Abstract

Oxygen consumption in marine sediments is often coupled to the oxidation of sulphide generated by degradation of organic matter in deeper, oxygen-free layers. Geochemical observations have shown that this coupling can be mediated by electric currents carried by unidentified electron transporters across centimetre-wide zones. Here we present evidence that the native conductors are long, filamentous bacteria. They abounded in sediment zones with electric currents and along their length they contained strings with distinct properties in accordance with a function as electron transporters. Living, electrical cables add a new dimension to the understanding of interactions in nature and may find use in technology development.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Accessions

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

All sequences are deposited in GenBank/EMBL/DDBJ under accession numbers JX091023JX091073.

References

  1. 1.

    in Marine Geochemistry (eds & ) 173–207 (Springer, 2000)

  2. 2.

    , , , & Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463, 1071–1074 (2010)

  3. 3.

    , , & Sulfur, iron-, and calcium cycling associated with natural electric currents running through marine sediment. Geochim. Cosmochim. Acta 92, 1–13 (2012)

  4. 4.

    , & Microbial interspecies electron transfer via electric currents through conductive minerals. Proc. Natl Acad. Sci. USA 109, 10042–10046 (2012)

  5. 5.

    et al. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nature Geosci. 3, 417–421 (2010)

  6. 6.

    , & Continuous periplasm in a filamentous, heterocyst-forming cyanobacterium. Mol. Microbiol. 65, 1139–1145 (2007)

  7. 7.

    , & Near-static dielectric polarization of individual carbon nanotubes. Nano Lett. 7, 2729–2733 (2007)

  8. 8.

    et al. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc. Natl Acad. Sci. USA 107, 18127–18131 (2010)

  9. 9.

    et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005)

  10. 10.

    , & Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl. Environ. Microbiol. 70, 1234–1237 (2004)

  11. 11.

    et al. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330, 1413–1415 (2010)

  12. 12.

    , , , & Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc. Natl Acad. Sci. USA 108, 15248–15252 (2011)

  13. 13.

    Reactive iron in marine-sediments. Geochim. Cosmochim. Acta 53, 619–632 (1989)

  14. 14.

    et al. Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374, 713–715 (1994)

  15. 15.

    et al. Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J. 1, 341–353 (2007)

  16. 16.

    , , , & Impact of bacterial NO3 transport on sediment biogeochemistry. Appl. Environ. Microbiol. 71, 7575–7577 (2005)

  17. 17.

    , & An amperometric microsensor for the determination of H2S in aquatic environments. Anal. Chem. 68, 4351–4357 (1996)

  18. 18.

    An oxygen microsensor with a guard cathode. Limnol. Oceanogr. 34, 474–478 (1989)

  19. 19.

    & Microelectrodes: their use in microbial ecology. Adv. Microb. Ecol. 9, 293–352 (1986)

  20. 20.

    , , , & Quantitative noncontact electrostatic force imaging of nanocrystal polarizability. J. Phys. Chem. B 107, 1525–1531 (2003)

Download references

Acknowledgements

The authors thank P. G. Sørensen and L. B. Pedersen for construction of microsensors. Thanks to K. E. Thomsen for operating the TEM. B. B. Jørgensen is thanked for his general support. This research was financially supported by the European Research Council (L.P.N.), the Danish National Research Foundation (N.R.-P., C.P., K.U.K., L.S., M.D.), the Danish Council for Independent Research | Natural Sciences (FNU) (L.P.N.), the German Max Planck Society (N.R.-P., C.P., K.U.K., L.S.) and the Villum Foundation (M.D.).

Author information

Affiliations

  1. Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark

    • Christian Pfeffer
    • , Kasper Urup Kjeldsen
    • , Lars Schreiber
    • , Andreas Schramm
    • , Nils Risgaard-Petersen
    •  & Lars Peter Nielsen
  2. Section for Microbiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark

    • Steffen Larsen
    • , Rikke Louise Meyer
    • , Andreas Schramm
    •  & Lars Peter Nielsen
  3. Centre for DNA Nanotechnology (CDNA), Interdisciplinary Nanoscience Center (iNANO), Aarhus University, 8000 Aarhus C, Denmark

    • Jie Song
    • , Mingdong Dong
    • , Flemming Besenbacher
    •  & Rikke Louise Meyer
  4. Department of Biological Sciences, University of Southern California, Los Angeles, California 90089, USA

    • Yuri A. Gorby
    •  & Kar Man Leung
  5. Department of Physics and Astronomy, University of Southern California, Los Angeles, California 90089, USA

    • Mohamed Y. El-Naggar
    •  & Kar Man Leung

Authors

  1. Search for Christian Pfeffer in:

  2. Search for Steffen Larsen in:

  3. Search for Jie Song in:

  4. Search for Mingdong Dong in:

  5. Search for Flemming Besenbacher in:

  6. Search for Rikke Louise Meyer in:

  7. Search for Kasper Urup Kjeldsen in:

  8. Search for Lars Schreiber in:

  9. Search for Yuri A. Gorby in:

  10. Search for Mohamed Y. El-Naggar in:

  11. Search for Kar Man Leung in:

  12. Search for Andreas Schramm in:

  13. Search for Nils Risgaard-Petersen in:

  14. Search for Lars Peter Nielsen in:

Contributions

This study was conceived by L.P.N., N.R.-P. and A.S. Experimental work: C.P. FISH and molecular phylogeny: S.L. Single-cell identification: K.U.K. and L.S. AFM: R.L.M., J.S. and M.D. SEM and EFM: J.S., M.D. and F.B. TEM: L.P.N. and J.S. Conductivity measurements using nanofabricated electro discs: J.S., Y.A.G., M.Y.E.-N., K.M.L. and C.P. All authors contributed to discussions of the data and preparation of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Nils Risgaard-Petersen or Lars Peter Nielsen.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Methods, Supplementary Figure 1, Supplementary Table 1 and Supplementary References.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature11586

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Newsletter Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing