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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]
  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.
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. doi:10.1128/aem.00223-17.
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. doi:10.1128/aem.00223-17. https://www.osti.gov/servlets/purl/1536857.
@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 = {2017},
month = {3}
}

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    • DOI: 10.1128/mbio.01273-18

    Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome
    journal, October 2018


    Stratification of Diversity and Activity of Methanogenic and Methanotrophic Microorganisms in a Nitrogen-Fertilized Italian Paddy Soil
    journal, November 2017

    • Vaksmaa, Annika; van Alen, Theo A.; Ettwig, Katharina F.
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.02127

    Comparative Metatranscriptomics of Wheat Rhizosphere Microbiomes in Disease Suppressive and Non-suppressive Soils for Rhizoctonia solani AG8
    journal, May 2018


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

    Geobacter Protein Nanowires
    journal, September 2019