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Title: Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils

Abstract

The possibility thatMethanothrix(formerlyMethanosaeta) andGeobacterspecies cooperate via direct interspecies electron transfer (DIET) in terrestrial methanogenic environments was investigated in rice paddy soils. Genes with high sequence similarity to the gene for the PilA pilin monomer of the electrically conductive pili (e-pili) ofGeobacter sulfurreducensaccounted for over half of the PilA gene sequences in metagenomic libraries and 42% of the mRNA transcripts in RNA sequencing (RNA-seq) libraries. This abundance of e-pilin genes and transcripts is significant because e-pili can serve as conduits for DIET. Most of the e-pilin genes and transcripts were affiliated withGeobacterspecies, but sequences most closely related to putative e-pilin genes from genera such asDesulfobacterium,Deferribacter,Geoalkalibacter, andDesulfobacula, were also detected. Approximately 17% of all metagenomic and metatranscriptomic bacterial sequences clustered withGeobacterspecies, and the finding thatGeobacterspp. were actively transcribing growth-related genes indicated that they were metabolically active in the soils. Genes coding for e-pilin were among the most highly transcribedGeobactergenes. In addition, homologs of genes encoding OmcS, ac-type cytochrome associated with the e-pili ofG. sulfurreducensand required for DIET, were also highly expressed in the soils.Methanothrixspecies in the soils highly expressed genes for enzymes involved in the reduction of carbon dioxide to methane. DIET is the only electron donor known to support CO2reduction inMethanothrix.more » Thus, these results are consistent with a model in whichGeobacterspecies were providing electrons toMethanothrixspecies for methane production through electrical connections of e-pili.Methanothrixspecies are some of the most important microbial contributors to global methane production, but surprisingly little is known about their physiology and ecology. The possibility that DIET is a source of electrons forMethanothrixin methanogenic rice paddy soils is important because it demonstrates that the contribution thatMethanothrixmakes to methane production in terrestrial environments may extend beyond the conversion of acetate to methane. Furthermore, defined coculture studies have suggested that whenMethanothrixspecies receive some of their energy from DIET, they grow faster than when acetate is their sole energy source. Thus,Methanothrixgrowth and metabolism in methanogenic soils may be faster and more robust than generally considered. The results also suggest that the reason thatGeobacterspecies are repeatedly found to be among the most metabolically active microorganisms in methanogenic soils is that they grow syntrophically in cooperation withMethanothrixspp., and possibly other methanogens, via DIET.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [3];  [3];  [3]; ORCiD logo [3];  [3]
+ Show Author Affiliations
  1. Western New England Univ., Springfield, MA (United States). Dept. of Physical and Biological Sciences; Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology
  2. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology; Univ. of California Berkeley, Berkeley, CA (United States). Energy Biosciences Inst.
  3. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology
Publication Date:
Research Org.:
Univ. of Massachusetts, Amherst, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1536857
Grant/Contract Number:  
SC0004485
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 83; Journal Issue: 9; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Microbiology

Citation Formats

Holmes, Dawn E., Shrestha, Pravin M., Walker, David J. F., Dang, Yan, Nevin, Kelly P., Woodard, Trevor L., Lovley, Derek R., and Schloss, Patrick D. Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils. United States: N. p., 2017. Web. doi:10.1128/aem.00223-17.
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Holmes, Dawn E., Shrestha, Pravin M., Walker, David J. F., Dang, Yan, Nevin, Kelly P., Woodard, Trevor L., Lovley, Derek R., & Schloss, Patrick D. Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils. United States. https://doi.org/10.1128/aem.00223-17
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Holmes, Dawn E., Shrestha, Pravin M., Walker, David J. F., Dang, Yan, Nevin, Kelly P., Woodard, Trevor L., Lovley, Derek R., and Schloss, Patrick D. Fri . "Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils". United States. https://doi.org/10.1128/aem.00223-17. https://www.osti.gov/servlets/purl/1536857.
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@article{osti_1536857,
title = {Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils},
author = {Holmes, Dawn E. and Shrestha, Pravin M. and Walker, David J. F. and Dang, Yan and Nevin, Kelly P. and Woodard, Trevor L. and Lovley, Derek R. and Schloss, Patrick D.},
abstractNote = {The possibility thatMethanothrix(formerlyMethanosaeta) andGeobacterspecies cooperate via direct interspecies electron transfer (DIET) in terrestrial methanogenic environments was investigated in rice paddy soils. Genes with high sequence similarity to the gene for the PilA pilin monomer of the electrically conductive pili (e-pili) ofGeobacter sulfurreducensaccounted for over half of the PilA gene sequences in metagenomic libraries and 42% of the mRNA transcripts in RNA sequencing (RNA-seq) libraries. This abundance of e-pilin genes and transcripts is significant because e-pili can serve as conduits for DIET. Most of the e-pilin genes and transcripts were affiliated withGeobacterspecies, but sequences most closely related to putative e-pilin genes from genera such asDesulfobacterium,Deferribacter,Geoalkalibacter, andDesulfobacula, were also detected. Approximately 17% of all metagenomic and metatranscriptomic bacterial sequences clustered withGeobacterspecies, and the finding thatGeobacterspp. were actively transcribing growth-related genes indicated that they were metabolically active in the soils. Genes coding for e-pilin were among the most highly transcribedGeobactergenes. In addition, homologs of genes encoding OmcS, ac-type cytochrome associated with the e-pili ofG. sulfurreducensand required for DIET, were also highly expressed in the soils.Methanothrixspecies in the soils highly expressed genes for enzymes involved in the reduction of carbon dioxide to methane. DIET is the only electron donor known to support CO2reduction inMethanothrix. Thus, these results are consistent with a model in whichGeobacterspecies were providing electrons toMethanothrixspecies for methane production through electrical connections of e-pili.Methanothrixspecies are some of the most important microbial contributors to global methane production, but surprisingly little is known about their physiology and ecology. The possibility that DIET is a source of electrons forMethanothrixin methanogenic rice paddy soils is important because it demonstrates that the contribution thatMethanothrixmakes to methane production in terrestrial environments may extend beyond the conversion of acetate to methane. Furthermore, defined coculture studies have suggested that whenMethanothrixspecies receive some of their energy from DIET, they grow faster than when acetate is their sole energy source. Thus,Methanothrixgrowth and metabolism in methanogenic soils may be faster and more robust than generally considered. The results also suggest that the reason thatGeobacterspecies are repeatedly found to be among the most metabolically active microorganisms in methanogenic soils is that they grow syntrophically in cooperation withMethanothrixspp., and possibly other methanogens, via DIET.},
doi = {10.1128/aem.00223-17},
journal = {Applied and Environmental Microbiology},
number = 9,
volume = 83,
place = {United States},
year = {Fri Mar 03 00:00:00 EST 2017},
month = {Fri Mar 03 00:00:00 EST 2017}
}
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https://doi.org/10.1128/aem.00223-17
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    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.02127

    Geobacteraceae are important members of mercury-methylating microbial communities of sediments impacted by waste water releases
    journal, January 2018

    Methanogens and Iron-Reducing Bacteria: the Overlooked Members of Mercury-Methylating Microbial Communities in Boreal Lakes
    journal, September 2018

    • Bravo, Andrea G.; Peura, Sari; Buck, Moritz
    • Applied and Environmental Microbiology, Vol. 84, Issue 23
    • DOI: 10.1128/aem.01774-18

    Geobacter Protein Nanowires
    journal, September 2019

    Syntrophic growth with direct interspecies electron transfer between pili-free Geobacter species
    journal, June 2018

    Electron and Proton Flux for Carbon Dioxide Reduction in Methanosarcina barkeri During Direct Interspecies Electron Transfer
    journal, December 2018

    • Holmes, Dawn E.; Rotaru, Amelia-Elena; Ueki, Toshiyuki
    • Frontiers in Microbiology, Vol. 9
    • DOI: 10.3389/fmicb.2018.03109

    Metatranscriptomic Evidence for Magnetite Nanoparticle-Stimulated Acetoclastic Methanogenesis under Continuous Agitation
    journal, September 2019

    • Inaba, Ryo; Nagoya, Misa; Kouzuma, Atsushi
    • Applied and Environmental Microbiology, Vol. 85, Issue 23
    • DOI: 10.1128/aem.01733-19

    Metatranscriptomic insights into microbial consortia driving methane metabolism in paddy soils
    journal, March 2018

    Electro-Microbiology as a Promising Approach Towards Renewable Energy and Environmental Sustainability
    journal, July 2018

    The mechanisms of biochar interactions with microorganisms in soil
    journal, September 2019

    • Gorovtsov, Andrey V.; Minkina, Tatiana M.; Mandzhieva, Saglara S.
    • Environmental Geochemistry and Health, Vol. 42, Issue 8
    • DOI: 10.1007/s10653-019-00412-5

    Construction of a Geobacter Strain With Exceptional Growth on Cathodes
    journal, July 2018

    Stimulation of carbon nanomaterials on syntrophic oxidation of butyrate in sediment enrichments and a defined coculture
    journal, August 2018

    Stimulation of Smithella ‐dominating propionate oxidation in a sediment enrichment by magnetite and carbon nanotubes
    journal, March 2019

    • Xia, Xingxuan; Zhang, Jianchao; Song, Tianze
    • Environmental Microbiology Reports, Vol. 11, Issue 2
    • DOI: 10.1111/1758-2229.12737

    The chemodiversity of paddy soil dissolved organic matter correlates with microbial community at continental scales
    journal, October 2018

    Extracellular electron uptake in Methanosarcinales is independent of multiheme c-type cytochromes
    journal, January 2020

    Stimulation of carbon nanomaterials on syntrophic oxidation of butyrate in sediment enrichments and a defined coculture
    journal, August 2018

    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

    Electron and Proton Flux for Carbon Dioxide Reduction in Methanosarcina barkeri During Direct Interspecies Electron Transfer
    journal, December 2018

    • Holmes, Dawn E.; Rotaru, Amelia-Elena; Ueki, Toshiyuki
    • Frontiers in Microbiology, Vol. 9
    • DOI: 10.3389/fmicb.2018.03109

    Geobacter Protein Nanowires
    journal, September 2019

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