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

Title: Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil

Abstract

ABSTRACT Soil ecosystems harbor diverse microorganisms and yet remain only partially characterized as neither single-cell sequencing nor whole-community sequencing offers a complete picture of these complex communities. Thus, the genetic and metabolic potential of this “uncultivated majority” remains underexplored. To address these challenges, we applied a pooled-cell-sorting-based mini-metagenomics approach and compared the results to bulk metagenomics. Informatic binning of these data produced 200 mini-metagenome assembled genomes (sorted-MAGs) and 29 bulk metagenome assembled genomes (MAGs). The sorted and bulk MAGs increased the known phylogenetic diversity of soil taxa by 7.2% with respect to the Joint Genome Institute IMG/M database and showed clade-specific sequence recruitment patterns across diverse terrestrial soil metagenomes. Additionally, sorted-MAGs expanded the rare biosphere not captured through MAGs from bulk sequences, exemplified through phylogenetic and functional analyses of members of the phylum Bacteroidetes . Analysis of 67 Bacteroidetes sorted-MAGs showed conserved patterns of carbon metabolism across four clades. These results indicate that mini-metagenomics enables genome-resolved investigation of predicted metabolism and demonstrates the utility of combining metagenomics methods to tap into the diversity of heterogeneous microbial assemblages. IMPORTANCE Microbial ecologists have historically used cultivation-based approaches as well as amplicon sequencing and shotgun metagenomics to characterize microbial diversity in soil. However,more » challenges persist in the study of microbial diversity, including the recalcitrance of the majority of microorganisms to laboratory cultivation and limited sequence assembly from highly complex samples. The uncultivated majority thus remains a reservoir of untapped genetic diversity. To address some of the challenges associated with bulk metagenomics as well as low throughput of single-cell genomics, we applied flow cytometry-enabled mini-metagenomics to capture expanded microbial diversity from forest soil and compare it to soil bulk metagenomics. Our resulting data from this pooled-cell sorting approach combined with bulk metagenomics revealed increased phylogenetic diversity through novel soil taxa and rare biosphere members. In-depth analysis of genomes within the highly represented Bacteroidetes phylum provided insights into conserved and clade-specific patterns of carbon metabolism.« less


Citation Formats

Alteio, L. V., Schulz, F., Seshadri, R., Varghese, N., Rodriguez-Reillo, W., Ryan, E., Goudeau, D., Eichorst, S. A., Malmstrom, R. R., Bowers, R. M., Katz, L. A., Blanchard, J. L., Woyke, T., and Jansson, ed., Janet K. Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil. United States: N. p., 2020. Web. doi:10.1128/mSystems.00768-19.
Alteio, L. V., Schulz, F., Seshadri, R., Varghese, N., Rodriguez-Reillo, W., Ryan, E., Goudeau, D., Eichorst, S. A., Malmstrom, R. R., Bowers, R. M., Katz, L. A., Blanchard, J. L., Woyke, T., & Jansson, ed., Janet K. Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil. United States. doi:10.1128/mSystems.00768-19.
Alteio, L. V., Schulz, F., Seshadri, R., Varghese, N., Rodriguez-Reillo, W., Ryan, E., Goudeau, D., Eichorst, S. A., Malmstrom, R. R., Bowers, R. M., Katz, L. A., Blanchard, J. L., Woyke, T., and Jansson, ed., Janet K. Tue . "Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil". United States. doi:10.1128/mSystems.00768-19.
@article{osti_1603713,
title = {Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil},
author = {Alteio, L. V. and Schulz, F. and Seshadri, R. and Varghese, N. and Rodriguez-Reillo, W. and Ryan, E. and Goudeau, D. and Eichorst, S. A. and Malmstrom, R. R. and Bowers, R. M. and Katz, L. A. and Blanchard, J. L. and Woyke, T. and Jansson, ed., Janet K.},
abstractNote = {ABSTRACT Soil ecosystems harbor diverse microorganisms and yet remain only partially characterized as neither single-cell sequencing nor whole-community sequencing offers a complete picture of these complex communities. Thus, the genetic and metabolic potential of this “uncultivated majority” remains underexplored. To address these challenges, we applied a pooled-cell-sorting-based mini-metagenomics approach and compared the results to bulk metagenomics. Informatic binning of these data produced 200 mini-metagenome assembled genomes (sorted-MAGs) and 29 bulk metagenome assembled genomes (MAGs). The sorted and bulk MAGs increased the known phylogenetic diversity of soil taxa by 7.2% with respect to the Joint Genome Institute IMG/M database and showed clade-specific sequence recruitment patterns across diverse terrestrial soil metagenomes. Additionally, sorted-MAGs expanded the rare biosphere not captured through MAGs from bulk sequences, exemplified through phylogenetic and functional analyses of members of the phylum Bacteroidetes . Analysis of 67 Bacteroidetes sorted-MAGs showed conserved patterns of carbon metabolism across four clades. These results indicate that mini-metagenomics enables genome-resolved investigation of predicted metabolism and demonstrates the utility of combining metagenomics methods to tap into the diversity of heterogeneous microbial assemblages. IMPORTANCE Microbial ecologists have historically used cultivation-based approaches as well as amplicon sequencing and shotgun metagenomics to characterize microbial diversity in soil. However, challenges persist in the study of microbial diversity, including the recalcitrance of the majority of microorganisms to laboratory cultivation and limited sequence assembly from highly complex samples. The uncultivated majority thus remains a reservoir of untapped genetic diversity. To address some of the challenges associated with bulk metagenomics as well as low throughput of single-cell genomics, we applied flow cytometry-enabled mini-metagenomics to capture expanded microbial diversity from forest soil and compare it to soil bulk metagenomics. Our resulting data from this pooled-cell sorting approach combined with bulk metagenomics revealed increased phylogenetic diversity through novel soil taxa and rare biosphere members. In-depth analysis of genomes within the highly represented Bacteroidetes phylum provided insights into conserved and clade-specific patterns of carbon metabolism.},
doi = {10.1128/mSystems.00768-19},
journal = {mSystems},
number = [2],
volume = [5],
place = {United States},
year = {2020},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1128/mSystems.00768-19

Save / Share:

Works referenced in this record:

Uncultivated microbes in need of their own taxonomy
journal, July 2017

  • Konstantinidis, Konstantinos T.; Rosselló-Móra, Ramon; Amann, Rudolf
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.113

After All, Only Millions?
journal, July 2016


Extreme genome reduction in symbiotic bacteria
journal, November 2011

  • McCutcheon, John P.; Moran, Nancy A.
  • Nature Reviews Microbiology, Vol. 10, Issue 1
  • DOI: 10.1038/nrmicro2670

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

Recovering complete and draft population genomes from metagenome datasets
journal, March 2016


The whole-soil carbon flux in response to warming
journal, March 2017


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

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


Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes?
journal, February 2016

  • Graham, Emily B.; Knelman, Joseph E.; Schindlbacher, Andreas
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00214

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

Toward Accurate and Quantitative Comparative Metagenomics
journal, August 2016


Cultivation of unculturable soil bacteria
journal, September 2012


Focused Metabolism of β-Glucans by the Soil Bacteroidetes Species Chitinophaga pinensis
journal, November 2018

  • McKee, Lauren S.; Martínez-Abad, Antonio; Ruthes, Andrea C.
  • Applied and Environmental Microbiology, Vol. 85, Issue 2
  • DOI: 10.1128/AEM.02231-18

Present and Future of Culturing Bacteria
journal, September 2017


The Importance of Revisiting Legionellales Diversity
journal, December 2018

  • Duron, Olivier; Doublet, Patricia; Vavre, Fabrice
  • Trends in Parasitology, Vol. 34, Issue 12
  • DOI: 10.1016/j.pt.2018.09.008

FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection
journal, March 2018

  • Seshadri, Rekha; Leahy, Sinead C.; Attwood, Graeme T.
  • Nature Biotechnology, Vol. 36, Issue 4
  • DOI: 10.1038/nbt.4110

Chlamydia cell biology and pathogenesis
journal, April 2016

  • Elwell, Cherilyn; Mirrashidi, Kathleen; Engel, Joanne
  • Nature Reviews Microbiology, Vol. 14, Issue 6
  • DOI: 10.1038/nrmicro.2016.30

Complete Genome Sequence of “Candidatus Sulcia muelleri” ML, an Obligate Nutritional Symbiont of Maize Leafhopper ( Dalbulus maidis )
journal, January 2015


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


MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences
journal, March 2014

  • Luo, Chengwei; Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T.
  • Nucleic Acids Research, Vol. 42, Issue 8
  • DOI: 10.1093/nar/gku169

Embracing the unknown: disentangling the complexities of the soil microbiome
journal, August 2017


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

Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

Correcting for 16S rRNA gene copy numbers in microbiome surveys remains an unsolved problem
journal, February 2018


The future is now: single-cell genomics of bacteria and archaea
journal, May 2013


Adaptive seeds tame genomic sequence comparison
journal, January 2011


Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens
journal, February 2019

  • Berghuis, Bojk A.; Yu, Feiqiao Brian; Schulz, Frederik
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 11
  • DOI: 10.1073/pnas.1815631116

Microbial Extracellular Polymeric Substances: Ecological Function and Impact on Soil Aggregation
journal, July 2018

  • Costa, Ohana Y. A.; Raaijmakers, Jos M.; Kuramae, Eiko E.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.01636

MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002


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

The all-intracellular order Legionellales is unexpectedly diverse, globally distributed and lowly abundant
journal, September 2018

  • Graells, Tiscar; Ishak, Helena; Larsson, Madeleine
  • FEMS Microbiology Ecology, Vol. 94, Issue 12
  • DOI: 10.1093/femsec/fiy185

Giant viruses with an expanded complement of translation system components
journal, April 2017


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

The Dynamics and Time Scale of Ongoing Genomic Erosion in Symbiotic Bacteria
journal, January 2009


Reconstructing each cell's genome within complex microbial communities—dream or reality?
journal, January 2015


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

Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes
journal, May 2013

  • Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam
  • Nature Biotechnology, Vol. 31, Issue 6
  • DOI: 10.1038/nbt.2579

Soil-specific limitations for access and analysis of soil microbial communities by metagenomics: Limitations in soil metagenomics
journal, June 2011


Structure and function of enzymes acting on chitin and chitosan
journal, January 2010

  • Hoell, Ingunn A.; Vaaje-Kolstad, Gustav; Eijsink, Vincent G. H.
  • Biotechnology and Genetic Engineering Reviews, Vol. 27, Issue 1
  • DOI: 10.1080/02648725.2010.10648156

Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae
journal, March 2015


Acclimatization of soil respiration to warming in a tall grass prairie
journal, October 2001

  • Luo, Yiqi; Wan, Shiqiang; Hui, Dafeng
  • Nature, Vol. 413, Issue 6856
  • DOI: 10.1038/35098065

Relic DNA is abundant in soil and obscures estimates of soil microbial diversity
journal, December 2016


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

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


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

Back to the Future of Soil Metagenomics
journal, February 2016


Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum
journal, June 2013

  • McLean, J. S.; Lombardo, M. -J.; Badger, J. H.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 26
  • DOI: 10.1073/pnas.1219809110

Long-term forest soil warming alters microbial communities in temperate forest soils
journal, February 2015

  • DeAngelis, Kristen M.; Pold, Grace; TopçuoÄŸlu, Begüm D.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00104

Potential for primary productivity in a globally-distributed bacterial phototroph
journal, March 2018


Micro-scale determinants of bacterial diversity in soil
journal, November 2013

  • Vos, Michiel; Wolf, Alexandra B.; Jennings, Sarah J.
  • FEMS Microbiology Reviews, Vol. 37, Issue 6
  • DOI: 10.1111/1574-6976.12023

Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life
journal, September 2017

  • Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria
  • Nature Microbiology, Vol. 2, Issue 11
  • DOI: 10.1038/s41564-017-0012-7

Strategies to improve reference databases for soil microbiomes
journal, December 2016

  • Choi, Jinlyung; Yang, Fan; Stepanauskas, Ramunas
  • The ISME Journal, Vol. 11, Issue 4
  • DOI: 10.1038/ismej.2016.168

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

Giant Viruses of Amoebas: An Update
journal, March 2016


Functional characterization of polysaccharide utilization loci in the marine Bacteroidetes ‘Gramella forsetii’ KT0803
journal, February 2014

  • Kabisch, Antje; Otto, Andreas; König, Sten
  • The ISME Journal, Vol. 8, Issue 7
  • DOI: 10.1038/ismej.2014.4

Microbial diversity drives multifunctionality in terrestrial ecosystems
journal, January 2016

  • Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10541

Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments : Genomic insights into acidobacteria
journal, March 2018

  • Eichorst, Stephanie A.; Trojan, Daniela; Roux, Simon
  • Environmental Microbiology, Vol. 20, Issue 3
  • DOI: 10.1111/1462-2920.14043

A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea
journal, December 2009

  • Wu, Dongying; Hugenholtz, Philip; Mavromatis, Konstantinos
  • Nature, Vol. 462, Issue 7276
  • DOI: 10.1038/nature08656

Reconstructing rare soil microbial genomes using in situ enrichments and metagenomics
journal, April 2015


Comparative Genomics Suggests an Independent Origin of Cytoplasmic Incompatibility in Cardinium hertigii
journal, October 2012


Microbial mediation of carbon-cycle feedbacks to climate warming
journal, December 2011

  • Zhou, Jizhong; Xue, Kai; Xie, Jianping
  • Nature Climate Change, Vol. 2, Issue 2
  • DOI: 10.1038/nclimate1331

Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae
journal, August 2013

  • Lagkouvardos, Ilias; Weinmaier, Thomas; Lauro, Federico M.
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.142

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

Critical Assessment of Metagenome Interpretation—a benchmark of metagenomics software
journal, October 2017

  • Sczyrba, Alexander; Hofmann, Peter; Belmann, Peter
  • Nature Methods, Vol. 14, Issue 11
  • DOI: 10.1038/nmeth.4458

Extracellular DNA in natural environments: features, relevance and applications
journal, June 2018

  • Nagler, Magdalena; Insam, Heribert; Pietramellara, Giacomo
  • Applied Microbiology and Biotechnology, Vol. 102, Issue 15
  • DOI: 10.1007/s00253-018-9120-4

Single cell genomics: an individual look at microbes
journal, October 2012


Complete genome sequence of Chitinophaga pinensis type strain (UQM 2034T)
journal, February 2010

  • Glavina Del Rio, Tijana; Abt, Birte; Spring, Stefan
  • Standards in Genomic Sciences, Vol. 2, Issue 1
  • DOI: 10.4056/sigs.661199

Marine amoebae with cytoplasmic and perinuclear symbionts deeply branching in the Gammaproteobacteria
journal, August 2015

  • Schulz, Frederik; Tyml, Tomáš; Pizzetti, Ilaria
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep13381

Ecology of marine Bacteroidetes: a comparative genomics approach
journal, January 2013

  • Fernández-Gómez, Beatriz; Richter, Michael; Schüler, Margarete
  • The ISME Journal, Vol. 7, Issue 5
  • DOI: 10.1038/ismej.2012.169

BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences
journal, February 2016

  • Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae
  • Journal of Molecular Biology, Vol. 428, Issue 4
  • DOI: 10.1016/j.jmb.2015.11.006

The Underestimation of Global Microbial Diversity
journal, September 2016


The trajectory of microbial single-cell sequencing
journal, October 2017

  • Woyke, Tanja; Doud, Devin F. R.; Schulz, Frederik
  • Nature Methods, Vol. 14, Issue 11
  • DOI: 10.1038/nmeth.4469

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

Proteomic Dissection of the Cellulolytic Machineries Used by Soil-Dwelling Bacteroidetes
journal, November 2018


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

Chlamydiae as Symbionts in Eukaryotes
journal, October 2008


Accelerated Profile HMM Searches
journal, October 2011


Metagenomics uncovers gaps in amplicon-based detection of microbial diversity
journal, February 2016


Characterization of a 'Bacteroidetes' symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of 'Candidatus Cardinium hertigii'
journal, May 2004

  • Zchori-Fein, E.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 3
  • DOI: 10.1099/ijs.0.02957-0

Major New Microbial Groups Expand Diversity and Alter our Understanding of the Tree of Life
journal, March 2018


Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica
journal, November 2009


Hidden diversity of soil giant viruses
journal, November 2018


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


Soil Warming and Carbon-Cycle Feedbacks to the Climate System
journal, December 2002


Forest Soil Bacteria: Diversity, Involvement in Ecosystem Processes, and Response to Global Change
journal, April 2017

  • Lladó, Salvador; López-Mondéjar, Rubén; Baldrian, Petr
  • Microbiology and Molecular Biology Reviews, Vol. 81, Issue 2
  • DOI: 10.1128/MMBR.00063-16

Environmental and Gut Bacteroidetes: The Food Connection
journal, January 2011

  • Thomas, François; Hehemann, Jan-Hendrik; Rebuffet, Etienne
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00093

Dividing the Large Glycoside Hydrolase Family 43 into Subfamilies: a Motivation for Detailed Enzyme Characterization
journal, January 2016

  • Mewis, Keith; Lenfant, Nicolas; Lombard, Vincent
  • Applied and Environmental Microbiology, Vol. 82, Issue 6
  • DOI: 10.1128/AEM.03453-15

MEGAN-LR: new algorithms allow accurate binning and easy interactive exploration of metagenomic long reads and contigs
journal, January 2018


The bright side of microbial dark matter: lessons learned from the uncultivated majority
journal, June 2016


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

Scaling laws predict global microbial diversity
journal, May 2016

  • Locey, Kenneth J.; Lennon, Jay T.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 21
  • DOI: 10.1073/pnas.1521291113

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


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


Use of Ichip for High-Throughput In Situ Cultivation of "Uncultivable" Microbial Species
journal, February 2010

  • Nichols, D.; Cahoon, N.; Trakhtenberg, E. M.
  • Applied and Environmental Microbiology, Vol. 76, Issue 8
  • DOI: 10.1128/AEM.01754-09

The Genome of the Amoeba Symbiont "Candidatus Amoebophilus asiaticus" Reveals Common Mechanisms for Host Cell Interaction among Amoeba-Associated Bacteria
journal, December 2009

  • Schmitz-Esser, S.; Tischler, P.; Arnold, R.
  • Journal of Bacteriology, Vol. 192, Issue 4
  • DOI: 10.1128/JB.01379-09