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Title: Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere

Abstract

Assigning a functional role to a microorganism has historically relied on cultivation of isolates or detection of environmental genome-based biomarkers using a posteriori knowledge of function. However, the emerging field of function-driven single-cell genomics aims to expand this paradigm by identifying and capturing individual microbes based on their in situ functions or traits. To identify and characterize yet uncultivated microbial taxa involved in cellulose degradation, we developed and benchmarked a function-driven single-cell screen, which we applied to a microbial community inhabiting the Great Boiling Spring (GBS) Geothermal Field, northwest Nevada. Our approach involved recruiting microbes to fluorescently labeled cellulose particles, and then isolating single microbe-bound particles via fluorescence-activated cell sorting. The microbial community profiles prior to sorting were determined via bulk sample 16S rRNA gene amplicon sequencing. The flow-sorted cellulose-bound microbes were subjected to whole genome amplification and shotgun sequencing, followed by phylogenetic placement. Next, putative cellulase genes were identified, expressed and tested for activity against derivatives of cellulose and xylose. Alongside typical cellulose degraders, including members of the Actinobacteria, Bacteroidetes, and Chloroflexi, we found divergent cellulases encoded in the genome of a recently described candidate phylum from the rare biosphere, Goldbacteria, and validated their cellulase activity. As this genomemore » represents a species-level organism with novel and phylogenetically distinct cellulolytic activity, we propose the name Candidatus ‘Cellulosimonas argentiregionis’. We expect that this function-driven single-cell approach can be extended to a broad range of substrates, linking microbial taxonomy directly to in situ function.« less

Authors:
 [1];  [1]; ORCiD logo [1];  [2];  [3];  [1];  [4];  [4]; ORCiD logo [4];  [1]; ORCiD logo [5]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]; ORCiD logo [5]; ORCiD logo [8]
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  4. Univ. of Wisconsin, Madison, WI (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Univ. of Nevada, Las Vegas, NV (United States)
  7. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Merced, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Joint BioEnergy Institute (JBEI), Emeryville, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1609108
Alternate Identifier(s):
OSTI ID: 1579340
Grant/Contract Number:  
AC02-05CH11231; SC0018409; FC02- 07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 14; Journal Issue: 3; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Doud, Devin F. R., Bowers, Robert M., Schulz, Frederik, De Raad, Markus, Deng, Kai, Tarver, Angela, Glasgow, Evan, Vander Meulen, Kirk, Fox, Brian, Deutsch, Sam, Yoshikuni, Yasuo, Northen, Trent, Hedlund, Brian P., Singer, Steven W., Ivanova, Natalia, and Woyke, Tanja. Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere. United States: N. p., 2019. Web. https://doi.org/10.1038/s41396-019-0557-y.
Doud, Devin F. R., Bowers, Robert M., Schulz, Frederik, De Raad, Markus, Deng, Kai, Tarver, Angela, Glasgow, Evan, Vander Meulen, Kirk, Fox, Brian, Deutsch, Sam, Yoshikuni, Yasuo, Northen, Trent, Hedlund, Brian P., Singer, Steven W., Ivanova, Natalia, & Woyke, Tanja. Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere. United States. https://doi.org/10.1038/s41396-019-0557-y
Doud, Devin F. R., Bowers, Robert M., Schulz, Frederik, De Raad, Markus, Deng, Kai, Tarver, Angela, Glasgow, Evan, Vander Meulen, Kirk, Fox, Brian, Deutsch, Sam, Yoshikuni, Yasuo, Northen, Trent, Hedlund, Brian P., Singer, Steven W., Ivanova, Natalia, and Woyke, Tanja. Thu . "Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere". United States. https://doi.org/10.1038/s41396-019-0557-y. https://www.osti.gov/servlets/purl/1609108.
@article{osti_1609108,
title = {Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere},
author = {Doud, Devin F. R. and Bowers, Robert M. and Schulz, Frederik and De Raad, Markus and Deng, Kai and Tarver, Angela and Glasgow, Evan and Vander Meulen, Kirk and Fox, Brian and Deutsch, Sam and Yoshikuni, Yasuo and Northen, Trent and Hedlund, Brian P. and Singer, Steven W. and Ivanova, Natalia and Woyke, Tanja},
abstractNote = {Assigning a functional role to a microorganism has historically relied on cultivation of isolates or detection of environmental genome-based biomarkers using a posteriori knowledge of function. However, the emerging field of function-driven single-cell genomics aims to expand this paradigm by identifying and capturing individual microbes based on their in situ functions or traits. To identify and characterize yet uncultivated microbial taxa involved in cellulose degradation, we developed and benchmarked a function-driven single-cell screen, which we applied to a microbial community inhabiting the Great Boiling Spring (GBS) Geothermal Field, northwest Nevada. Our approach involved recruiting microbes to fluorescently labeled cellulose particles, and then isolating single microbe-bound particles via fluorescence-activated cell sorting. The microbial community profiles prior to sorting were determined via bulk sample 16S rRNA gene amplicon sequencing. The flow-sorted cellulose-bound microbes were subjected to whole genome amplification and shotgun sequencing, followed by phylogenetic placement. Next, putative cellulase genes were identified, expressed and tested for activity against derivatives of cellulose and xylose. Alongside typical cellulose degraders, including members of the Actinobacteria, Bacteroidetes, and Chloroflexi, we found divergent cellulases encoded in the genome of a recently described candidate phylum from the rare biosphere, Goldbacteria, and validated their cellulase activity. As this genome represents a species-level organism with novel and phylogenetically distinct cellulolytic activity, we propose the name Candidatus ‘Cellulosimonas argentiregionis’. We expect that this function-driven single-cell approach can be extended to a broad range of substrates, linking microbial taxonomy directly to in situ function.},
doi = {10.1038/s41396-019-0557-y},
journal = {The ISME Journal},
number = 3,
volume = 14,
place = {United States},
year = {2019},
month = {11}
}

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Works referenced in this record:

Anvi’o: an advanced analysis and visualization platform for ‘omics data
journal, January 2015

  • Eren, A. Murat; Esen, Özcan C.; Quince, Christopher
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.1319

Ecology and exploration of the rare biosphere
journal, March 2015

  • Lynch, Michael D. J.; Neufeld, Josh D.
  • Nature Reviews Microbiology, Vol. 13, Issue 4
  • DOI: 10.1038/nrmicro3400

Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community
journal, July 2007

  • Robert, C.; Chassard, C.; Lawson, P. A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 7
  • DOI: 10.1099/ijs.0.64998-0

Cellulases: ambiguous nonhomologous enzymes in a genomic perspective
journal, October 2011


Novel High-Rank Phylogenetic Lineages within a Sulfur Spring (Zodletone Spring, Oklahoma), Revealed Using a Combined Pyrosequencing-Sanger Approach
journal, February 2012

  • Youssef, Noha; Steidley, Brandi L.; Elshahed, Mostafa S.
  • Applied and Environmental Microbiology, Vol. 78, Issue 8
  • DOI: 10.1128/AEM.00002-12

Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

Genomics of Aerobic Cellulose Utilization Systems in Actinobacteria
journal, June 2012


Periplasmic Cytophaga hutchinsonii Endoglucanases Are Required for Use of Crystalline Cellulose as the Sole Source of Carbon and Energy
journal, June 2016

  • Zhu, Yongtao; Han, Lanlan; Hefferon, Kathleen L.
  • Applied and Environmental Microbiology, Vol. 82, Issue 15
  • DOI: 10.1128/AEM.01298-16

Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
journal, August 2017

  • Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas
  • Nature Biotechnology, Vol. 35, Issue 8
  • DOI: 10.1038/nbt.3893

Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity
journal, September 1998


Active Site and Laminarin Binding in Glycoside Hydrolase Family 55
journal, March 2015

  • Bianchetti, Christopher M.; Takasuka, Taichi E.; Deutsch, Sam
  • Journal of Biological Chemistry, Vol. 290, Issue 19
  • DOI: 10.1074/jbc.M114.623579

RNAmmer: consistent and rapid annotation of ribosomal RNA genes
journal, April 2007

  • Lagesen, Karin; Hallin, Peter; Rødland, Einar Andreas
  • Nucleic Acids Research, Vol. 35, Issue 9
  • DOI: 10.1093/nar/gkm160

Rapid Kinetic Characterization of Glycosyl Hydrolases Based on Oxime Derivatization and Nanostructure-Initiator Mass Spectrometry (NIMS)
journal, May 2014

  • Deng, Kai; Takasuka, Taichi E.; Heins, Richard
  • ACS Chemical Biology, Vol. 9, Issue 7
  • DOI: 10.1021/cb5000289

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

Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


Characterization of All Family-9 Glycoside Hydrolases Synthesized by the Cellulosome-producing Bacterium Clostridium cellulolyticum
journal, January 2014

  • Ravachol, Julie; Borne, Romain; Tardif, Chantal
  • Journal of Biological Chemistry, Vol. 289, Issue 11
  • DOI: 10.1074/jbc.M113.545046

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Characterization of the cellulolytic complex (cellulosome) produced by Clostridium cellulolyticum.
journal, January 1997


Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs
journal, March 2004


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

Rare species contribute disproportionately to the functional structure of species assemblages
journal, April 2016

  • Leitão, Rafael P.; Zuanon, Jansen; Villéger, Sébastien
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1828
  • DOI: 10.1098/rspb.2016.0084

Identification and characterization of a multidomain hyperthermophilic cellulase from an archaeal enrichment
journal, July 2011

  • Graham, Joel E.; Clark, Melinda E.; Nadler, Dana C.
  • Nature Communications, Vol. 2, Issue 1
  • DOI: 10.1038/ncomms1373

Cellulosomal Scaffoldin-Like Proteins from Ruminococcus flavefaciens
journal, March 2001


Kallotenue papyrolyticum gen. nov., sp. nov., a cellulolytic and filamentous thermophile that represents a novel lineage (Kallotenuales ord. nov., Kallotenuaceae fam. nov.) within the class Chloroflexia
journal, August 2013

  • Cole, J. K.; Gieler, B. A.; Heisler, D. L.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 12
  • DOI: 10.1099/ijs.0.053348-0

Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments
journal, March 2017

  • Hernsdorf, Alex W.; Amano, Yuki; Miyakawa, Kazuya
  • The ISME Journal, Vol. 11, Issue 8
  • DOI: 10.1038/ismej.2017.39

Community Microrespirometry and Molecular Analyses Reveal a Diverse Energy Economy in Great Boiling Spring and Sandy's Spring West in the U.S. Great Basin
journal, March 2013

  • Murphy, Caitlin N.; Dodsworth, Jeremy A.; Babbitt, Aaron B.
  • Applied and Environmental Microbiology, Vol. 79, Issue 10
  • DOI: 10.1128/AEM.00139-13

Clostridium cellulolyticum : model organism of mesophilic cellulolytic clostridia
journal, September 2005


Uncultivated thermophiles: current status and spotlight on ‘Aigarchaeota’
journal, June 2015

  • Hedlund, Brian P.; Murugapiran, Senthil K.; Alba, Timothy W.
  • Current Opinion in Microbiology, Vol. 25
  • DOI: 10.1016/j.mib.2015.06.008

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


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


CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

OpenMSI Arrayed Analysis Toolkit: Analyzing Spatially Defined Samples Using Mass Spectrometry Imaging
journal, May 2017


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

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

Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia
journal, June 2016

  • Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 28
  • DOI: 10.1073/pnas.1603757113

IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014

  • Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
  • Molecular Biology and Evolution, Vol. 32, Issue 1
  • DOI: 10.1093/molbev/msu300

Horizontal Gene Transfer as an Indispensable Driver for Evolution of Neocallimastigomycota into a Distinct Gut-Dwelling Fungal Lineage
journal, May 2019

  • Murphy, Chelsea L.; Youssef, Noha H.; Hanafy, Radwa A.
  • Applied and Environmental Microbiology, Vol. 85, Issue 15
  • DOI: 10.1128/AEM.00988-19

SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes
journal, May 2012


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

Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea
journal, January 2013

  • Yelton, Alexis P.; Comolli, Luis R.; Justice, Nicholas B.
  • BMC Genomics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2164-14-485

Decontamination of MDA Reagents for Single Cell Whole Genome Amplification
journal, October 2011


Where less may be more: how the rare biosphere pulls ecosystems strings
journal, January 2017

  • Jousset, Alexandre; Bienhold, Christina; Chatzinotas, Antonis
  • The ISME Journal, Vol. 11, Issue 4
  • DOI: 10.1038/ismej.2016.174

ARB: a software environment for sequence data
journal, February 2004


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

Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia
journal, April 2012


Stable isotope probing — linking microbial identity to function
journal, May 2005

  • Dumont, Marc G.; Murrell, J. Colin
  • Nature Reviews Microbiology, Vol. 3, Issue 6
  • DOI: 10.1038/nrmicro1162

trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

Genomics of cellulosic biofuels
journal, August 2008


Deletion of the Cytophaga hutchinsonii type IX secretion system gene sprP results in defects in gliding motility and cellulose utilization
journal, November 2013


Pyrosequencing Reveals High-Temperature Cellulolytic Microbial Consortia in Great Boiling Spring after In Situ Lignocellulose Enrichment
journal, March 2013


An automated Raman-based platform for the sorting of live cells by functional properties
journal, March 2019

  • Lee, Kang Soo; Palatinszky, Márton; Pereira, Fátima C.
  • Nature Microbiology, Vol. 4, Issue 6
  • DOI: 10.1038/s41564-019-0394-9

Tracking heavy water (D 2 O) incorporation for identifying and sorting active microbial cells
journal, December 2014

  • Berry, David; Mader, Esther; Lee, Tae Kwon
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
  • DOI: 10.1073/pnas.1420406112

Genome Sequence of the Cellulolytic Gliding Bacterium Cytophaga hutchinsonii
journal, March 2007

  • Xie, G.; Bruce, D. C.; Challacombe, J. F.
  • Applied and Environmental Microbiology, Vol. 73, Issue 11
  • DOI: 10.1128/AEM.00225-07

High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries
journal, November 2018


Stable isotope probing in the metagenomics era: A bridge towards improved bioremediation
journal, March 2013


Genomic Analysis of "Elusimicrobium minutum," the First Cultivated Representative of the Phylum "Elusimicrobia" (Formerly Termite Group 1)
journal, March 2009

  • Herlemann, D. P. R.; Geissinger, O.; Ikeda-Ohtsubo, W.
  • Applied and Environmental Microbiology, Vol. 75, Issue 9
  • DOI: 10.1128/AEM.02698-08

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


Biomass pretreatment: Fundamentals toward application
journal, November 2011


ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data
journal, September 2016

  • Yu, Guangchuang; Smith, David K.; Zhu, Huachen
  • Methods in Ecology and Evolution, Vol. 8, Issue 1
  • DOI: 10.1111/2041-210X.12628

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

Novel approaches in function-driven single-cell genomics
journal, June 2017


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

Microfluidic-based mini-metagenomics enables discovery of novel microbial lineages from complex environmental samples
journal, July 2017


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

Pfam: the protein families database
journal, November 2013

  • Finn, Robert D.; Bateman, Alex; Clements, Jody
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1223

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

Genome Sequence of the Polysaccharide-Degrading, Thermophilic Anaerobe Spirochaeta thermophila DSM 6192
journal, October 2010

  • Angelov, A.; Liebl, S.; Ballschmiter, M.
  • Journal of Bacteriology, Vol. 192, Issue 24
  • DOI: 10.1128/JB.01023-10

Clathrate nanostructures for mass spectrometry
journal, October 2007

  • Northen, Trent R.; Yanes, Oscar; Northen, Michael T.
  • Nature, Vol. 449, Issue 7165
  • DOI: 10.1038/nature06195

The Sequence Alignment/Map format and SAMtools
journal, June 2009


Cellulases and their interaction with cellulose
journal, September 1994


Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment
journal, August 2013

  • Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3120

Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae)
journal, May 2003


Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs
journal, January 2016

  • Eloe-Fadrosh, Emiley A.; Paez-Espino, David; Jarett, Jessica
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10476

Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles
journal, July 2017

  • Stepanauskas, Ramunas; Fergusson, Elizabeth A.; Brown, Joseph
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-00128-z

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    journal, February 2020

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    • Nature Reviews Microbiology, Vol. 18, Issue 4
    • DOI: 10.1038/s41579-020-0323-1