skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Niche differentiation is spatially and temporally regulated in the rhizosphere

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. Finally, metatranscriptome-defined guilds provide a framework to model rhizosphere succession and its consequences formore » soil carbon cycling.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5];  [5]; ORCiD logo [5]; ORCiD logo [6];  [6]; ORCiD logo [1]
  1. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  2. Univ. of California, Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Oklahoma, Norman, OK (United States); Tsinghua Univ., Beijing (China)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1597728
Alternate Identifier(s):
OSTI ID: 1623334
Report Number(s):
LLNL-JRNL-772364
Journal ID: ISSN 1751-7362; ark:/13030/qt8vc6d014
Grant/Contract Number:  
AC02-05CH11231; SCW1589; SCW1039; SC0010570; SC0016247; SC10010566; AC52-07NA27344; 1487; 1472
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 14; Journal Issue: 4; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; microbial ecology; microbiome; soil microbiology; Environmental sciences; Biological and medical sciences

Citation Formats

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., and Pett-Ridge, Jennifer. Niche differentiation is spatially and temporally regulated in the rhizosphere. United States: N. p., 2020. Web. doi:10.1038/s41396-019-0582-x.
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. Niche differentiation is spatially and temporally regulated in the rhizosphere. United States. doi:https://doi.org/10.1038/s41396-019-0582-x
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., and Pett-Ridge, Jennifer. Fri . "Niche differentiation is spatially and temporally regulated in the rhizosphere". United States. doi:https://doi.org/10.1038/s41396-019-0582-x. https://www.osti.gov/servlets/purl/1597728.
@article{osti_1597728,
title = {Niche differentiation is spatially and temporally regulated in the rhizosphere},
author = {Nuccio, Erin E. and Starr, Evan and Karaoz, Ulas and Brodie, Eoin L. and Zhou, Jizhong and Tringe, Susannah G. and Malmstrom, Rex R. and Woyke, Tanja and Banfield, Jillian F. and Firestone, Mary K. and Pett-Ridge, Jennifer},
abstractNote = {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. Finally, metatranscriptome-defined guilds provide a framework to model rhizosphere succession and its consequences for soil carbon cycling.},
doi = {10.1038/s41396-019-0582-x},
journal = {The ISME Journal},
number = 4,
volume = 14,
place = {United States},
year = {2020},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

A Theoretical Model of Litter Decay and Microbial Interaction
journal, May 2006


Mineral protection of soil carbon counteracted by root exudates
journal, March 2015

  • Keiluweit, Marco; Bougoure, Jeremy J.; Nico, Peter S.
  • Nature Climate Change, Vol. 5, Issue 6
  • DOI: 10.1038/nclimate2580

Cytochrome cbb3 oxidase and bacterial microaerobic metabolism
journal, August 2002

  • Pitcher, R. S.; Brittain, T.; Watmugh, N. J.
  • Biochemical Society Transactions, Vol. 30, Issue 4
  • DOI: 10.1042/bst0300653

Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018


Structure, variation, and assembly of the root-associated microbiomes of rice
journal, January 2015

  • Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1414592112

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

Concluding Remarks
journal, January 1957


Cover crop root contributions to soil carbon in a no-till corn bioenergy cropping system
journal, January 2017

  • Austin, Emily E.; Wickings, Kyle; McDaniel, Marshall D.
  • GCB Bioenergy, Vol. 9, Issue 7
  • DOI: 10.1111/gcbb.12428

Responses of soil bacterial and fungal communities to extreme desiccation and rewetting
journal, July 2013

  • Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.104

Microbiomes in light of traits: A phylogenetic perspective
journal, November 2015


SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011

  • Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
  • Nature Methods, Vol. 8, Issue 10
  • DOI: 10.1038/nmeth.1701

Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups
journal, June 2012

  • Placella, S. A.; Brodie, E. L.; Firestone, M. K.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1204306109

Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010

  • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000080107

Litter chemistry influences decomposition through activity of specific microbial functional guilds
journal, May 2018

  • Bhatnagar, Jennifer M.; Peay, Kabir G.; Treseder, Kathleen K.
  • Ecological Monographs, Vol. 88, Issue 3
  • DOI: 10.1002/ecm.1303

Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition
journal, December 2000


Review of mechanisms and quantification of priming effects
journal, October 2000


GtRNAdb: a database of transfer RNA genes detected in genomic sequence
journal, January 2009

  • Chan, P. P.; Lowe, T. M.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn787

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Microgradients of Microbial Oxygen Consumption in a Barley Rhizosphere Model System
journal, January 1993


A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
journal, August 2018

  • Parks, Donovan H.; Chuvochina, Maria; Waite, David W.
  • Nature Biotechnology, Vol. 36, Issue 10
  • DOI: 10.1038/nbt.4229

New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities
journal, July 2012


FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


Rhizosphere microbiome assemblage is affected by plant development
journal, November 2013

  • Chaparro, Jacqueline M.; Badri, Dayakar V.; Vivanco, Jorge M.
  • The ISME Journal, Vol. 8, Issue 4
  • DOI: 10.1038/ismej.2013.196

Microbial hotspots and hot moments in soil: Concept & review
journal, April 2015


Patterns and Processes of Microbial Community Assembly
journal, September 2013

  • Nemergut, D. R.; Schmidt, S. K.; Fukami, T.
  • Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
  • DOI: 10.1128/MMBR.00051-12

ProDeGe: a computational protocol for fully automated decontamination of genomes
journal, June 2015

  • Tennessen, Kristin; Andersen, Evan; Clingenpeel, Scott
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.100

Genome-centric view of carbon processing in thawing permafrost
journal, July 2018


Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil
journal, April 2011


Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach
journal, November 2011

  • Tannock, Gerald W.; Wilson, Charlotte M.; Loach, Diane
  • The ISME Journal, Vol. 6, Issue 5
  • DOI: 10.1038/ismej.2011.161

Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling
journal, February 2018

  • López-Mondéjar, Ruben; Brabcová, Vendula; Štursová, Martina
  • The ISME Journal, Vol. 12, Issue 7
  • DOI: 10.1038/s41396-018-0084-2

Function and functional redundancy in microbial systems
journal, April 2018

  • Louca, Stilianos; Polz, Martin F.; Mazel, Florent
  • Nature Ecology & Evolution, Vol. 2, Issue 6
  • DOI: 10.1038/s41559-018-0519-1

Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology
journal, June 2015


Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass
journal, May 2016

  • Nuccio, Erin E.; Anderson-Furgeson, James; Estera, Katerina Y.
  • Ecology, Vol. 97, Issue 5
  • DOI: 10.1890/15-0882.1

SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Identification of microbial populations driving biopolymer degradation in acidic peatlands by metatranscriptomic analysis
journal, September 2016

  • Ivanova, Anastasia A.; Wegner, Carl-Eric; Kim, Yongkyu
  • Molecular Ecology, Vol. 25, Issue 19
  • DOI: 10.1111/mec.13806

Niche and host-associated functional signatures of the root surface microbiome
journal, September 2014

  • Ofek-Lalzar, Maya; Sela, Noa; Goldman-Voronov, Milana
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5950

Bacterial community assembly based on functional genes rather than species
journal, August 2011

  • Burke, C.; Steinberg, P.; Rusch, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 34
  • DOI: 10.1073/pnas.1101591108

Genomic Potential for Polysaccharide Deconstruction in Bacteria
journal, December 2014

  • Berlemont, Renaud; Martiny, Adam C.
  • Applied and Environmental Microbiology, Vol. 81, Issue 4
  • DOI: 10.1128/AEM.03718-14

A new view of the tree of life
journal, April 2016


QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Transfer of Bacteroides succinogenes (Hungate) to Fibrobacter gen. nov. as Fibrobacter succinogenes comb. nov. and Description of Fibrobacter intestinalis sp. nov.
journal, October 1988

  • Montgomery, L.; Flesher, B.; Stahl, D.
  • International Journal of Systematic Bacteriology, Vol. 38, Issue 4
  • DOI: 10.1099/00207713-38-4-430

Commentary: Oil degradation and biosurfactant production by the deep sea bacterium Dietzia maris As-13-3
journal, January 2016

  • Rahman, Pattanathu K. S. M.; Sekhon Randhawa, Kamaljeet K.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01557

Emergent simplicity in microbial community assembly
journal, August 2018


Genome Sequence of the Verrucomicrobium Opitutus terrae PB90-1, an Abundant Inhabitant of Rice Paddy Soil Ecosystems
journal, March 2011

  • van Passel, M. W. J.; Kant, R.; Palva, A.
  • Journal of Bacteriology, Vol. 193, Issue 9
  • DOI: 10.1128/JB.00228-11

Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon
journal, July 2018


NCBI BLAST: a better web interface
journal, May 2008

  • Johnson, M.; Zaretskaya, I.; Raytselis, Y.
  • Nucleic Acids Research, Vol. 36, Issue Web Server
  • DOI: 10.1093/nar/gkn201

The priming effect of organic matter: a question of microbial competition?
journal, June 2003


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
journal, October 2017

  • Wang, Kefeng; Peng, Changhui; Zhu, Qiuan
  • Journal of Advances in Modeling Earth Systems, Vol. 9, Issue 6
  • DOI: 10.1002/2017MS000920

The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016

  • Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
  • Ecology Letters, Vol. 19, Issue 8
  • DOI: 10.1111/ele.12630

Mapping of Sugar and Amino Acid Availability in Soil around Roots with Bacterial Sensors of Sucrose and Tryptophan
journal, January 1999


Genomic and Physiological Characterization of the Verrucomicrobia Isolate Diplosphaera colitermitum gen. nov., sp. nov., Reveals Microaerophily and Nitrogen Fixation Genes
journal, December 2011

  • Wertz, John T.; Kim, Eunji; Breznak, John A.
  • Applied and Environmental Microbiology, Vol. 78, Issue 5
  • DOI: 10.1128/AEM.06466-11

The Ecology of Soil Carbon: Pools, Vulnerabilities, and Biotic and Abiotic Controls
journal, November 2017


Carbon input by roots into the soil: Quantification of rhizodeposition from root to ecosystem scale
journal, September 2017

  • Pausch, Johanna; Kuzyakov, Yakov
  • Global Change Biology, Vol. 24, Issue 1
  • DOI: 10.1111/gcb.13850

Phylogenetic Distribution of Potential Cellulases in Bacteria
journal, December 2012

  • Berlemont, Renaud; Martiny, Adam C.
  • Applied and Environmental Microbiology, Vol. 79, Issue 5
  • DOI: 10.1128/AEM.03305-12

Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere
journal, August 2016

  • Yan, Yan; Kuramae, Eiko E.; de Hollander, Mattias
  • The ISME Journal, Vol. 11, Issue 1
  • DOI: 10.1038/ismej.2016.108

Disentangling carbon flow across microbial kingdoms in the rhizosphere of maize
journal, July 2019


Selective progressive response of soil microbial community to wild oat roots
journal, November 2008

  • DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z.
  • The ISME Journal, Vol. 3, Issue 2
  • DOI: 10.1038/ismej.2008.103

An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011

  • McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
  • The ISME Journal, Vol. 6, Issue 3
  • DOI: 10.1038/ismej.2011.139

Rebuilding community ecology from functional traits
journal, April 2006


Stimulation of Different Functional Groups of Bacteria by Various Plant Residues as a Driver of Soil Priming Effect
journal, February 2013


Transcriptional interactions suggest niche segregation among microorganisms in the human gut
journal, August 2016

  • Plichta, Damian Rafal; Juncker, Agnieszka Sierakowska; Bertalan, Marcelo
  • Nature Microbiology, Vol. 1, Issue 11
  • DOI: 10.1038/nmicrobiol.2016.152

Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls
journal, November 2016

  • Kallenbach, Cynthia M.; Frey, Serita D.; Grandy, A. Stuart
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13630

Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface
journal, January 2018

  • Probst, Alexander J.; Ladd, Bethany; Jarett, Jessica K.
  • Nature Microbiology, Vol. 3, Issue 3
  • DOI: 10.1038/s41564-017-0098-y

dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012

  • Yin, Yanbin; Mao, Xizeng; Yang, Jincai
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks479

Bacterial quorum sensing and nitrogen cycling in rhizosphere soil: Bacterial QS and rhizosphere nitrogen cycling
journal, November 2008


Genomic features of bacterial adaptation to plants
journal, December 2017

  • Levy, Asaf; Salas Gonzalez, Isai; Mittelviefhaus, Maximilian
  • Nature Genetics, Vol. 50, Issue 1
  • DOI: 10.1038/s41588-017-0012-9

Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation
journal, February 2005

  • Rasse, Daniel P.; Rumpel, Cornelia; Dignac, Marie-France
  • Plant and Soil, Vol. 269, Issue 1-2
  • DOI: 10.1007/s11104-004-0907-y

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Causes and consequences of biological diversity in soil
journal, January 2002


Bacterial reference genes for gene expression studies by RT-qPCR: survey and analysis
journal, July 2015

  • Rocha, Danilo J. P.; Santos, Carolina S.; Pacheco, Luis G. C.
  • Antonie van Leeuwenhoek, Vol. 108, Issue 3
  • DOI: 10.1007/s10482-015-0524-1

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Taxonomical and functional microbial community selection in soybean rhizosphere
journal, February 2014

  • Mendes, Lucas W.; Kuramae, Eiko E.; Navarrete, Acácio A.
  • The ISME Journal, Vol. 8, Issue 8
  • DOI: 10.1038/ismej.2014.17

Microbial formation of stable soil carbon is more efficient from belowground than aboveground input
journal, November 2018


Using stable isotopes to explore root-microbe-mineral interactions in soil
journal, June 2017


The Limiting Similarity, Convergence, and Divergence of Coexisting Species
journal, September 1967

  • Macarthur, Robert; Levins, Richard
  • The American Naturalist, Vol. 101, Issue 921
  • DOI: 10.1086/282505

Cephaloticoccus gen. nov., a new genus of ‘Verrucomicrobia’ containing two novel species isolated from Cephalotes ant guts
journal, August 2016

  • Lin, Jonathan Y.; Russell, Jacob A.; Sanders, Jon G.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 8
  • DOI: 10.1099/ijsem.0.001141

Microbial expression profiles in the rhizosphere of willows depend on soil contamination
journal, September 2013

  • Yergeau, Etienne; Sanschagrin, Sylvie; Maynard, Christine
  • The ISME Journal, Vol. 8, Issue 2
  • DOI: 10.1038/ismej.2013.163

The Niche Exploitation Pattern of the Blue-Gray Gnatcatcher
journal, February 1967

  • Root, Richard B.
  • Ecological Monographs, Vol. 37, Issue 4
  • DOI: 10.2307/1942327

Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

tRNADB-CE 2011: tRNA gene database curated manually by experts
journal, November 2010

  • Abe, T.; Ikemura, T.; Sugahara, J.
  • Nucleic Acids Research, Vol. 39, Issue Database
  • DOI: 10.1093/nar/gkq1007

Oligonucleotide Microarray for the Study of Functional Gene Diversity in the Nitrogen Cycle in the Environment
journal, February 2003


Manipulating the soil microbiome to increase soil health and plant fertility
journal, May 2012

  • Chaparro, Jacqueline M.; Sheflin, Amy M.; Manter, Daniel K.
  • Biology and Fertility of Soils, Vol. 48, Issue 5
  • DOI: 10.1007/s00374-012-0691-4

Microbial control over carbon cycling in soil
journal, January 2012


Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics
journal, April 2014


IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes
journal, October 2018

  • Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky901

Combining multiple functional annotation tools increases coverage of metabolic annotation
journal, December 2018


Identification of Cellulose-Responsive Bacterial and Fungal Communities in Geographically and Edaphically Different Soils by Using Stable Isotope Probing
journal, January 2012

  • Eichorst, Stephanie A.; Kuske, Cheryl R.
  • Applied and Environmental Microbiology, Vol. 78, Issue 7
  • DOI: 10.1128/AEM.07313-11

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

  • Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13219

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Synthesis and modeling perspectives of rhizosphere priming
journal, August 2013

  • Cheng, Weixin; Parton, William J.; Gonzalez-Meler, Miquel A.
  • New Phytologist, Vol. 201, Issue 1
  • DOI: 10.1111/nph.12440

Plant coexistence and the niche
journal, November 2004


Sizing up metatranscriptomics
journal, August 2012

  • Moran, Mary Ann; Satinsky, Brandon; Gifford, Scott M.
  • The ISME Journal, Vol. 7, Issue 2
  • DOI: 10.1038/ismej.2012.94

Predictive genomic traits for bacterial growth in culture versus actual growth in soil
journal, May 2019


Microbial community assembly differs across minerals in a rhizosphere microcosm
journal, September 2018

  • Whitman, Thea; Neurath, Rachel; Perera, Adele
  • Environmental Microbiology, Vol. 20, Issue 12
  • DOI: 10.1111/1462-2920.14366

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems
journal, March 2008