Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option

Walker, David J.  F.; Nevin, Kelly P.; Holmes, Dawn E.; Rotaru, Amelia-Elena; Ward, Joy E.; Woodard, Trevor L.; Zhu, Jiaxin; Ueki, Toshiyuki; Nonnenmann, Stephen S.; McInerney, Michael J.; Lovley, Derek R.

doi:10.1038/s41396-019-0575-9

Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option

Journal Article · Thu Jan 02 00:00:00 EST 2020 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-019-0575-9· OSTI ID:1604770

Walker, David J. F. ^[1]; Nevin, Kelly P. ^[2]; Holmes, Dawn E. ^[3]; Rotaru, Amelia-Elena ^[4]; Ward, Joy E. ^[2]; Woodard, Trevor L. ^[2]; Zhu, Jiaxin ^[2]; Ueki, Toshiyuki ^[2]; Nonnenmann, Stephen S. ^[2]; ^[5]; Lovley, Derek R. ^[2]

Univ. of Massachusetts, Amherst, MA (United States); University of Oklahoma
Univ. of Massachusetts, Amherst, MA (United States)
Univ. of Massachusetts, Amherst, MA (United States); Western New England University, Springfield, MA (United States)
Univ. of Massachusetts, Amherst, MA (United States); Univ. of Southern Denmark, Odense (Denmark)
Univ. of Oklahoma, Norman, OK (United States)

Syntrophic interspecies electron exchange is necessary for the stable functioning of diverse anaerobic microbial communities. Hydrogen/formate interspecies electron transfer (HFIT), in which H₂ and/or formate function as diffusible electron carriers, has been considered to be the primary mechanism for electron transfer because most common syntrophs were thought to lack biochemical components, such as electrically conductive pili (e-pili), necessary for direct interspecies electron transfer (DIET). Herein we report that Syntrophus aciditrophicus, one of the most intensively studied microbial models for HFIT, produces e-pili and can grow via DIET. Heterologous expression of the putative S. aciditrophicus type IV pilin gene in Geobacter sulfurreducens yielded conductive pili of the same diameter (4 nm) and conductance of the native S. aciditrophicus pili and enabled long-range electron transport in G. sulfurreducens. S. aciditrophicus lacked abundant c-type cytochromes often associated with DIET. Pilin genes likely to yield e-pili were found in other genera of hydrogen/formate-producing syntrophs. The discovery that DIET is a likely option for diverse syntrophs that are abundant in many anaerobic environments necessitates a reexamination of the paradigm that HFIT is the predominant mechanism for syntrophic electron exchange within anaerobic microbial communities of biogeochemical and practical significance.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Oklahoma, Norman, OK (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-96ER20214

OSTI ID:: 1604770

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 3 Vol. 14; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Microbial interspecies interactions: recent findings in syntrophic consortia Kouzuma, Atsushi; Kato, Souichiro; Watanabe, Kazuya Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00477	journal	May 2015
Synthetic Biological Protein Nanowires with High Conductivity Tan, Yang; Adhikari, Ramesh Y.; Malvankar, Nikhil S. Small, Vol. 12, Issue 33 https://doi.org/10.1002/smll.201601112	journal	July 2016
Syntrophus aciditrophicus sp. nov., a new anaerobic bacterium that degrades fatty acids and benzoate in syntrophic association with hydrogen-using microorganisms Jackson, Bradley E.; Bhupathiraju, V. K.; Tanner, Ralph S. Archives of Microbiology, Vol. 171, Issue 2 https://doi.org/10.1007/s002030050685	journal	January 1999
Biological synthesis of high-conductive pili in aerobic bacterium Pseudomonas aeruginosa Liu, Xi; Wang, Shiwei; Xu, Anming Applied Microbiology and Biotechnology, Vol. 103, Issue 3 https://doi.org/10.1007/s00253-018-9484-5	journal	December 2018
Correlation between microbial community and granule conductivity in anaerobic bioreactors for brewery wastewater treatment Shrestha, Pravin Malla; Malvankar, Nikhil S.; Werner, Jeffrey J. Bioresource Technology, Vol. 174 https://doi.org/10.1016/j.biortech.2014.10.004	journal	December 2014
Advances towards understanding and engineering direct interspecies electron transfer in anaerobic digestion Barua, Sajib; Dhar, Bipro Ranjan Bioresource Technology, Vol. 244 https://doi.org/10.1016/j.biortech.2017.08.023	journal	November 2017
Ferroferric oxide triggered possible direct interspecies electron transfer between Syntrophomonas and Methanosaeta to enhance waste activated sludge anaerobic digestion Zhao, Zisheng; Li, Yang; Yu, Qilin Bioresource Technology, Vol. 250 https://doi.org/10.1016/j.biortech.2017.11.003	journal	February 2018
Direct interspecies electron transfer via conductive materials: A perspective for anaerobic digestion applications Park, Jeong-Hoon; Kang, Hyun-Jin; Park, Kang-Hee Bioresource Technology, Vol. 254 https://doi.org/10.1016/j.biortech.2018.01.095	journal	April 2018
Electrically conductive pili: Biological function and potential applications in electronics Lovley, Derek R. Current Opinion in Electrochemistry, Vol. 4, Issue 1 https://doi.org/10.1016/j.coelec.2017.08.015	journal	August 2017
Syntrophy in anaerobic global carbon cycles McInerney, Michael J.; Sieber, Jessica R.; Gunsalus, Robert P. Current Opinion in Biotechnology, Vol. 20, Issue 6 https://doi.org/10.1016/j.copbio.2009.10.001	journal	December 2009
Improving anaerobic digestion via direct interspecies electron transfer requires development of suitable characterization methods Van Steendam, Caroline; Smets, Ilse; Skerlos, Steven Current Opinion in Biotechnology, Vol. 57 https://doi.org/10.1016/j.copbio.2019.03.018	journal	June 2019
Type IV Pilus Structure by Cryo-Electron Microscopy and Crystallography: Implications for Pilus Assembly and Functions Craig, Lisa; Volkmann, Niels; Arvai, Andrew S. Molecular Cell, Vol. 23, Issue 5, p. 651-662 https://doi.org/10.1016/j.molcel.2006.07.004	journal	September 2006
Type IV pili: paradoxes in form and function Craig, Lisa; Li, Juliana Current Opinion in Structural Biology, Vol. 18, Issue 2 https://doi.org/10.1016/j.sbi.2007.12.009	journal	April 2008
Communities stimulated with ethanol to perform direct interspecies electron transfer for syntrophic metabolism of propionate and butyrate Zhao, Zhiqiang; Zhang, Yaobin; Yu, Qilin Water Research, Vol. 102 https://doi.org/10.1016/j.watres.2016.07.005	journal	October 2016
Methane Production and Conductive Materials: A Critical Review Martins, Gilberto; Salvador, Andreia F.; Pereira, Luciana Environmental Science & Technology, Vol. 52, Issue 18 https://doi.org/10.1021/acs.est.8b01913	journal	August 2018
Transcriptome of Geobacter uraniireducens growing in uranium-contaminated subsurface sediments Holmes, Dawn E.; O'Neil, Regina A.; Chavan, Milind A. The ISME Journal, Vol. 3, Issue 2 https://doi.org/10.1038/ismej.2008.89	journal	October 2008
Happy together: microbial communities that hook up to swap electrons Lovley, Derek R. The ISME Journal, Vol. 11, Issue 2 https://doi.org/10.1038/ismej.2016.136	journal	November 2016
Electrically conductive pili from pilin genes of phylogenetically diverse microorganisms Walker, David JF; Adhikari, Ramesh Y.; Holmes, Dawn E. The ISME Journal, Vol. 12, Issue 1 https://doi.org/10.1038/ismej.2017.141	journal	September 2017
Extracellular electron transfer via microbial nanowires Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena Nature, Vol. 435, Issue 7045, p. 1098-1101 https://doi.org/10.1038/nature03661	journal	June 2005
Mechanistic stratification in electroactive biofilms of Geobacter sulfurreducens mediated by pilus nanowires Steidl, Rebecca J.; Lampa-Pastirk, Sanela; Reguera, Gemma Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12217	journal	August 2016
Structure of the Neisseria meningitidis Type IV pilus Kolappan, Subramania; Coureuil, Mathieu; Yu, Xiong Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13015	journal	October 2016
Syntrophic anaerobic photosynthesis via direct interspecies electron transfer Ha, Phuc T.; Lindemann, Stephen R.; Shi, Liang Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms13924	journal	January 2017
Visualization of charge propagation along individual pili proteins using ambient electrostatic force microscopy Malvankar, Nikhil S.; Yalcin, Sibel Ebru; Tuominen, Mark T. Nature Nanotechnology, Vol. 9, Issue 12 https://doi.org/10.1038/nnano.2014.236	journal	October 2014
Extracellular electron transfer mechanisms between microorganisms and minerals Shi, Liang; Dong, Hailiang; Reguera, Gemma Nature Reviews Microbiology, Vol. 14, Issue 10 https://doi.org/10.1038/nrmicro.2016.93	journal	August 2016
A comprehensive guide to pilus biogenesis in Gram-negative bacteria Hospenthal, Manuela K.; Costa, Tiago R. D.; Waksman, Gabriel Nature Reviews Microbiology, Vol. 15, Issue 6 https://doi.org/10.1038/nrmicro.2017.40	journal	May 2017
Electron transfer in syntrophic communities of anaerobic bacteria and archaea Stams, Alfons J. M.; Plugge, Caroline M. Nature Reviews Microbiology, Vol. 7, Issue 8 https://doi.org/10.1038/nrmicro2166	journal	August 2009
A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria Light, Samuel H.; Su, Lin; Rivera-Lugo, Rafael Nature, Vol. 562, Issue 7725 https://doi.org/10.1038/s41586-018-0498-z	journal	September 2018
Stimulation of carbon nanomaterials on syntrophic oxidation of butyrate in sediment enrichments and a defined coculture Zhang, Wei; Zhang, Jianchao; Lu, Yahai Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30745-7	journal	August 2018
Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire Filman, David J.; Marino, Stephen F.; Ward, Joy E. Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0448-9	journal	June 2019
Thermally activated charge transport in microbial protein nanowires Lampa-Pastirk, Sanela; Veazey, Joshua P.; Walsh, Kathleen A. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23517	journal	March 2016
A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua Energy Environ. Sci., Vol. 7, Issue 1 https://doi.org/10.1039/C3EE42189A	journal	January 2014
Conductivity of individual Geobacter pili Adhikari, Ramesh Y.; Malvankar, Nikhil S.; Tuominen, Mark T. RSC Advances, Vol. 6, Issue 10 https://doi.org/10.1039/C5RA28092C	journal	January 2016
Promoting direct interspecies electron transfer with activated carbon Liu, Fanghua; Rotaru, Amelia-Elena; Shrestha, Pravin M. Energy & Environmental Science, Vol. 5, Issue 10 https://doi.org/10.1039/c2ee22459c	journal	January 2012
The genome of Syntrophus aciditrophicus: Life at the thermodynamic limit of microbial growth McInerney, M. J.; Rohlin, L.; Mouttaki, H. Proceedings of the National Academy of Sciences, Vol. 104, Issue 18 https://doi.org/10.1073/pnas.0610456104	journal	April 2007
Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis Akashi, Hiroshi; Gojobori, Takashi Proceedings of the National Academy of Sciences, Vol. 99, Issue 6 https://doi.org/10.1073/pnas.062526999	journal	March 2002
Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism Cologgi, D. L.; Lampa-Pastirk, S.; Speers, A. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 37, p. 15248-15252 https://doi.org/10.1073/pnas.1108616108	journal	September 2011
Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens Aklujkar, M.; Coppi, M. V.; Leang, C. Microbiology, Vol. 159, Issue Pt_3 https://doi.org/10.1099/mic.0.064089-0	journal	January 2013
The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism: Importance of interspecies hydrogen and formate transfer Sieber, Jessica R.; Le, Huynh M.; McInerney, Michael J. Environmental Microbiology, Vol. 16, Issue 1 https://doi.org/10.1111/1462-2920.12269	journal	October 2013
Effect of dilution on methanogenesis, hydrogen turnover and interspecies hydrogen transfer in anoxic paddy soil Conrad, Ralf; Babbel, Monika FEMS Microbiology Letters, Vol. 62, Issue 1 https://doi.org/10.1111/j.1574-6968.1989.tb03654.x	journal	January 1989
Temporal change of gas metabolism by hydrogen-syntrophic methanogenic bacterial associations in anoxic paddy soil Conrad, Ralf; Mayer, Hans-Peter; WÃ¼st, Monika FEMS Microbiology Letters, Vol. 62, Issue 4 https://doi.org/10.1111/j.1574-6968.1989.tb03701.x	journal	June 1989
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria Summers, Z. M.; Fogarty, H. E.; Leang, C. Science, Vol. 330, Issue 6009, p. 1413-1415 https://doi.org/10.1126/science.1196526	journal	December 2010
Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils Holmes, Dawn E.; Shrestha, Pravin M.; Walker, David J. F. Applied and Environmental Microbiology, Vol. 83, Issue 9 https://doi.org/10.1128/AEM.00223-17	journal	March 2017
Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua Applied and Environmental Microbiology, Vol. 80, Issue 15 https://doi.org/10.1128/AEM.00895-14	journal	May 2014
Interspecies Electron Transfer via Hydrogen and Formate Rather than Direct Electrical Connections in Cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens Rotaru, Amelia-Elena; Shrestha, Pravin M.; Liu, Fanghua Applied and Environmental Microbiology, Vol. 78, Issue 21 https://doi.org/10.1128/AEM.01946-12	journal	August 2012
A Geobacter sulfurreducens Strain Expressing Pseudomonas aeruginosa Type IV Pili Localizes OmcS on Pili but Is Deficient in Fe(III) Oxide Reduction and Current Production Liu, Xing; Tremblay, Pier-Luc; Malvankar, Nikhil S. Applied and Environmental Microbiology, Vol. 80, Issue 3 https://doi.org/10.1128/AEM.02938-13	journal	December 2013
Transcriptomic and Genetic Analysis of Direct Interspecies Electron Transfer Shrestha, Pravin Malla; Rotaru, Amelia-Elena; Summers, Zarath M. Applied and Environmental Microbiology, Vol. 79, Issue 7 https://doi.org/10.1128/AEM.03837-12	journal	February 2013
Gas Metabolism Evidence in Support of the Juxtaposition of Hydrogen-Producing and Methanogenic Bacteria in Sewage Sludge and Lake Sediments Conrad, R.; Phelps, T. J.; Zeikus, J. G. Applied and Environmental Microbiology, Vol. 50, Issue 3 https://doi.org/10.1128/AEM.50.3.595-601.1985	journal	January 1985
Control of Interspecies Electron Flow during Anaerobic Digestion: Significance of Formate Transfer versus Hydrogen Transfer during Syntrophic Methanogenesis in Flocs Thiele, Jurgen H.; Zeikus, J. Gregory Applied and Environmental Microbiology, Vol. 54, Issue 1 https://doi.org/10.1128/AEM.54.1.20-29.1988	journal	January 1988
Diffusion of the Interspecies Electron Carriers H2 and Formate in Methanogenic Ecosystems and Its Implications in the Measurement of Km for H2 or Formate Uptake Boone, David R.; Johnson, Richard L.; Liu, Yitai Applied and Environmental Microbiology, Vol. 55, Issue 7 https://doi.org/10.1128/AEM.55.7.1735-1741.1989	journal	January 1989
Evidence for anaerobic syntrophic benzoate degradation threshold and isolation of the syntrophic benzoate degrader. Hopkins, B. T.; McInerney, M. J.; Warikoo, V. Applied and environmental microbiology, Vol. 61, Issue 2 https://doi.org/10.1128/AEM.61.2.526-530.1995	journal	January 1995
Development of a Genetic System for Geobacter sulfurreducens Coppi, M. V.; Leang, C.; Sandler, S. J. Applied and Environmental Microbiology, Vol. 67, Issue 7, p. 3180-3187 https://doi.org/10.1128/AEM.67.7.3180-3187.2001	journal	July 2001
Structural Basis for Metallic-Like Conductivity in Microbial Nanowires Malvankar, Nikhil S.; Vargas, Madeline; Nevin, Kelly mBio, Vol. 6, Issue 2 https://doi.org/10.1128/mBio.00084-15	journal	March 2015
Aromatic Amino Acids Required for Pili Conductivity and Long-Range Extracellular Electron Transport in Geobacter sulfurreducens Vargas, Madeline; Malvankar, Nikhil S.; Tremblay, Pier-Luc mBio, Vol. 4, Issue 2 https://doi.org/10.1128/mBio.00105-13	journal	March 2013
Potential for Direct Interspecies Electron Transfer in Methanogenic Wastewater Digester Aggregates Morita, Masahiko; Malvankar, Nikhil S.; Franks, Ashley E. mBio, Vol. 2, Issue 4 https://doi.org/10.1128/mBio.00159-11	journal	August 2011
Aromatic Amino Acids Required for Pili Conductivity and Long-Range Extracellular Electron Transport in Geobacter sulfurreducens Vargas, Madeline; Malvankar, Nikhil S.; Tremblay, Pier-Luc mBio, Vol. 4, Issue 2 https://doi.org/10.1128/mBio.00210-13	journal	April 2013
Geobacter Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms Ueki, Toshiyuki; Nevin, Kelly P.; Rotaru, Amelia-Elena mBio, Vol. 9, Issue 4 https://doi.org/10.1128/mBio.01273-18	journal	July 2018
The Archaellum of Methanospirillum hungatei Is Electrically Conductive Walker, David J. F.; Martz, Eric; Holmes, Dawn E. mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mbio.00579-19	journal	April 2019
Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens Yields Pili with Exceptional Conductivity Tan, Yang; Adhikari, Ramesh Y.; Malvankar, Nikhil S. mBio, Vol. 8, Issue 1 https://doi.org/10.1128/mbio.02203-16	journal	January 2017
Syntrophy Goes Electric: Direct Interspecies Electron Transfer Lovley, Derek R. Annual Review of Microbiology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-micro-030117-020420	journal	September 2017
Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation Sieber, Jessica R.; McInerney, Michael J.; Gunsalus, Robert P. Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-090110-102844	journal	October 2012
Anode Biofilm Transcriptomics Reveals Outer Surface Components Essential for High Density Current Production in Geobacter sulfurreducens Fuel Cells Nevin, Kelly P.; Kim, Byoung-Chan; Glaven, Richard H. PLoS ONE, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pone.0005628	journal	May 2009
Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens Yields Pili with Exceptional Conductivity R., Lovley, Derek; Yang, Tan,; Y., Adhikari, Ramesh The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/9mrz-ax63	text	January 2017
A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Light, Samuel H.; Su, Lin; Rivera-Lugo, Rafael Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.70978	text	January 2018
Link between capacity for current production and syntrophic growth in Geobacter species Rotaru, Amelia-Elena; Woodard, Trevor L.; Nevin, Kelly P. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00744	journal	July 2015
Expanding the Diet for DIET: Electron Donors Supporting Direct Interspecies Electron Transfer (DIET) in Defined Co-Cultures Wang, Li-Ying; Nevin, Kelly P.; Woodard, Trevor L. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00236	journal	March 2016
The Low Conductivity of Geobacter uraniireducens Pili Suggests a Diversity of Extracellular Electron Transfer Mechanisms in the Genus Geobacter Tan, Yang; Adhikari, Ramesh Y.; Malvankar, Nikhil S. Frontiers in Microbiology, Vol. 07 https://doi.org/10.3389/fmicb.2016.00980	journal	June 2016
Electron and Proton Flux for Carbon Dioxide Reduction in Methanosarcina barkeri During Direct Interspecies Electron Transfer Holmes, Dawn E.; Rotaru, Amelia-Elena; Ueki, Toshiyuki Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03109	journal	December 2018
Geobacter Protein Nanowires Lovley, Derek R.; Walker, David J. F. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02078	journal	September 2019
The electrically conductive pili of Geobacter Species are a recently evolved feature for extracellular electron transfer Holmes, Dawn E.; Dang, Yan; Walker, David J. F. Microbiology Society https://doi.org/10.6084/m9.figshare.3395002	dataset	January 2016
The electrically conductive pili of Geobacter Species are a recently evolved feature for extracellular electron transfer Holmes, Dawn E.; Dang, Yan; Walker, David J. F. Microbiology Society https://doi.org/10.6084/m9.figshare.3395002.v1	dataset	January 2016

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