Published August 22, 2025 | Version Published
Journal Article Open

Redox conduction facilitates direct interspecies electron transport in anaerobic methanotrophic consortia

  • 1. ROR icon Peking University
  • 2. ROR icon University of Southern California
  • 3. ROR icon California Institute of Technology
  • 4. ROR icon University of Bremen
  • 5. ROR icon Max Planck Institute for Marine Microbiology

Abstract

Anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) form syntrophic partnerships in marine sediments to consume greenhouse gas methane. While direct interspecies electron transport is proposed to enable ANME/SRB symbiosis, its electrochemical properties remain uncharacterized. Here, using sediment-free enrichment cultures, we measured the electron transport capabilities of marine consortia under physiological conditions. Diverse ANME/SRB consortia exhibited high dry conductance close to electrogenic biofilms. This conductance diminished upon exposure to heat or oxygen but was preserved following paraformaldehyde fixation, indicating a biomolecular origin for this electric charge transfer. Cyclic voltammetry revealed redox activity centered at 28 ± 11, 94 ± 6, and 24 ± 7 millivolts for ANME-1/Desulfofervidus, ANME-2a/Seep-SRB1, and ANME-2a+2c/Seep-SRB1+2 consortia, respectively. Generator-collector measurements further demonstrated that these redox components facilitate electron transport over micrometer-scale distances, sufficient to link archaeal and bacterial partners. Collectively, our results establish that marine ANME/SRB symbiosis uses redox conduction, consistent with multiheme cytochrome c, for direct interspecies electron transport.

Copyright and License

© 2025 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

Acknowledgement

We thank S. Menger, A. Seebeck, and S. Connon for assistance with continuous cultivation of the anaerobic methanotrophic enrichment cultures. We thank J. Leadbetter for providing access to laboratory facilities. Disclaimer: This report was prepared as an account of work sponsored by an agency of the US government. Neither the US government nor any agency thereof, nor any of their employees, makes any warranty, express or implied; assumes any legal liability or responsibility for the accuracy, completeness, or usefulness of any information, apparatus, product, or process disclosed; or represents that its use would not infringe privately owned rights. Reference herein to any specific commercial product, process, or service by trade name, trademark, manufacturer, or otherwise does not necessarily constitute or imply its endorsement, recommendation, or favoring by the US government or any agency thereof. The views and opinions of authors expressed herein do not necessarily state or reflect those of the US government or any agency thereof.

Funding

Work in the M.Y.E.-N. laboratory was supported by the US Department of Energy, Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences (DE-FG02-13ER16415) and the Air Force Office of Scientific Research (FA9550-19-1-0249). Work in V.J.O. laboratory was supported by the US Department of Energy, Office of Science, Office of Biological and Environmental Research (DE-SC0022991). Work in H.Y. laboratory was supported by the National Natural Science Foundation of China (no. 42377109). Work in G.W. laboratory was supported by Germany’s Excellence Initiative/Strategy through the Cluster of Excellence “The Ocean Floor-Earth’s Uncharted Interface” (EXC-2077–390741603).

Data Availability

The 16S rRNA gene amplicon sequences from the sediment-free enrichment cultures have been deposited in the National Center for Biotechnology Information (NCBI) under BioProject accession no. PRJNA758896 (www.ncbi.nlm.nih.gov/sra/PRJNA758896). All other data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.

Supplemental Material

Figs. S1 to S7 (PDF)

Files

sciadv.adw4289.pdf

Files (4.1 MB)

Name Size Download all
md5:c6139cbb709e7f0a240d90826ae31045
769.8 kB Preview Download
md5:a98c2a965fa740b93a0e64abb58e02bd
3.3 MB Preview Download

Additional details

Identifiers

Related works

Describes
Journal Article: 40845095 (PMID)
Journal Article: PMC12372872 (PMCID)
Is supplemented by
Dataset: http://www.ncbi.nlm.nih.gov/sra/PRJNA758896 (URL)
Supplemental Material: https://www.science.org/doi/suppl/10.1126/sciadv.adw4289/suppl_file/sciadv.adw4289_sm.pdf (URL)

Funding

United States Department of Energy
DE-FG02-13ER16415
United States Air Force Office of Scientific Research
FA9550-19-1-0249
United States Department of Energy
DE-SC0022991
National Natural Science Foundation of China
42377109
Deutsche Forschungsgemeinschaft
EXC-2077–390741603

Dates

Accepted
2025-07-22

Caltech Custom Metadata

Caltech groups
Division of Geological and Planetary Sciences (GPS)
Publication Status
Published