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

Title: Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface

Abstract

Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, the Verrucomicrobia are underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of the Verrucomicrobia phylum by describing a novel genus, “Candidatus Marcellius,” belonging to the order Opitutales. “Ca. Marcellius” was recovered from a shale-derived produced fluid metagenome collected 313 days after hydraulic fracturing, the deepest environment from which a member of the Verrucomicrobia has been recovered to date. We uncover genomic attributes that may explain the capacity of this organism to inhabit a shale gas well, including the potential for utilization of organic polymers common in hydraulic fracturing fluids, nitrogen fixation, adaptation to high salinities, and adaptive immunity via CRISPR-Cas. To illuminate the phylogenetic and environmental distribution of these metabolic and adaptive traits across the Verrucomicrobia phylum, we performed a comparative genomic analysis of 31 publicly available, nearly complete Verrucomicrobia genomes. Our genomic findings extend the environmental distribution of the Verrucomicrobia 2.3 kilometers into the terrestrialmore » subsurface. Moreover, we reveal traits widely encoded across members of the Verrucomicrobia, including the capacity to degrade hemicellulose and to adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3];  [4];  [4]; ORCiD logo [5];  [2];  [2];  [6]
  1. Univ. of Manchester (United Kingdom)
  2. Colorado State Univ., Fort Collins, CO (United States)
  3. The Research Institute at Nationwide Children's Hospital, Columbus, OH (United States)
  4. The Ohio State Univ., Columbus, OH (United States)
  5. Univ. of New Hampshire, Durham, NH (United States)
  6. Univ. of Wisconsin, Madison, WI (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); West Virginia Univ., Morgantown, WV (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Energy Technology Laboratory (NETL); Natural Environment Research Council Research Fellowship; National Science Foundation (NSF)
OSTI Identifier:
1626160
Grant/Contract Number:  
AC02-05CH11231; FE0024297; NE/R013462/1; 1342701; EAR-1847684
Resource Type:
Accepted Manuscript
Journal Name:
mSphere
Additional Journal Information:
Journal Volume: 4; Journal Issue: 6; Journal ID: ISSN 2379-5042
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; microbiology; glycoside hydrolases; viruse; shale; hypersaline; hydraulic fracturing

Citation Formats

Nixon, Sophie L., Daly, Rebecca A., Borton, Mikayla A., Solden, Lindsey M., Welch, Susan A., Cole, David R., Mouser, Paula J., Wilkins, Michael J., Wrighton, Kelly C., and Suen, Garret. Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface. United States: N. p., 2019. Web. doi:10.1128/msphere.00613-19.
Nixon, Sophie L., Daly, Rebecca A., Borton, Mikayla A., Solden, Lindsey M., Welch, Susan A., Cole, David R., Mouser, Paula J., Wilkins, Michael J., Wrighton, Kelly C., & Suen, Garret. Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface. United States. https://doi.org/10.1128/msphere.00613-19
Nixon, Sophie L., Daly, Rebecca A., Borton, Mikayla A., Solden, Lindsey M., Welch, Susan A., Cole, David R., Mouser, Paula J., Wilkins, Michael J., Wrighton, Kelly C., and Suen, Garret. Wed . "Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface". United States. https://doi.org/10.1128/msphere.00613-19. https://www.osti.gov/servlets/purl/1626160.
@article{osti_1626160,
title = {Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface},
author = {Nixon, Sophie L. and Daly, Rebecca A. and Borton, Mikayla A. and Solden, Lindsey M. and Welch, Susan A. and Cole, David R. and Mouser, Paula J. and Wilkins, Michael J. and Wrighton, Kelly C. and Suen, Garret},
abstractNote = {Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, the Verrucomicrobia are underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of the Verrucomicrobia phylum by describing a novel genus, “Candidatus Marcellius,” belonging to the order Opitutales. “Ca. Marcellius” was recovered from a shale-derived produced fluid metagenome collected 313 days after hydraulic fracturing, the deepest environment from which a member of the Verrucomicrobia has been recovered to date. We uncover genomic attributes that may explain the capacity of this organism to inhabit a shale gas well, including the potential for utilization of organic polymers common in hydraulic fracturing fluids, nitrogen fixation, adaptation to high salinities, and adaptive immunity via CRISPR-Cas. To illuminate the phylogenetic and environmental distribution of these metabolic and adaptive traits across the Verrucomicrobia phylum, we performed a comparative genomic analysis of 31 publicly available, nearly complete Verrucomicrobia genomes. Our genomic findings extend the environmental distribution of the Verrucomicrobia 2.3 kilometers into the terrestrial subsurface. Moreover, we reveal traits widely encoded across members of the Verrucomicrobia, including the capacity to degrade hemicellulose and to adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum.},
doi = {10.1128/msphere.00613-19},
journal = {mSphere},
number = 6,
volume = 4,
place = {United States},
year = {Wed Dec 18 00:00:00 EST 2019},
month = {Wed Dec 18 00:00:00 EST 2019}
}

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

Citation Metrics:
Cited by: 23 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

An updated evolutionary classification of CRISPR–Cas systems
journal, September 2015

  • Makarova, Kira S.; Wolf, Yuri I.; Alkhnbashi, Omer S.
  • Nature Reviews Microbiology, Vol. 13, Issue 11, p. 722-736
  • DOI: 10.1038/nrmicro3569

Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia
text, January 2012

  • Gary, Xie,; K., Swan, Brandon; G., Chain, Patrick S.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/fzc0-xq44

Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula
journal, June 2020


Reconstruction of Diverse Verrucomicrobial Genomes from Metagenome Datasets of Freshwater Reservoirs
journal, November 2017

  • Cabello-Yeves, Pedro J.; Ghai, Rohit; Mehrshad, Maliheh
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02131

New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
journal, December 2016

  • Solden, Lindsey M.; Hoyt, David W.; Collins, William B.
  • The ISME Journal, Vol. 11, Issue 3
  • DOI: 10.1038/ismej.2016.150

Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2
journal, February 2012


Microbial Community Structure and Functional Potential Along a Hypersaline Gradient
journal, July 2018


A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
journal, September 2018

  • Vavourakis, Charlotte D.; Andrei, Adrian-Stefan; Mehrshad, Maliheh
  • Microbiome, Vol. 6, Issue 1
  • DOI: 10.1186/s40168-018-0548-7

Metagenomic De Novo Assembly of an Aquatic Representative of the Verrucomicrobial Class Spartobacteria
journal, May 2013

  • Herlemann, Daniel P. R.; Lundin, Daniel; Labrenz, Matthias
  • mBio, Vol. 4, Issue 3
  • DOI: 10.1128/mBio.00569-12

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

InterProScan: protein domains identifier
journal, July 2005

  • Quevillon, E.; Silventoinen, V.; Pillai, S.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki442

KAAS: an automatic genome annotation and pathway reconstruction server
journal, May 2007

  • Moriya, Y.; Itoh, M.; Okuda, S.
  • Nucleic Acids Research, Vol. 35, Issue S2, p. W182-W185
  • DOI: 10.1093/nar/gkm321

Gene and translation initiation site prediction in metagenomic sequences
journal, July 2012


Cerasicoccus arenae gen. nov., sp. nov., a carotenoid-producing marine representative of the family Puniceicoccaceae within the phylum ‘Verrucomicrobia’, isolated from marine sand
journal, September 2007

  • Yoon, Jaewoo; Matsuo, Yoshihide; Matsuda, Satoru
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 9
  • DOI: 10.1099/ijs.0.65102-0

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


Detection of Diazotrophy in the Acetylene-Fermenting Anaerobe Pelobacter sp. Strain SFB93
journal, June 2017

  • Akob, Denise M.; Baesman, Shaun M.; Sutton, John M.
  • Applied and Environmental Microbiology, Vol. 83, Issue 17
  • DOI: 10.1128/AEM.01198-17

Bacterial Communities Associated with Production Facilities of Two Newly Drilled Thermogenic Natural Gas Wells in the Barnett Shale (Texas, USA)
journal, May 2012

  • Davis, James P.; Struchtemeyer, Christopher G.; Elshahed, Mostafa S.
  • Microbial Ecology, Vol. 64, Issue 4
  • DOI: 10.1007/s00248-012-0073-3

New Strategies for Cultivation and Detection of Previously Uncultured Microbes
journal, August 2004


Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales
journal, September 2016


Classifying the uncultivated microbial majority: A place for metagenomic data in the Candidatus proposal
journal, June 2015

  • Konstantinidis, Konstantinos T.; Rosselló-Móra, Ramon
  • Systematic and Applied Microbiology, Vol. 38, Issue 4
  • DOI: 10.1016/j.syapm.2015.01.001

Ruficoccus amylovorans gen. nov., sp. nov., an amylolytic and nitrate-reducing diazotroph of the family Puniceicoccaceae
journal, April 2017

  • Lin, Shih-Yao; Hameed, Asif; Liu, You-Cheng
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 4
  • DOI: 10.1099/ijsem.0.001723

Biodegradation of polyacrylamide by bacteria isolated from activated sludge and oil-contaminated soil
journal, March 2010


EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data
journal, May 2011

  • Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C.
  • Genome Biology, Vol. 12, Issue 5
  • DOI: 10.1186/gb-2011-12-5-r44

Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
journal, October 2013


Microbial life at high salt concentrations: phylogenetic and metabolic diversity
journal, January 2008


The under-recognized dominance of Verrucomicrobia in soil bacterial communities
journal, July 2011


Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses
journal, September 2016

  • Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E.
  • Nature, Vol. 537, Issue 7622
  • DOI: 10.1038/nature19366

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

Limisphaera ngatamarikiensis gen. nov., sp. nov., a thermophilic, pink-pigmented coccus isolated from subaqueous mud of a geothermal hotspring
journal, April 2015

  • Anders, Heike; Power, Jean F.; MacKenzie, Andrew D.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue Pt_4
  • DOI: 10.1099/ijs.0.000063

Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium
journal, September 2004

  • Derrien, M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5
  • DOI: 10.1099/ijs.0.02873-0

Influence of the Drilling Mud Formulation Process on the Bacterial Communities in Thermogenic Natural Gas Wells of the Barnett Shale
journal, May 2011

  • Struchtemeyer, Christopher G.; Davis, James P.; Elshahed, Mostafa S.
  • Applied and Environmental Microbiology, Vol. 77, Issue 14
  • DOI: 10.1128/AEM.00233-11

Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’
journal, October 2016


Temporal Changes in Microbial Ecology and Geochemistry in Produced Water from Hydraulically Fractured Marcellus Shale Gas Wells
journal, May 2014

  • Cluff, Maryam A.; Hartsock, Angela; MacRae, Jean D.
  • Environmental Science & Technology, Vol. 48, Issue 11
  • DOI: 10.1021/es501173p

Comparative genomics and physiology of the genus Methanohalophilus , a prevalent methanogen in hydraulically fractured shale
journal, December 2018

  • Borton, Mikayla A.; Daly, Rebecca A.; O'Banion, Bridget
  • Environmental Microbiology, Vol. 20, Issue 12
  • DOI: 10.1111/1462-2920.14467

Phylogenetic Analysis of a Microbialite-Forming Microbial Mat from a Hypersaline Lake of the Kiritimati Atoll, Central Pacific
journal, June 2013


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


Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia
journal, November 2007

  • Dunfield, Peter F.; Yuryev, Anton; Senin, Pavel
  • Nature, Vol. 450, Issue 7171
  • DOI: 10.1038/nature06411

Hydraulic fracturing offers view of microbial life in the deep terrestrial subsurface
journal, August 2016

  • Mouser, Paula J.; Borton, Mikayla; Darrah, Thomas H.
  • FEMS Microbiology Ecology, Vol. 92, Issue 11
  • DOI: 10.1093/femsec/fiw166

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

Characterization and Identification of Numerically Abundant Culturable Bacteria from the Anoxic Bulk Soil of Rice Paddy Microcosms
journal, November 1999


Terrimicrobium sacchariphilum gen. nov., sp. nov., an anaerobic bacterium of the class 'Spartobacteria' in the phylum Verrucomicrobia, isolated from a rice paddy field
journal, February 2014

  • Qiu, Y. -L.; Kuang, X. -z.; Shi, X. -s.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 5
  • DOI: 10.1099/ijs.0.060244-0

Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
journal, September 2017


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


Microbial diversity and methanogenic activity of Antrim Shale formation waters from recently fractured wells
journal, January 2013


Unusual biology across a group comprising more than 15% of domain Bacteria
journal, June 2015

  • Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C.
  • Nature, Vol. 523, Issue 7559
  • DOI: 10.1038/nature14486

Detection and Cultivation of Soil Verrucomicrobia
journal, December 2005


Microbial Community Changes in Hydraulic Fracturing Fluids and Produced Water from Shale Gas Extraction
journal, October 2013

  • Murali Mohan, Arvind; Hartsock, Angela; Bibby, Kyle J.
  • Environmental Science & Technology, Vol. 47, Issue 22
  • DOI: 10.1021/es402928b

Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing
journal, December 2018


Microbial response to drying and rewetting: osmotic and matric effects
journal, September 2011


Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics
journal, October 2017


Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales
journal, June 2018

  • Borton, Mikayla A.; Hoyt, David W.; Roux, Simon
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
  • DOI: 10.1073/pnas.1800155115

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

Sulfide Generation by Dominant Halanaerobium Microorganisms in Hydraulically Fractured Shales
journal, July 2017


Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum
journal, June 2016

  • Spring, Stefan; Bunk, Boyke; Spröer, Cathrin
  • The ISME Journal, Vol. 10, Issue 12
  • DOI: 10.1038/ismej.2016.84

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Rubritalea marina gen. nov., sp. nov., a marine representative of the phylum ‘Verrucomicrobia’, isolated from a sponge (Porifera)
journal, November 2006

  • Scheuermayer, Matthias; Gulder, Tobias A. M.; Bringmann, Gerhard
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 56, Issue 11
  • DOI: 10.1099/00207713-56-11-2723-c

Quantitative Survey and Structural Classification of Hydraulic Fracturing Chemicals Reported in Unconventional Gas Production
journal, March 2016

  • Elsner, Martin; Hoelzer, Kathrin
  • Environmental Science & Technology, Vol. 50, Issue 7
  • DOI: 10.1021/acs.est.5b02818

Molecular identification of Bacteria and Eukarya inhabiting an Antarctic cryoconite hole
journal, January 2003


Cerasicoccus maritimus sp. nov. and Cerasicoccus frondis sp. nov., two peptidoglycan-less marine verrucomicrobial species, and description of Verrucomicrobia phyl. nov., nom. rev.
journal, January 2010

  • Yoon, Jaewoo; Matsuo, Yoshihide; Matsuda, Satoru
  • The Journal of General and Applied Microbiology, Vol. 56, Issue 3
  • DOI: 10.2323/jgam.56.213

Bringing your tools to CyVerse Discovery Environment using Docker
journal, January 2016


Bringing your tools to CyVerse Discovery Environment using Docker
journal, January 2016


Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum 'Verrucomicrobia' isolated from seawater in Japan
journal, May 2007

  • Yoon, J.; Yasumoto-Hirose, M.; Katsuta, A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 5
  • DOI: 10.1099/ijs.0.64755-0

Bringing your tools to CyVerse Discovery Environment using Docker
journal, January 2016


High Diversity of Culturable Prokaryotes in a Lithifying Hypersaline Microbial Mat
journal, March 2015


Rubritalea marina gen. nov., sp. nov., a marine representative of the phylum 'Verrucomicrobia', isolated from a sponge (Porifera)
journal, September 2006

  • Scheuermayer, M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 9
  • DOI: 10.1099/ijs.0.64360-0

An Assessment of the Diversity of Culturable Bacteria from Main Root of Sugar Beet
journal, January 2014

  • Okazaki, Kazuyuki; Iino, Takao; Kuroda, Yosuke
  • Microbes and Environments, Vol. 29, Issue 2
  • DOI: 10.1264/jsme2.me13182

Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV)
journal, October 2017

  • Lefkowitz, Elliot J.; Dempsey, Donald M.; Hendrickson, Robert Curtis
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx932

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

Metabolic Capability of a Predominant Halanaerobium sp. in Hydraulically Fractured Gas Wells and Its Implication in Pipeline Corrosion
journal, June 2016

  • Liang, Renxing; Davidova, Irene A.; Marks, Christopher R.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00988

Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice‐covered Lakes
journal, July 2018

  • Tran, Patricia; Ramachandran, Arthi; Khawasik, Ola
  • Environmental Microbiology, Vol. 20, Issue 7
  • DOI: 10.1111/1462-2920.14283

A modular method for the extraction of DNA and RNA, and the separation of DNA pools from diverse environmental sample types
journal, May 2015


Nitrogen fixation by the verrucomicrobial methanotroph ‘Methylacidiphilum fumariolicum’ SolV
journal, April 2010

  • Khadem, Ahmad F.; Pol, Arjan; Jetten, Mike S. M.
  • Microbiology, Vol. 156, Issue 4
  • DOI: 10.1099/mic.0.036061-0

Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division 'Verrucomicrobia' isolated from rice paddy soil
journal, November 2001

  • Chin, K. J.; Liesack, W.; Janssen, P. H.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 51, Issue 6
  • DOI: 10.1099/00207713-51-6-1965

Luteolibacter flavescens sp. nov., isolated from deep seawater
journal, March 2017

  • Zhang, Chongya; Dong, Bolin; Wang, Ruijun
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 3
  • DOI: 10.1099/ijsem.0.001713