Enquist, B.; Weiher, E. Trends in Ecology & Evolution, Vol. 21, Issue 4 https://doi.org/10.1016/j.tree.2006.02.002	journal	April 2006
Selective progressive response of soil microbial community to wild oat roots DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z. The ISME Journal, Vol. 3, Issue 2 https://doi.org/10.1038/ismej.2008.103	journal	November 2008
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea McDonald, Daniel; Price, Morgan N.; Goodrich, Julia The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.139	journal	December 2011
Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach Tannock, Gerald W.; Wilson, Charlotte M.; Loach, Diane The ISME Journal, Vol. 6, Issue 5 https://doi.org/10.1038/ismej.2011.161	journal	November 2011
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Sizing up metatranscriptomics Moran, Mary Ann; Satinsky, Brandon; Gifford, Scott M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.94	journal	August 2012
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
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
Rhizosphere microbiome assemblage is affected by plant development Chaparro, Jacqueline M.; Badri, Dayakar V.; Vivanco, Jorge M. The ISME Journal, Vol. 8, Issue 4 https://doi.org/10.1038/ismej.2013.196	journal	November 2013
Taxonomical and functional microbial community selection in soybean rhizosphere Mendes, Lucas W.; Kuramae, Eiko E.; Navarrete, Acácio A. The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.17	journal	February 2014
ProDeGe: a computational protocol for fully automated decontamination of genomes Tennessen, Kristin; Andersen, Evan; Clingenpeel, Scott The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.100	journal	June 2015
Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere Yan, Yan; Kuramae, Eiko E.; de Hollander, Mattias The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.108	journal	August 2016
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life Parks, Donovan H.; Chuvochina, Maria; Waite, David W. Nature Biotechnology, Vol. 36, Issue 10 https://doi.org/10.1038/nbt.4229	journal	August 2018
Mineral protection of soil carbon counteracted by root exudates Keiluweit, Marco; Bougoure, Jeremy J.; Nico, Peter S. Nature Climate Change, Vol. 5, Issue 6 https://doi.org/10.1038/nclimate2580	journal	March 2015
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls Kallenbach, Cynthia M.; Frey, Serita D.; Grandy, A. Stuart Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13630	journal	November 2016
Niche and host-associated functional signatures of the root surface microbiome Ofek-Lalzar, Maya; Sela, Noa; Goldman-Voronov, Milana Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5950	journal	September 2014
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Transcriptional interactions suggest niche segregation among microorganisms in the human gut Plichta, Damian Rafal; Juncker, Agnieszka Sierakowska; Bertalan, Marcelo Nature Microbiology, Vol. 1, Issue 11 https://doi.org/10.1038/nmicrobiol.2016.152	journal	August 2016
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics Rinke, Christian; Lee, Janey; Nath, Nandita Nature Protocols, Vol. 9, Issue 5 https://doi.org/10.1038/nprot.2014.067	journal	April 2014
Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology Prosser, James I. Nature Reviews Microbiology, Vol. 13, Issue 7 https://doi.org/10.1038/nrmicro3468	journal	June 2015
Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling López-Mondéjar, Ruben; Brabcová, Vendula; Štursová, Martina The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0084-2	journal	February 2018
Predictive genomic traits for bacterial growth in culture versus actual growth in soil Li, Junhui; Mau, Rebecca L.; Dijkstra, Paul The ISME Journal, Vol. 13, Issue 9 https://doi.org/10.1038/s41396-019-0422-z	journal	May 2019
Function and functional redundancy in microbial systems Louca, Stilianos; Polz, Martin F.; Mazel, Florent Nature Ecology & Evolution, Vol. 2, Issue 6 https://doi.org/10.1038/s41559-018-0519-1	journal	April 2018
Microbial formation of stable soil carbon is more efficient from belowground than aboveground input Sokol, Noah W.; Bradford, Mark A. Nature Geoscience, Vol. 12, Issue 1 https://doi.org/10.1038/s41561-018-0258-6	journal	November 2018
Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface Probst, Alexander J.; Ladd, Bethany; Jarett, Jessica K. Nature Microbiology, Vol. 3, Issue 3 https://doi.org/10.1038/s41564-017-0098-y	journal	January 2018
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
Genome-centric view of carbon processing in thawing permafrost Woodcroft, Ben J.; Singleton, Caitlin M.; Boyd, Joel A. Nature, Vol. 560, Issue 7716 https://doi.org/10.1038/s41586-018-0338-1	journal	July 2018
Genomic features of bacterial adaptation to plants Levy, Asaf; Salas Gonzalez, Isai; Mittelviefhaus, Maximilian Nature Genetics, Vol. 50, Issue 1 https://doi.org/10.1038/s41588-017-0012-9	journal	December 2017
Cytochrome cbb3 oxidase and bacterial microaerobic metabolism Pitcher, R. S.; Brittain, T.; Watmugh, N. J. Biochemical Society Transactions, Vol. 30, Issue 4 https://doi.org/10.1042/bst0300653	journal	August 2002
The diversity and biogeography of soil bacterial communities Fierer, N.; Jackson, R. B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0507535103	journal	January 2006
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Bacterial community assembly based on functional genes rather than species Burke, C.; Steinberg, P.; Rusch, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1101591108	journal	August 2011
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups Placella, S. A.; Brodie, E. L.; Firestone, M. K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1204306109	journal	June 2012
Structure, variation, and assembly of the root-associated microbiomes of rice Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1414592112	journal	January 2015
Causes and consequences of biological diversity in soil Bardgett, R. Zoology, Vol. 105, Issue 4 https://doi.org/10.1078/0944-2006-00072	journal	January 2002
The Limiting Similarity, Convergence, and Divergence of Coexisting Species Macarthur, Robert; Levins, Richard The American Naturalist, Vol. 101, Issue 921 https://doi.org/10.1086/282505	journal	September 1967
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
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
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
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
NCBI BLAST: a better web interface Johnson, M.; Zaretskaya, I.; Raytselis, Y. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn201	journal	May 2008
GtRNAdb: a database of transfer RNA genes detected in genomic sequence Chan, P. P.; Lowe, T. M. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn787	journal	January 2009
tRNADB-CE 2011: tRNA gene database curated manually by experts Abe, T.; Ikemura, T.; Sugahara, J. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq1007	journal	November 2010
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky901	journal	October 2018
Transfer of Bacteroides succinogenes (Hungate) to Fibrobacter gen. nov. as Fibrobacter succinogenes comb. nov. and Description of Fibrobacter intestinalis sp. nov. Montgomery, L.; Flesher, B.; Stahl, D. International Journal of Systematic Bacteriology, Vol. 38, Issue 4 https://doi.org/10.1099/00207713-38-4-430	journal	October 1988
Cephaloticoccus gen. nov., a new genus of ‘Verrucomicrobia’ containing two novel species isolated from Cephalotes ant guts Lin, Jonathan Y.; Russell, Jacob A.; Sanders, Jon G. International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 8 https://doi.org/10.1099/ijsem.0.001141	journal	August 2016
Concluding Remarks Hutchinson, G. E. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 22, Issue 0 https://doi.org/10.1101/SQB.1957.022.01.039	journal	January 1957
Microbial community assembly differs across minerals in a rhizosphere microcosm Whitman, Thea; Neurath, Rachel; Perera, Adele Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14366	journal	September 2018
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J. Ecology Letters, Vol. 19, Issue 8 https://doi.org/10.1111/ele.12630	journal	June 2016
Carbon input by roots into the soil: Quantification of rhizodeposition from root to ecosystem scale Pausch, Johanna; Kuzyakov, Yakov Global Change Biology, Vol. 24, Issue 1 https://doi.org/10.1111/gcb.13850	journal	September 2017
Cover crop root contributions to soil carbon in a no-till corn bioenergy cropping system Austin, Emily E.; Wickings, Kyle; McDaniel, Marshall D. GCB Bioenergy, Vol. 9, Issue 7 https://doi.org/10.1111/gcbb.12428	journal	January 2017
The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems van der Heijden, Marcel G. A.; Bardgett, Richard D.; van Straalen, Nico M. Ecology Letters, Vol. 11, Issue 3 https://doi.org/10.1111/j.1461-0248.2007.01139.x	journal	March 2008
Bacterial quorum sensing and nitrogen cycling in rhizosphere soil: Bacterial QS and rhizosphere nitrogen cycling DeAngelis, Kristen M.; Lindow, Steven E.; Firestone, Mary K. FEMS Microbiology Ecology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00550.x	journal	November 2008
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities Ihrmark, Katarina; Bödeker, Inga T. M.; Cruz-Martinez, Karelyn FEMS Microbiology Ecology, Vol. 82, Issue 3 https://doi.org/10.1111/j.1574-6941.2012.01437.x	journal	July 2012
Identification of microbial populations driving biopolymer degradation in acidic peatlands by metatranscriptomic analysis Ivanova, Anastasia A.; Wegner, Carl-Eric; Kim, Yongkyu Molecular Ecology, Vol. 25, Issue 19 https://doi.org/10.1111/mec.13806	journal	September 2016
Synthesis and modeling perspectives of rhizosphere priming Cheng, Weixin; Parton, William J.; Gonzalez-Meler, Miquel A. New Phytologist, Vol. 201, Issue 1 https://doi.org/10.1111/nph.12440	journal	August 2013
Microbiomes in light of traits: A phylogenetic perspective Martiny, J. B. H.; Jones, S. E.; Lennon, J. T. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aac9323	journal	November 2015
Emergent simplicity in microbial community assembly Goldford, Joshua E.; Lu, Nanxi; Bajić, Djordje Science, Vol. 361, Issue 6401 https://doi.org/10.1126/science.aat1168	journal	August 2018
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
Phylogenetic Distribution of Potential Cellulases in Bacteria Berlemont, Renaud; Martiny, Adam C. Applied and Environmental Microbiology, Vol. 79, Issue 5 https://doi.org/10.1128/AEM.03305-12	journal	December 2012
Genomic Potential for Polysaccharide Deconstruction in Bacteria Berlemont, Renaud; Martiny, Adam C. Applied and Environmental Microbiology, Vol. 81, Issue 4 https://doi.org/10.1128/AEM.03718-14	journal	December 2014
Genomic and Physiological Characterization of the Verrucomicrobia Isolate Diplosphaera colitermitum gen. nov., sp. nov., Reveals Microaerophily and Nitrogen Fixation Genes Wertz, John T.; Kim, Eunji; Breznak, John A. Applied and Environmental Microbiology, Vol. 78, Issue 5 https://doi.org/10.1128/AEM.06466-11	journal	December 2011
Identification of Cellulose-Responsive Bacterial and Fungal Communities in Geographically and Edaphically Different Soils by Using Stable Isotope Probing Eichorst, Stephanie A.; Kuske, Cheryl R. Applied and Environmental Microbiology, Vol. 78, Issue 7 https://doi.org/10.1128/AEM.07313-11	journal	January 2012
Microgradients of Microbial Oxygen Consumption in a Barley Rhizosphere Model System Højberg, Ole; Sørensen, Jan Applied and Environmental Microbiology, Vol. 59, Issue 2 https://doi.org/10.1128/AEM.59.2.431-437.1993	journal	January 1993
Mapping of Sugar and Amino Acid Availability in Soil around Roots with Bacterial Sensors of Sucrose and Tryptophan Jaeger, C. H.; Lindow, S. E.; Miller, W. Applied and Environmental Microbiology, Vol. 65, Issue 6 https://doi.org/10.1128/AEM.65.6.2685-2690.1999	journal	January 1999
Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition Griffiths, R. I.; Whiteley, A. S.; O'Donnell, A. G. Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5488-5491.2000	journal	December 2000
Oligonucleotide Microarray for the Study of Functional Gene Diversity in the Nitrogen Cycle in the Environment Taroncher-Oldenburg, G.; Griner, E. M.; Francis, C. A. Applied and Environmental Microbiology, Vol. 69, Issue 2 https://doi.org/10.1128/AEM.69.2.1159-1171.2003	journal	February 2003
Genome Sequence of the Verrucomicrobium Opitutus terrae PB90-1, an Abundant Inhabitant of Rice Paddy Soil Ecosystems van Passel, M. W. J.; Kant, R.; Palva, A. Journal of Bacteriology, Vol. 193, Issue 9 https://doi.org/10.1128/JB.00228-11	journal	March 2011
Patterns and Processes of Microbial Community Assembly Nemergut, D. R.; Schmidt, S. K.; Fukami, T. Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3 https://doi.org/10.1128/MMBR.00051-12	journal	September 2013
Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons Shi, Shengjing; Nuccio, Erin; Herman, Donald J. mBio, Vol. 6, Issue 4 https://doi.org/10.1128/mBio.00746-15	journal	August 2015
The Ecology of Soil Carbon: Pools, Vulnerabilities, and Biotic and Abiotic Controls Jackson, Robert B.; Lajtha, Kate; Crow, Susan E. Annual Review of Ecology, Evolution, and Systematics, Vol. 48, Issue 1 https://doi.org/10.1146/annurev-ecolsys-112414-054234	journal	November 2017
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
Combining multiple functional annotation tools increases coverage of metabolic annotation Griesemer, Marc; Kimbrel, Jeffrey A.; Zhou, Carol E. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-5221-9	journal	December 2018
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
Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon Starr, Evan P.; Shi, Shengjing; Blazewicz, Steven J. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0499-z	journal	July 2018
A Theoretical Model of Litter Decay and Microbial Interaction Moorhead, Daryl L.; Sinsabaugh, Robert L. Ecological Monographs, Vol. 76, Issue 2 https://doi.org/10.1890/0012-9615(2006)076[0151:ATMOLD]2.0.CO;2	journal	May 2006
Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass Nuccio, Erin E.; Anderson-Furgeson, James; Estera, Katerina Y. Ecology, Vol. 97, Issue 5 https://doi.org/10.1890/15-0882.1	journal	May 2016
The Niche Exploitation Pattern of the Blue-Gray Gnatcatcher Root, Richard B. Ecological Monographs, Vol. 37, Issue 4 https://doi.org/10.2307/1942327	journal	February 1967
Microbial control over carbon cycling in soil Schimel, Joshua P.; Schaeffer, Sean M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00348	journal	January 2012
Primer and platform effects on 16S rRNA tag sequencing Tremblay, Julien; Singh, Kanwar; Fern, Alison Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00771	journal	August 2015
Commentary: Oil degradation and biosurfactant production by the deep sea bacterium Dietzia maris As-13-3 Rahman, Pattanathu K. S. M.; Sekhon Randhawa, Kamaljeet K. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01557	journal	January 2016

Similar Records

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

Journal Article · Tue Sep 26 20:00:00 EDT 2023 · mSystems · OSTI ID:2203352

Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
Biological and medical sciences
Environmental sciences
Microbial ecology
Microbiome
Soil microbiology
microbial ecology
microbiome
soil microbiology

Niche differentiation is spatially and temporally regulated in the rhizosphere

Citation Formats

References (101)

Similar Records

Related Subjects