Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep

Abstract

We report Syntrophic consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) consume large amounts of methane and serve as the foundational microorganisms in marine methane seeps. Despite their importance in the carbon cycle, research on the physiology of ANME-SRB consortia has been hampered by the slow growth and complex physicochemical environment the consortia inhabit. Here, we report successful sediment-free enrichment of ANME-SRB consortia from deep-sea methane seep sediments in the Santa Monica Basin, California. Anoxic Percoll density gradients and size-selective filtration were used to separate ANME-SRB consortia from sediment particles and single cells to accelerate the cultivation process. Over a 3-year period, a subset of the sediment-associated ANME and SRB lineages, predominantly comprised of ANME-2a/2b (“Candidatus Methanocomedenaceae”) and their syntrophic bacterial partners, SEEP-SRB1/2, adapted and grew under defined laboratory conditions. Metagenome-assembled genomes from several enrichments revealed that ANME-2a, SEEP-SRB1, and Methanococcoides in different enrichments from the same inoculum represented distinct species, whereas other coenriched microorganisms were closely related at the species level. This suggests that ANME, SRB, and Methanococcoides are more genetically diverse than other members in methane seeps. Flow cytometry sorting and sequencing of cell aggregates revealed that Methanococcoides, Anaerolineales, and SEEP-SRB1 were overrepresented in multiple ANME-2amore » cell aggregates relative to the bulk metagenomes, suggesting they were physically associated and possibly interacting. Overall, this study represents a successful case of selective cultivation of anaerobic slow-growing microorganisms from sediments based on their physical characteristics, introducing new opportunities for detailed genomic, physiological, biochemical, and ecological analyses. Biological anaerobic oxidation of methane (AOM) coupled with sulfate reduction represents a large methane sink in global ocean sediments. Methane consumption is carried out by syntrophic archaeal-bacterial consortia and fuels a unique ecosystem, yet the interactions in these slow-growing syntrophic consortia and with other associated community members remain poorly understood. The significance of this study is the establishment of sediment-free enrichment cultures of anaerobic methanotrophic archaea and sulfate-reducing bacteria performing AOM with sulfate using selective cultivation approaches based on size, density, and metabolism. By reconstructing microbial genomes and analyzing community composition of the enrichment cultures and cell aggregates, we shed light on the diversity of microorganisms physically associated with AOM consortia beyond the core syntrophic partners. These enrichment cultures offer simplified model systems to extend our understanding of the diversity of microbial interactions within marine methane seeps.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1];  [2];  [2]; ORCiD logo [2];  [1]
+ Show Author Affiliations
  1. California Institute of Technology (CalTech), Pasadena, CA (United States)
  2. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States).Joint Genome Institute
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Netherlands Organisation for Scientific Research
OSTI Identifier:
1960231
Grant/Contract Number:  
AC02-05CH11231; SC0016469; 019.153LW.039
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 88; Journal Issue: 11; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; anaerobic oxidation of methane; anaerobic methanotrophic archaea; ANME; cultivation; flow cytometry; genomics; interspecies interaction

Citation Formats

Yu, Hang, Speth, Daan R., Connon, Stephanie A., Goudeau, Danielle, Malmstrom, Rex R., Woyke, Tanja, and Orphan, Victoria J. Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep. United States: N. p., 2022. Web. doi:10.1128/aem.02109-21.
Copy to clipboard
Yu, Hang, Speth, Daan R., Connon, Stephanie A., Goudeau, Danielle, Malmstrom, Rex R., Woyke, Tanja, & Orphan, Victoria J. Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep. United States. https://doi.org/10.1128/aem.02109-21
Copy to clipboard
Yu, Hang, Speth, Daan R., Connon, Stephanie A., Goudeau, Danielle, Malmstrom, Rex R., Woyke, Tanja, and Orphan, Victoria J. Mon . "Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep". United States. https://doi.org/10.1128/aem.02109-21. https://www.osti.gov/servlets/purl/1960231.
Copy to clipboard
@article{osti_1960231,
title = {Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep},
author = {Yu, Hang and Speth, Daan R. and Connon, Stephanie A. and Goudeau, Danielle and Malmstrom, Rex R. and Woyke, Tanja and Orphan, Victoria J.},
abstractNote = {We report Syntrophic consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) consume large amounts of methane and serve as the foundational microorganisms in marine methane seeps. Despite their importance in the carbon cycle, research on the physiology of ANME-SRB consortia has been hampered by the slow growth and complex physicochemical environment the consortia inhabit. Here, we report successful sediment-free enrichment of ANME-SRB consortia from deep-sea methane seep sediments in the Santa Monica Basin, California. Anoxic Percoll density gradients and size-selective filtration were used to separate ANME-SRB consortia from sediment particles and single cells to accelerate the cultivation process. Over a 3-year period, a subset of the sediment-associated ANME and SRB lineages, predominantly comprised of ANME-2a/2b (“Candidatus Methanocomedenaceae”) and their syntrophic bacterial partners, SEEP-SRB1/2, adapted and grew under defined laboratory conditions. Metagenome-assembled genomes from several enrichments revealed that ANME-2a, SEEP-SRB1, and Methanococcoides in different enrichments from the same inoculum represented distinct species, whereas other coenriched microorganisms were closely related at the species level. This suggests that ANME, SRB, and Methanococcoides are more genetically diverse than other members in methane seeps. Flow cytometry sorting and sequencing of cell aggregates revealed that Methanococcoides, Anaerolineales, and SEEP-SRB1 were overrepresented in multiple ANME-2a cell aggregates relative to the bulk metagenomes, suggesting they were physically associated and possibly interacting. Overall, this study represents a successful case of selective cultivation of anaerobic slow-growing microorganisms from sediments based on their physical characteristics, introducing new opportunities for detailed genomic, physiological, biochemical, and ecological analyses. Biological anaerobic oxidation of methane (AOM) coupled with sulfate reduction represents a large methane sink in global ocean sediments. Methane consumption is carried out by syntrophic archaeal-bacterial consortia and fuels a unique ecosystem, yet the interactions in these slow-growing syntrophic consortia and with other associated community members remain poorly understood. The significance of this study is the establishment of sediment-free enrichment cultures of anaerobic methanotrophic archaea and sulfate-reducing bacteria performing AOM with sulfate using selective cultivation approaches based on size, density, and metabolism. By reconstructing microbial genomes and analyzing community composition of the enrichment cultures and cell aggregates, we shed light on the diversity of microorganisms physically associated with AOM consortia beyond the core syntrophic partners. These enrichment cultures offer simplified model systems to extend our understanding of the diversity of microbial interactions within marine methane seeps.},
doi = {10.1128/aem.02109-21},
journal = {Applied and Environmental Microbiology},
number = 11,
volume = 88,
place = {United States},
year = {Mon May 23 00:00:00 EDT 2022},
month = {Mon May 23 00:00:00 EDT 2022}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/aem.02109-21
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Microbial interactions: from networks to models
journal, July 2012

  • Faust, Karoline; Raes, Jeroen
  • Nature Reviews Microbiology, Vol. 10, Issue 8
  • DOI: 10.1038/nrmicro2832

Bacterial chemolithoautotrophy via manganese oxidation
journal, July 2020

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

Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters
journal, May 1969

Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011

"Candidatus Cloacamonas Acidaminovorans": Genome Sequence Reconstruction Provides a First Glimpse of a New Bacterial Division
journal, February 2008

  • Pelletier, E.; Kreimeyer, A.; Bocs, S.
  • Journal of Bacteriology, Vol. 190, Issue 7
  • DOI: 10.1128/JB.01248-07

In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate
journal, January 2007

Stimulation of in vitro anaerobic oxidation of methane rate in a continuous high-pressure bioreactor
journal, May 2010

Genomic and enzymatic evidence of acetogenesis by anaerobic methanotrophic archaea
journal, August 2020

Variations in Archaeal and Bacterial Diversity Associated with the Sulfate-Methane Transition Zone in Continental Margin Sediments (Santa Barbara Basin, California)
journal, January 2009

  • Harrison, B. K.; Zhang, H.; Berelson, W.
  • Applied and Environmental Microbiology, Vol. 75, Issue 6
  • DOI: 10.1128/AEM.01812-08

Global dispersion and local diversification of the methane seep microbiome
journal, March 2015

  • Ruff, S. Emil; Biddle, Jennifer F.; Teske, Andreas P.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 13
  • DOI: 10.1073/pnas.1421865112

The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation
journal, April 2009

  • Allen, Michelle A.; Lauro, Federico M.; Williams, Timothy J.
  • The ISME Journal, Vol. 3, Issue 9
  • DOI: 10.1038/ismej.2009.45

Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction
journal, February 2016

A Methanogenic Archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov.
journal, December 1992

Enrichment of anaerobic methanotrophs in sulfate-reducing membrane bioreactors
journal, October 2009

  • Meulepas, Roel J. W.; Jagersma, Christian G.; Gieteling, Jarno
  • Biotechnology and Bioengineering, Vol. 104, Issue 3
  • DOI: 10.1002/bit.22412

New cell extraction procedure applied to deep subsurface sediments: Cell extraction of deep subsurface sediments
journal, June 2008

  • Kallmeyer, Jens; Smith, David C.; Spivack, Arthur J.
  • Limnology and Oceanography: Methods, Vol. 6, Issue 6
  • DOI: 10.4319/lom.2008.6.236

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

Methane Seep in Shallow-Water Permeable Sediment Harbors High Diversity of Anaerobic Methanotrophic Communities, Elba, Italy
journal, March 2016

Double Labeling of Oligonucleotide Probes for Fluorescence In Situ Hybridization (DOPE-FISH) Improves Signal Intensity and Increases rRNA Accessibility
journal, December 2009

  • Stoecker, K.; Dorninger, C.; Daims, H.
  • Applied and Environmental Microbiology, Vol. 76, Issue 3
  • DOI: 10.1128/AEM.02456-09

Microbes trading electricity in consortia of environmental and biotechnological significance
journal, February 2021

Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments
journal, May 2002

  • Orphan, V. J.; House, C. H.; Hinrichs, K.-U.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 11, p. 7663-7668
  • DOI: 10.1073/pnas.072210299

A sediment flow-through system to study the impact of shifting fluid and methane flow regimes on the efficiency of the benthic methane filter
journal, January 2014

  • Steeb, Philip; Linke, Peter; Treude, Tina
  • Limnology and Oceanography: Methods, Vol. 12, Issue 1
  • DOI: 10.4319/lom.2014.12.25

Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system
journal, March 2016

  • Speth, Daan R.; in ’t Zandt, Michiel H.; Guerrero-Cruz, Simon
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11172

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

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

Missing lithotroph identified as new planctomycete
journal, July 1999

  • Strous, Marc; Fuerst, John A.; Kramer, Evelien H. M.
  • Nature, Vol. 400, Issue 6743
  • DOI: 10.1038/22749

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
journal, September 2018

  • Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik
  • Nature Reviews Microbiology, Vol. 16, Issue 10
  • DOI: 10.1038/s41579-018-0076-2

A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
journal, May 2002

  • Huber, Harald; Hohn, Michael J.; Rachel, Reinhard
  • Nature, Vol. 417, Issue 6884
  • DOI: 10.1038/417063a

Biogenic formation of amorphous carbon by anaerobic methanotrophs and select methanogens
journal, October 2021

  • Allen, Kylie D.; Wegener, Gunter; Matthew Sublett, D.
  • Science Advances, Vol. 7, Issue 44
  • DOI: 10.1126/sciadv.abg9739

Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea
journal, December 2018

Bellilinea caldifistulae gen. nov., sp. nov. and Longilinea arvoryzae gen. nov., sp. nov., strictly anaerobic, filamentous bacteria of the phylum Chloroflexi isolated from methanogenic propionate-degrading consortia
journal, October 2007

  • Yamada, Takeshi; Imachi, Hiroyuki; Ohashi, Akiyoshi
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 10
  • DOI: 10.1099/ijs.0.65098-0

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

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

Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea
journal, January 2022

Metabolic Capabilities of Microorganisms Involved in and Associated with the Anaerobic Oxidation of Methane
journal, February 2016

Anaerobic Oxidation of Methane: Progress with an Unknown Process
journal, October 2009

Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling
journal, March 2015

  • Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C.
  • Current Biology, Vol. 25, Issue 6
  • DOI: 10.1016/j.cub.2015.01.014

Identification of a Redox Active Thioquinoxalinol Sulfate Compound Produced by an Anaerobic Methane-Oxidizing Microbial Consortium
journal, December 2019

Sulfate differentially stimulates but is not respired by diverse anaerobic methanotrophic archaea
journal, July 2021

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

Microbial diversity and community structure of a highly active anaerobic methane-oxidizing sulfate-reducing enrichment
journal, December 2009

Enrichment of ANME-2 dominated anaerobic methanotrophy from cold seep sediment in an external ultrafiltration membrane bioreactor
journal, March 2018

  • Bhattarai, Susma; Cassarini, Chiara; Rene, Eldon R.
  • Engineering in Life Sciences, Vol. 18, Issue 6
  • DOI: 10.1002/elsc.201700148

Diversity and Distribution of Methanotrophic Archaea at Cold Seeps
journal, January 2005

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

Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
journal, July 2019

Growth and Population Dynamics of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a Continuous-Flow Bioreactor
journal, July 2005

Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle
journal, December 2014

  • He, Xuesong; McLean, Jeffrey S.; Edlund, Anna
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 1
  • DOI: 10.1073/pnas.1419038112

Growth of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a High-Pressure Membrane Capsule Bioreactor
journal, December 2014

  • Timmers, Peer H. A.; Gieteling, Jarno; Widjaja-Greefkes, H. C. Aura
  • Applied and Environmental Microbiology, Vol. 81, Issue 4
  • DOI: 10.1128/AEM.03255-14

Genomic insights into members of the candidate phylum Hyd24-12 common in mesophilic anaerobic digesters
journal, April 2016

  • Kirkegaard, Rasmus Hansen; Dueholm, Morten Simonsen; McIlroy, Simon Jon
  • The ISME Journal, Vol. 10, Issue 10
  • DOI: 10.1038/ismej.2016.43

Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics
journal, May 2008

  • Pernthaler, A.; Dekas, A. E.; Brown, C. T.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 19
  • DOI: 10.1073/pnas.0711303105

The globally widespread genus Sulfurimonas: versatile energy metabolisms and adaptations to redox clines
journal, September 2015

Thermophilic archaea activate butane via alkyl-coenzyme M formation
journal, October 2016

  • Laso-Pérez, Rafael; Wegener, Gunter; Knittel, Katrin
  • Nature, Vol. 539, Issue 7629
  • DOI: 10.1038/nature20152

High-pressure systems for gas-phase free continuous incubation of enriched marine microbial communities performing anaerobic oxidation of methane
journal, February 2010

  • Deusner, Christian; Meyer, Volker; Ferdelman, Timothy G.
  • Biotechnology and Bioengineering, Vol. 105, Issue 3
  • DOI: 10.1002/bit.22553

A marine microbial consortium apparently mediating anaerobic oxidation of methane
journal, October 2000

  • Boetius, Antje; Ravenschlag, Katrin; Schubert, Carsten J.
  • Nature, Vol. 407, Issue 6804
  • DOI: 10.1038/35036572

Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor
journal, September 2003

The Impact of Methane on Microbial Communities at Marine Arctic Gas Hydrate Bearing Sediment
journal, September 2020

  • Carrier, Vincent; Svenning, Mette M.; Gründger, Friederike
  • Frontiers in Microbiology, Vol. 11
  • DOI: 10.3389/fmicb.2020.01932

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

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

DADA2: High-resolution sample inference from Illumina amplicon data
journal, May 2016

  • Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J.
  • Nature Methods, Vol. 13, Issue 7
  • DOI: 10.1038/nmeth.3869

dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication
journal, July 2017

  • Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon
  • The ISME Journal, Vol. 11, Issue 12
  • DOI: 10.1038/ismej.2017.126

Thermophilic anaerobic oxidation of methane by marine microbial consortia
journal, June 2011

  • Holler, Thomas; Widdel, Friedrich; Knittel, Katrin
  • The ISME Journal, Vol. 5, Issue 12
  • DOI: 10.1038/ismej.2011.77

Candidatus Syntrophosphaera thermopropionivorans: a novel player in syntrophic propionate oxidation during anaerobic digestion
journal, April 2019

  • Dyksma, Stefan; Gallert, Claudia
  • Environmental Microbiology Reports, Vol. 11, Issue 4
  • DOI: 10.1111/1758-2229.12759

Culture-Independent Analyses Reveal Novel Anaerolineaceae as Abundant Primary Fermenters in Anaerobic Digesters Treating Waste Activated Sludge
journal, June 2017

  • McIlroy, Simon J.; Kirkegaard, Rasmus H.; Dueholm, Morten S.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01134

Comparison of Archaeal and Bacterial Diversity in Methane Seep Carbonate Nodules and Host Sediments, Eel River Basin and Hydrate Ridge, USA
journal, May 2015

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

Growth and mechanism of filamentous-sulfur formation by Candidatus Arcobacter sulfidicus in opposing oxygen-sulfide gradients
journal, January 2007

Enrichment of a microbial community performing anaerobic oxidation of methane in a continuous high-pressure bioreactor
journal, June 2011

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep
journal, March 2019

Crystal structure of a key enzyme for anaerobic ethane activation
journal, July 2021

Insights into the ecology, evolution, and metabolism of the widespread Woesearchaeotal lineages
journal, June 2018

Putative Extracellular Electron Transfer in Methanogenic Archaea
journal, March 2021

Isolation and characterization of Flexilinea flocculi gen. nov., sp. nov., a filamentous, anaerobic bacterium belonging to the class Anaerolineae in the phylum Chloroflexi
journal, February 2016

  • Sun, Liwei; Toyonaga, Mayu; Ohashi, Akiko
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 2
  • DOI: 10.1099/ijsem.0.000822
    Sort by:
    [ × clear filter / sort ]

    Similar Records in DOE PAGES and OSTI.GOV collections: