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Title: Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea

Abstract

The anaerobic oxidation of methane by anaerobic methanotrophic (ANME) archaea in syntrophic partnership with deltaproteobacterial sulfate-reducing bacteria (SRB) is the primary mechanism for methane removal in ocean sediments. The mechanism of their syntrophy has been the subject of much research as traditional intermediate compounds, such as hydrogen and formate, failed to decouple the partners. Recent findings have indicated the potential for extracellular electron transfer from ANME archaea to SRB, though it is unclear how extracellular electrons are integrated into the metabolism of the SRB partner. We used metagenomics to reconstruct eight genomes from the globally distributed SEEP-SRB1 clade of ANME partner bacteria to determine what genomic features are required for syntrophy. The SEEP-SRB1 genomes contain large multiheme cytochromes that were not found in previously described free-living SRB and also lack periplasmic hydrogenases that may prevent an independent lifestyle without an extracellular source of electrons from ANME archaea. Metaproteomics revealed the expression of these cytochromes at in situ methane seep sediments from three sites along the Pacific coast of the United States. Phylogenetic analysis showed that these cytochromes appear to have been horizontally transferred from metal-respiring members of the Deltaproteobacteria such as Geobacter and may allow these syntrophic SRB to acceptmore » extracellular electrons in place of other chemical/organic electron donors. Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [1]
  1. California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  3. Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division; Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology
  5. Univ. of Queensland, Brisbane, QLD (Australia). Australian Centre for Ecogenomics. School of Chemistry and Molecular Biosciences
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Gordon and Betty Moore Foundation (United States); National Science Foundation (NSF)
OSTI Identifier:
1394609
Grant/Contract Number:  
AC05-00OR22725; SC0003940; SC0010574; GBMF3780; OCE-0939564
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 8; Journal Issue: 4; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ANME; AOM; anaerobic oxidation of methane; extracellular electron transfer; SEEP-SRB1; methane seeps; multiheme cytochrome; sulfate-reducing bacteria

Citation Formats

Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Hettich, Robert L., Tyson, Gene W., and Orphan, Victoria J.. Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. United States: N. p., 2017. Web. https://doi.org/10.1128/mBio.00530-17.
Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Hettich, Robert L., Tyson, Gene W., & Orphan, Victoria J.. Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. United States. https://doi.org/10.1128/mBio.00530-17
Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Hettich, Robert L., Tyson, Gene W., and Orphan, Victoria J.. Tue . "Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea". United States. https://doi.org/10.1128/mBio.00530-17. https://www.osti.gov/servlets/purl/1394609.
@article{osti_1394609,
title = {Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea},
author = {Skennerton, Connor T. and Chourey, Karuna and Iyer, Ramsunder and Hettich, Robert L. and Tyson, Gene W. and Orphan, Victoria J.},
abstractNote = {The anaerobic oxidation of methane by anaerobic methanotrophic (ANME) archaea in syntrophic partnership with deltaproteobacterial sulfate-reducing bacteria (SRB) is the primary mechanism for methane removal in ocean sediments. The mechanism of their syntrophy has been the subject of much research as traditional intermediate compounds, such as hydrogen and formate, failed to decouple the partners. Recent findings have indicated the potential for extracellular electron transfer from ANME archaea to SRB, though it is unclear how extracellular electrons are integrated into the metabolism of the SRB partner. We used metagenomics to reconstruct eight genomes from the globally distributed SEEP-SRB1 clade of ANME partner bacteria to determine what genomic features are required for syntrophy. The SEEP-SRB1 genomes contain large multiheme cytochromes that were not found in previously described free-living SRB and also lack periplasmic hydrogenases that may prevent an independent lifestyle without an extracellular source of electrons from ANME archaea. Metaproteomics revealed the expression of these cytochromes at in situ methane seep sediments from three sites along the Pacific coast of the United States. Phylogenetic analysis showed that these cytochromes appear to have been horizontally transferred from metal-respiring members of the Deltaproteobacteria such as Geobacter and may allow these syntrophic SRB to accept extracellular electrons in place of other chemical/organic electron donors. Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria.},
doi = {10.1128/mBio.00530-17},
journal = {mBio (Online)},
number = 4,
volume = 8,
place = {United States},
year = {2017},
month = {8}
}

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Works referenced in this record:

The InterPro protein families database: the classification resource after 15 years
journal, November 2014

  • Mitchell, Alex; Chang, Hsin-Yu; Daugherty, Louise
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1243

Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis
journal, December 2007

  • Pereira, Patrícia M.; He, Qiang; Valente, Filipa M. A.
  • Antonie van Leeuwenhoek, Vol. 93, Issue 4
  • DOI: 10.1007/s10482-007-9212-0

Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri
journal, May 2014

  • Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua
  • Applied and Environmental Microbiology, Vol. 80, Issue 15
  • DOI: 10.1128/AEM.00895-14

Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry
journal, February 2007

  • Elias, Joshua E.; Gygi, Steven P.
  • Nature Methods, Vol. 4, Issue 3
  • DOI: 10.1038/nmeth1019

Protein Identification False Discovery Rates for Very Large Proteomics Data Sets Generated by Tandem Mass Spectrometry
journal, July 2009

  • Reiter, Lukas; Claassen, Manfred; Schrimpf, Sabine P.
  • Molecular & Cellular Proteomics, Vol. 8, Issue 11
  • DOI: 10.1074/mcp.M900317-MCP200

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


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

Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange: Growth with electrons supplied solely by DIET
journal, September 2013

  • Shrestha, Pravin Malla; Rotaru, Amelia-Elena; Aklujkar, Muktak
  • Environmental Microbiology Reports, Vol. 5, Issue 6
  • DOI: 10.1111/1758-2229.12093

A protein trisulfide couples dissimilatory sulfate reduction to energy conservation
journal, December 2015


Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane
journal, September 2013

  • Green-Saxena, A.; Dekas, A. E.; Dalleska, N. F.
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.147

The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism
journal, July 2014

  • Venceslau, S. S.; Stockdreher, Y.; Dahl, C.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7
  • DOI: 10.1016/j.bbabio.2014.03.007

MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph
journal, January 2015


Transcriptomic and Genetic Analysis of Direct Interspecies Electron Transfer
journal, February 2013

  • Shrestha, Pravin Malla; Rotaru, Amelia-Elena; Summers, Zarath M.
  • Applied and Environmental Microbiology, Vol. 79, Issue 7
  • DOI: 10.1128/AEM.03837-12

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


Single cell activity reveals direct electron transfer in methanotrophic consortia
journal, September 2015

  • McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P.
  • Nature, Vol. 526, Issue 7574
  • DOI: 10.1038/nature15512

Changes in Protein Expression Across Laboratory and Field Experiments in Geobacter bemidjiensis
journal, February 2015

  • Merkley, Eric D.; Wrighton, Kelly C.; Castelle, Cindy J.
  • Journal of Proteome Research, Vol. 14, Issue 3
  • DOI: 10.1021/pr500983v

Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics
journal, September 2004


Microbial electron transport and energy conservation – the foundation for optimizing bioelectrochemical systems
journal, June 2015


Coupling a Detergent Lysis/Cleanup Methodology with Intact Protein Fractionation for Enhanced Proteome Characterization
journal, October 2012

  • Sharma, Ritin; Dill, Brian D.; Chourey, Karuna
  • Journal of Proteome Research, Vol. 11, Issue 12
  • DOI: 10.1021/pr300709k

Development of an Enhanced Metaproteomic Approach for Deepening the Microbiome Characterization of the Human Infant Gut
journal, October 2014

  • Xiong, Weili; Giannone, Richard J.; Morowitz, Michael J.
  • Journal of Proteome Research, Vol. 14, Issue 1
  • DOI: 10.1021/pr500936p

Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens
journal, February 2011


Marine sediments microbes capable of electrode oxidation as a surrogate for lithotrophic insoluble substrate metabolism
journal, January 2015

  • Rowe, Annette R.; Chellamuthu, Prithiviraj; Lam, Bonita
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00784

Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics
journal, December 2010

  • Chourey, Karuna; Jansson, Janet; VerBerkmoes, Nathan
  • Journal of Proteome Research, Vol. 9, Issue 12
  • DOI: 10.1021/pr100787q

Methyl sulfides as intermediates in the anaerobic oxidation of methane
journal, September 2007


Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria
journal, December 2010

  • Summers, Z. M.; Fogarty, H. E.; Leang, C.
  • Science, Vol. 330, Issue 6009, p. 1413-1415
  • DOI: 10.1126/science.1196526

Proteomic Stable Isotope Probing Reveals Biosynthesis Dynamics of Slow Growing Methane Based Microbial Communities
journal, April 2016


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


Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in Rhodospirillum rubrum
journal, July 2016


A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea
journal, January 2011

  • Pereira, Inês A. Cardoso; Ramos, Ana Raquel; Grein, Fabian
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00069

Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors
journal, November 2006

  • Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 50
  • DOI: 10.1073/pnas.0606379103

Spatial distribution of nitrogen fixation in methane seep sediment and the role of the ANME archaea: Nitrogen fixation in methane seep sediment
journal, September 2013

  • Dekas, Anne E.; Chadwick, Grayson L.; Bowles, Marshall W.
  • Environmental Microbiology, Vol. 16, Issue 10
  • DOI: 10.1111/1462-2920.12247

ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data
journal, February 2016

  • Huerta-Cepas, Jaime; Serra, François; Bork, Peer
  • Molecular Biology and Evolution, Vol. 33, Issue 6
  • DOI: 10.1093/molbev/msw046

Dosage-Dependent Proteome Response of Shewanella oneidensis MR-1 to Acute Chromate Challenge
journal, May 2007

  • Thompson, Melissa R.; VerBerkmoes, Nathan C.; Chourey, Karuna
  • Journal of Proteome Research, Vol. 6, Issue 5
  • DOI: 10.1021/pr060502x

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


A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane
journal, January 2014

  • Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua
  • Energy Environ. Sci., Vol. 7, Issue 1
  • DOI: 10.1039/C3EE42189A

Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock
journal, October 2016

  • Bagnoud, Alexandre; Chourey, Karuna; Hettich, Robert L.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12770

Comparative Analysis of Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in Anoxic Marine Sediments
journal, April 2001


Towards a Genome-Based Taxonomy for Prokaryotes
journal, September 2005


Roles of HynAB and Ech, the Only Two Hydrogenases Found in the Model Sulfate Reducer Desulfovibrio gigas
journal, August 2013

  • Morais-Silva, F. O.; Santos, C. I.; Rodrigues, R.
  • Journal of Bacteriology, Vol. 195, Issue 20
  • DOI: 10.1128/JB.00411-13

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

Genomic analyses of bacterial porin-cytochrome gene clusters
journal, November 2014


BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

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

Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group
journal, February 2010


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

The ‘porin-cytochrome’ model for microbe-to-mineral electron transfer: Microbe-to-mineral electron transfer
journal, May 2012


Diversity and Abundance of Aerobic and Anaerobic Methane Oxidizers at the Haakon Mosby Mud Volcano, Barents Sea
journal, March 2007

  • Losekann, T.; Knittel, K.; Nadalig, T.
  • Applied and Environmental Microbiology, Vol. 73, Issue 10
  • DOI: 10.1128/AEM.00016-07

Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia
journal, October 2009


Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics
journal, January 2013


Molecular Dynamics of the Shewanella oneidensis Response to Chromate Stress
journal, March 2006

  • Brown, Steven D.; Thompson, Melissa R.; VerBerkmoes, Nathan C.
  • Molecular & Cellular Proteomics, Vol. 5, Issue 6
  • DOI: 10.1074/mcp.M500394-MCP200

Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria
journal, October 2015

  • Wegener, Gunter; Krukenberg, Viola; Riedel, Dietmar
  • Nature, Vol. 526, Issue 7574
  • DOI: 10.1038/nature15733

Energy-Converting [NiFe] Hydrogenases from Archaea and Extremophiles: Ancestors of Complex I
journal, February 2004


Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens
journal, January 2013


GroopM: an automated tool for the recovery of population genomes from related metagenomes
journal, January 2014

  • Imelfort, Michael; Parks, Donovan; Woodcroft, Ben J.
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.603

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

MyriMatch:  Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007

  • Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 6, Issue 2
  • DOI: 10.1021/pr0604054

Proteinortho: Detection of (Co-)orthologs in large-scale analysis
journal, April 2011


Exploration of the ‘cytochromome’ of Desulfuromonas acetoxidans, a marine bacterium capable of powering microbial fuel cells
journal, January 2011

  • Alves, Alexandra S.; Paquete, Catarina M.; Fonseca, Bruno M.
  • Metallomics, Vol. 3, Issue 4
  • DOI: 10.1039/c0mt00084a

The Qrc Membrane Complex, Related to the Alternative Complex III, Is a Menaquinone Reductase Involved in Sulfate Respiration
journal, May 2010

  • Venceslau, Sofia S.; Lino, Rita R.; Pereira, Ines A. C.
  • Journal of Biological Chemistry, Vol. 285, Issue 30
  • DOI: 10.1074/jbc.M110.124305

Extracellular electron transfer mechanisms between microorganisms and minerals
journal, August 2016

  • Shi, Liang; Dong, Hailiang; Reguera, Gemma
  • Nature Reviews Microbiology, Vol. 14, Issue 10
  • DOI: 10.1038/nrmicro.2016.93

Seafloor oxygen consumption fuelled by methane from cold seeps
journal, August 2013

  • Boetius, Antje; Wenzhöfer, Frank
  • Nature Geoscience, Vol. 6, Issue 9
  • DOI: 10.1038/ngeo1926

Cytochromes c in Archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis
journal, May 2015


Electron transfer between the QmoABC membrane complex and adenosine 5′-phosphosulfate reductase
journal, April 2016

  • Duarte, Américo G.; Santos, André A.; Pereira, Inês A. C.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 4
  • DOI: 10.1016/j.bbabio.2016.01.001

The Tmc Complex from Desulfovibrio vulgaris Hildenborough Is Involved in Transmembrane Electron Transfer from Periplasmic Hydrogen Oxidation
journal, August 2006

  • Pereira, Patrícia M.; Teixeira, Miguel; Xavier, António V.
  • Biochemistry, Vol. 45, Issue 34
  • DOI: 10.1021/bi0610294

Assimilation of methane and inorganic carbon by microbial communities mediating the anaerobic oxidation of methane
journal, September 2008


Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways
journal, December 2013


Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities
journal, January 2005


Phylogenomic analysis of Candidatus ‘Izimaplasma’ species: free-living representatives from a Tenericutes clade found in methane seeps
journal, April 2016

  • Skennerton, Connor T.; Haroon, Mohamed F.; Briegel, Ariane
  • The ISME Journal, Vol. 10, Issue 11
  • DOI: 10.1038/ismej.2016.55

Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander
journal, April 2020


Thermophilic anaerobic oxidation of methane by marine microbial consortia
text, January 2011

  • Andreas, Teske,; Y., Kellermann, Matthias; Gunter, Wegener,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/ttyb-qm72

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    Physiology and Distribution of Archaeal Methanotrophs That Couple Anaerobic Oxidation of Methane with Sulfate Reduction
    journal, July 2019

    • Bhattarai, S.; Cassarini, C.; Lens, P. N. L.
    • Microbiology and Molecular Biology Reviews, Vol. 83, Issue 3
    • DOI: 10.1128/mmbr.00074-18

    Geobacter Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms
    journal, July 2018

    • Ueki, Toshiyuki; Nevin, Kelly P.; Rotaru, Amelia-Elena
    • mBio, Vol. 9, Issue 4
    • DOI: 10.1128/mbio.01273-18

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    journal, April 2018

    • McGlynn, Shawn E.; Chadwick, Grayson L.; O'Neill, Ariel
    • Applied and Environmental Microbiology, Vol. 84, Issue 11
    • DOI: 10.1128/aem.00399-18

    The Biogeochemical Sulfur Cycle of Marine Sediments
    journal, April 2019

    • Jørgensen, Bo Barker; Findlay, Alyssa J.; Pellerin, André
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.00849

    Extracellular Electron Transfer May Be an Overlooked Contribution to Pelagic Respiration in Humic-Rich Freshwater Lakes
    journal, January 2019


    Single-Cell Genomics Reveals a Diverse Metabolic Potential of Uncultivated Desulfatiglans-Related Deltaproteobacteria Widely Distributed in Marine Sediment
    journal, September 2018