DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil

Abstract

The functioning, health, and productivity of soil are intimately tied to a complex network of interactions, particularly in plant root-associated rhizosphere soil. We conducted a stable-isotope-informed, genome-resolved metagenomic study to trace carbon from Avena fatua grown in a 13CO2 atmosphere into soil. We collected paired rhizosphere and nonrhizosphere soil at 6 and 9 weeks of plant growth and extracted DNA that was then separated by density using ultracentrifugation. Thirty-two fractions from each of five samples were grouped by density, sequenced, assembled, and binned to generate 55 unique bacterial genomes that were ≥70% complete. We also identified complete 18S rRNA sequences of several 13C-enriched microeukaryotic bacterivores and fungi. We generated 10 circularized bacteriophage (phage) genomes, some of which were the most labeled entities in the rhizosphere, suggesting that phage may be important agents of turnover of plant-derived C in soil. CRISPR locus targeting connected one of these phage to a Burkholderiales host predicted to be a plant pathogen. Another highly labeled phage is predicted to replicate in a Catenulispora sp., a possible plant growth-promoting bacterium. We searched the genome bins for traits known to be used in interactions involving bacteria, microeukaryotes, and plant roots and found DNA from heavily 13C-labeled bacterialmore » genes thought to be involved in modulating plant signaling hormones, plant pathogenicity, and defense against microeukaryote grazing. Stable-isotope-informed, genome-resolved metagenomics indicated that phage can be important agents of turnover of plant-derived carbon in soil. Plants grow in intimate association with soil microbial communities; these microbes can facilitate the availability of essential resources to plants. Thus, plant productivity commonly depends on interactions with rhizosphere bacteria, viruses, and eukaryotes. Our work is significant because we identified the organisms that took up plant-derived organic C in rhizosphere soil and determined that many of the active bacteria are plant pathogens or can impact plant growth via hormone modulation. Further, by showing that bacteriophage accumulate CO2-derived carbon, we demonstrated their vital roles in redistribution of plant-derived C into the soil environment through bacterial cell lysis. The use of stable-isotope probing (SIP) to identify consumption (or lack thereof) of root-derived C by key microbial community members within highly complex microbial communities opens the way for assessing manipulations of bacteria and phage with potentially beneficial and detrimental traits, ultimately providing a path to improved plant health and soil carbon storage.« less

Authors:
 [1];  [2];  [3];  [4];  [5]; ORCiD logo [4]; ORCiD logo [3]; ORCiD logo [6]; ORCiD logo [7];
  1. Department of Plant and Microbial Biology, University of California, Berkeley, California, USA
  2. Lincoln Science Centre, AgResearch Ltd., Christchurch, New Zealand
  3. Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USA
  4. Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA, Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, Arizona, USA
  5. Biofilm Center, University of Duisburg—Essen, Essen, Germany
  6. Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, USA, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, California, USA
  7. Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, USA, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, California, USA, Department of Earth and Planetary Science, University of California, Berkeley, California, USA, Innovative Genomics Institute, Berkeley, California, USA, Chan Zuckerberg Biohub, San Francisco, California, USA
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); German Science Foundation; National Science Foundation (NSF); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1818172
Alternate Identifier(s):
OSTI ID: 1855191; OSTI ID: 1867551
Report Number(s):
LLNL-JRNL-814137
Journal ID: ISSN 2379-5042; e00085-21
Grant/Contract Number:  
SC0010570; SC0016247; SC10010566; SC0020172; SCW1589; SCW1632; AC02-05CH11231; DFG1603-1/1; AC52-07NA27344; CZO EAR-1331940; SC0010566; EAR-1331940
Resource Type:
Published Article
Journal Name:
mSphere
Additional Journal Information:
Journal Name: mSphere Journal Volume: 6 Journal Issue: 5; Journal ID: ISSN 2379-5042
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; plant growth; labeling; density separation; sequencing; enrichment; growth; 58 GEOSCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 54 ENVIRONMENTAL SCIENCES

Citation Formats

Starr, Evan P., Shi, Shengjing, Blazewicz, Steven J., Koch, Benjamin J., Probst, Alexander J., Hungate, Bruce A., Pett-Ridge, Jennifer, Firestone, Mary K., Banfield, Jillian F., and Young, ed., Vincent B. Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil. United States: N. p., 2021. Web. doi:10.1128/mSphere.00085-21.
Starr, Evan P., Shi, Shengjing, Blazewicz, Steven J., Koch, Benjamin J., Probst, Alexander J., Hungate, Bruce A., Pett-Ridge, Jennifer, Firestone, Mary K., Banfield, Jillian F., & Young, ed., Vincent B. Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil. United States. https://doi.org/10.1128/mSphere.00085-21
Starr, Evan P., Shi, Shengjing, Blazewicz, Steven J., Koch, Benjamin J., Probst, Alexander J., Hungate, Bruce A., Pett-Ridge, Jennifer, Firestone, Mary K., Banfield, Jillian F., and Young, ed., Vincent B. Wed . "Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil". United States. https://doi.org/10.1128/mSphere.00085-21.
@article{osti_1818172,
title = {Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil},
author = {Starr, Evan P. and Shi, Shengjing and Blazewicz, Steven J. and Koch, Benjamin J. and Probst, Alexander J. and Hungate, Bruce A. and Pett-Ridge, Jennifer and Firestone, Mary K. and Banfield, Jillian F. and Young, ed., Vincent B.},
abstractNote = {The functioning, health, and productivity of soil are intimately tied to a complex network of interactions, particularly in plant root-associated rhizosphere soil. We conducted a stable-isotope-informed, genome-resolved metagenomic study to trace carbon from Avena fatua grown in a 13CO2 atmosphere into soil. We collected paired rhizosphere and nonrhizosphere soil at 6 and 9 weeks of plant growth and extracted DNA that was then separated by density using ultracentrifugation. Thirty-two fractions from each of five samples were grouped by density, sequenced, assembled, and binned to generate 55 unique bacterial genomes that were ≥70% complete. We also identified complete 18S rRNA sequences of several 13C-enriched microeukaryotic bacterivores and fungi. We generated 10 circularized bacteriophage (phage) genomes, some of which were the most labeled entities in the rhizosphere, suggesting that phage may be important agents of turnover of plant-derived C in soil. CRISPR locus targeting connected one of these phage to a Burkholderiales host predicted to be a plant pathogen. Another highly labeled phage is predicted to replicate in a Catenulispora sp., a possible plant growth-promoting bacterium. We searched the genome bins for traits known to be used in interactions involving bacteria, microeukaryotes, and plant roots and found DNA from heavily 13C-labeled bacterial genes thought to be involved in modulating plant signaling hormones, plant pathogenicity, and defense against microeukaryote grazing. Stable-isotope-informed, genome-resolved metagenomics indicated that phage can be important agents of turnover of plant-derived carbon in soil. Plants grow in intimate association with soil microbial communities; these microbes can facilitate the availability of essential resources to plants. Thus, plant productivity commonly depends on interactions with rhizosphere bacteria, viruses, and eukaryotes. Our work is significant because we identified the organisms that took up plant-derived organic C in rhizosphere soil and determined that many of the active bacteria are plant pathogens or can impact plant growth via hormone modulation. Further, by showing that bacteriophage accumulate CO2-derived carbon, we demonstrated their vital roles in redistribution of plant-derived C into the soil environment through bacterial cell lysis. The use of stable-isotope probing (SIP) to identify consumption (or lack thereof) of root-derived C by key microbial community members within highly complex microbial communities opens the way for assessing manipulations of bacteria and phage with potentially beneficial and detrimental traits, ultimately providing a path to improved plant health and soil carbon storage.},
doi = {10.1128/mSphere.00085-21},
journal = {mSphere},
number = 5,
volume = 6,
place = {United States},
year = {Wed Oct 27 00:00:00 EDT 2021},
month = {Wed Oct 27 00:00:00 EDT 2021}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/mSphere.00085-21

Save / Share:

Works referenced in this record:

NO way to live; the various roles of nitric oxide in plant–pathogen interactions
journal, December 2005

  • Mur, Luis A. J.; Carver, Tim L. W.; Prats, Elena
  • Journal of Experimental Botany, Vol. 57, Issue 3
  • DOI: 10.1093/jxb/erj052

Salicylic Acid Inhibits Pathogen Growth in Plants through Repression of the Auxin Signaling Pathway
journal, October 2007

  • Wang, Dong; Pajerowska-Mukhtar, Karolina; Culler, Angela Hendrickson
  • Current Biology, Vol. 17, Issue 20
  • DOI: 10.1016/j.cub.2007.09.025

Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil
journal, May 2014

  • Blazewicz, Steven J.; Schwartz, Egbert; Firestone, Mary K.
  • Ecology, Vol. 95, Issue 5
  • DOI: 10.1890/13-1031.1

Host-linked soil viral ecology along a permafrost thaw gradient
journal, July 2018


Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing
journal, October 2018


Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization
journal, August 2012

  • Sharon, I.; Morowitz, M. J.; Thomas, B. C.
  • Genome Research, Vol. 23, Issue 1
  • DOI: 10.1101/gr.142315.112

dbCAN2: a meta server for automated carbohydrate-active enzyme annotation
journal, May 2018

  • Zhang, Han; Yohe, Tanner; Huang, Le
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky418

Mechanisms of action of plant growth promoting bacteria
journal, October 2017

  • Olanrewaju, Oluwaseyi Samuel; Glick, Bernard R.; Babalola, Olubukola Oluranti
  • World Journal of Microbiology and Biotechnology, Vol. 33, Issue 11
  • DOI: 10.1007/s11274-017-2364-9

A viability-linked metagenomic analysis of cleanroom environments: eukarya, prokaryotes, and viruses
journal, December 2015


InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001


Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant Interactions
book, August 2020

  • Pett-Ridge, Jennifer; Shi, Shengjing; Estera-Molina, Katerina
  • Rhizosphere Biology: Interactions Between Microbes and Plants
  • DOI: 10.1007/978-981-15-6125-2_2

Effect of mechanical damage on vigor, physiological parameters, and susceptibility of oat (Avena sativa) to Fusarium culmorum infection
journal, September 2011


Who's your neighbor? New computational approaches for functional genomics
journal, June 2000

  • Galperin, Michael Y.; Koonin, Eugene V.
  • Nature Biotechnology, Vol. 18, Issue 6
  • DOI: 10.1038/76443

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

Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants
journal, September 2015


Strong succession in arbuscular mycorrhizal fungal communities
journal, August 2018


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


MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015


VirSorter: mining viral signal from microbial genomic data
journal, January 2015

  • Roux, Simon; Enault, Francois; Hurwitz, Bonnie L.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.985

Graph Clustering Via a Discrete Uncoupling Process
journal, January 2008

  • Van Dongen, Stijn
  • SIAM Journal on Matrix Analysis and Applications, Vol. 30, Issue 1
  • DOI: 10.1137/040608635

antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences
journal, June 2011

  • Medema, Marnix H.; Blin, Kai; Cimermancic, Peter
  • Nucleic Acids Research, Vol. 39, Issue suppl_2
  • DOI: 10.1093/nar/gkr466

antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification
journal, April 2017

  • Blin, Kai; Wolf, Thomas; Chevrette, Marc G.
  • Nucleic Acids Research, Vol. 45, Issue W1
  • DOI: 10.1093/nar/gkx319

Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis
journal, July 2010

  • Bonfante, Paola; Genre, Andrea
  • Nature Communications, Vol. 1, Issue 1
  • DOI: 10.1038/ncomms1046

Notes on Methods for the Extraction of Small Soil Arthropods
journal, May 1953

  • Macfadyen, A.
  • The Journal of Animal Ecology, Vol. 22, Issue 1
  • DOI: 10.2307/1691

Quantitative Microbial Ecology through Stable Isotope Probing
journal, August 2015

  • Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert
  • Applied and Environmental Microbiology, Vol. 81, Issue 21
  • DOI: 10.1128/AEM.02280-15

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 1999

  • Ogata, H.; Goto, S.; Sato, K.
  • Nucleic Acids Research, Vol. 27, Issue 1
  • DOI: 10.1093/nar/27.1.29

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil
journal, November 2019

  • Starr, Evan P.; Nuccio, Erin E.; Pett-Ridge, Jennifer
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 51
  • DOI: 10.1073/pnas.1908291116

Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
journal, August 2015


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Stable isotope probing of bacterial community structure and gene expression in the rhizosphere of Arabidopsis thaliana
journal, March 2012


Microbial Phosphorus Solubilization and Its Potential for Use in Sustainable Agriculture
journal, June 2017

  • Alori, Elizabeth T.; Glick, Bernard R.; Babalola, Olubukola O.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.00971

Migratory Response of Soil Bacteria to Lyophyllum sp. Strain Karsten in Soil Microcosms
journal, March 2009

  • Warmink, J. A.; van Elsas, J. D.
  • Applied and Environmental Microbiology, Vol. 75, Issue 9
  • DOI: 10.1128/AEM.02110-08

CRISPRDetect: A flexible algorithm to define CRISPR arrays
journal, May 2016


Temporal changes of bacterial communities in the Tuber melanosporum ectomycorrhizosphere during ascocarp development
journal, January 2016


Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development
journal, March 2015


Heterotrophic growth of cyanobacteria and phage-mediated microbial loop in soil: Examination by stable isotope probing (SIP) method
journal, April 2012


Creating the CIPRES Science Gateway for inference of large phylogenetic trees
conference, November 2010

  • Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri
  • 2010 Gateway Computing Environments Workshop (GCE)
  • DOI: 10.1109/GCE.2010.5676129

UniProt Knowledgebase: a hub of integrated protein data
journal, January 2011


Structure and function of the global topsoil microbiome
journal, August 2018


Measurement Error and Resolution in Quantitative Stable Isotope Probing: Implications for Experimental Design
journal, August 2020


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


Stable-isotope probing and metagenomics reveal predation by protozoa drives E. coli removal in slow sand filters
journal, October 2014

  • Haig, Sarah-Jane; Schirmer, Melanie; D'Amore, Rosalinda
  • The ISME Journal, Vol. 9, Issue 4
  • DOI: 10.1038/ismej.2014.175

Characterization of an Insecticidal Toxin and Pathogenicity of Pseudomonas taiwanensis against Insects
journal, August 2014


HMMER web server: interactive sequence similarity searching
journal, May 2011

  • Finn, R. D.; Clements, J.; Eddy, S. R.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr367

A global atlas of the dominant bacteria found in soil
journal, January 2018

  • Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E.
  • Science, Vol. 359, Issue 6373
  • DOI: 10.1126/science.aap9516

Nematicidal Bacteria Associated to Pinewood Nematode Produce Extracellular Proteases
journal, November 2013


A Versatile Sample Processing Workflow for Metagenomic Pathogen Detection
journal, August 2018


Bacterial volatiles promote growth in Arabidopsis
journal, April 2003

  • Ryu, C. -M.; Farag, M. A.; Hu, C. -H.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
  • DOI: 10.1073/pnas.0730845100

Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone
journal, January 2016

  • Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F.
  • PeerJ, Vol. 4
  • DOI: 10.7717/peerj.2687

Accurate, multi-kb reads resolve complex populations and detect rare microorganisms
journal, February 2015

  • Sharon, Itai; Kertesz, Michael; Hug, Laura A.
  • Genome Research, Vol. 25, Issue 4
  • DOI: 10.1101/gr.183012.114

Accurate Estimation of Fungal Diversity and Abundance through Improved Lineage-Specific Primers Optimized for Illumina Amplicon Sequencing
journal, October 2016

  • Taylor, D. Lee; Walters, William A.; Lennon, Niall J.
  • Applied and Environmental Microbiology, Vol. 82, Issue 24
  • DOI: 10.1128/AEM.02576-16

Taxonomic Resolutions Based on 18S rRNA Genes: A Case Study of Subclass Copepoda
journal, June 2015


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


UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007


Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
journal, February 2015

  • Schubotz, Florence; Hays, Lindsay E.; Meyer-Dombard, D'Arcy R.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00042

Quantitative Analysis of Lysobacter Predation
journal, July 2015

  • Seccareccia, Ivana; Kost, Christian; Nett, Markus
  • Applied and Environmental Microbiology, Vol. 81, Issue 20
  • DOI: 10.1128/AEM.01781-15

GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants
journal, October 2006


Characterization of the 18S rRNA Gene for Designing Universal Eukaryote Specific Primers
journal, February 2014


Off the hook – how bacteria survive protozoan grazing
journal, July 2005


tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997


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

Estimating taxon‐specific population dynamics in diverse microbial communities
journal, January 2018

  • Koch, Benjamin J.; McHugh, Theresa A.; Hayer, Michaela
  • Ecosphere, Vol. 9, Issue 1
  • DOI: 10.1002/ecs2.2090

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


MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets
journal, October 2015


Belowground Response to Drought in a Tropical Forest Soil. I. Changes in Microbial Functional Potential and Metabolism
journal, April 2016


RNA-Based Stable Isotope Probing Suggests Allobaculum spp. as Particularly Active Glucose Assimilators in a Complex Murine Microbiota Cultured In Vitro
journal, January 2017

  • Herrmann, Elena; Young, Wayne; Rosendale, Douglas
  • BioMed Research International, Vol. 2017
  • DOI: 10.1155/2017/1829685

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


Incorporation of plant residue-derived carbon into the microeukaryotic community in a rice field soil revealed by DNA stable-isotope probing
journal, November 2011


Responses of soil microeukaryotic communities to short-term fumigation-incubation revealed by MiSeq amplicon sequencing
journal, October 2015


A high-efficiency, “low-technology” Tullgren-type extractor for soil microarthropods
journal, February 1991


Bacterial Secretion Systems: An Overview
journal, February 2016


Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy
journal, May 2018

  • Sieber, Christian M. K.; Probst, Alexander J.; Sharrar, Allison
  • Nature Microbiology, Vol. 3, Issue 7
  • DOI: 10.1038/s41564-018-0171-1

Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes
journal, June 2016


Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Niche differentiation is spatially and temporally regulated in the rhizosphere
journal, January 2020


IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis
journal, June 2018

  • Crits-Christoph, Alexander; Diamond, Spencer; Butterfield, Cristina N.
  • Nature, Vol. 558, Issue 7710
  • DOI: 10.1038/s41586-018-0207-y

Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria
journal, August 2015


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


A View to a Kill: The Bacterial Type VI Secretion System
journal, January 2014


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

Rhizosphere bacterial communities of dominant steppe plants shift in response to a gradient of simulated nitrogen deposition
journal, August 2015


Increased plant productivity and decreased microbial respiratory C loss by plant growth-promoting rhizobacteria under elevated CO2
journal, March 2015

  • Nie, Ming; Bell, Colin; Wallenstein, Matthew D.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep09212

Investigation of the microbial metabolism of carbon dioxide and hydrogen in the kangaroo foregut by stable isotope probing
journal, March 2014

  • Godwin, Scott; Kang, Alicia; Gulino, Lisa-Maree
  • The ISME Journal, Vol. 8, Issue 9
  • DOI: 10.1038/ismej.2014.25

The Ecological Role of Volatile and Soluble Secondary Metabolites Produced by Soil Bacteria
journal, April 2017


Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing
journal, September 2018


Control of Glucosylceramide Production and Morphogenesis by the Bar1 Ceramide Synthase in Fusarium graminearum
journal, April 2011


Metagenomic Analysis of the Bacterial Community Associated with the Taproot of Sugar Beet
journal, January 2015

  • Tsurumaru, Hirohito; Okubo, Takashi; Okazaki, Kazuyuki
  • Microbes and environments, Vol. 30, Issue 1
  • DOI: 10.1264/jsme2.ME14109

Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis
journal, April 2016

  • Esmaeel, Qassim; Pupin, Maude; Kieu, Nam Phuong
  • MicrobiologyOpen, Vol. 5, Issue 3
  • DOI: 10.1002/mbo3.347

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