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Filamentous bacteria transport electrons over centimetre distances

Nature volume 491, pages 218–221 (2012)Cite this article

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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.

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Figure 1: Filamentous Desulfobulbaceae in current-producing sediments.
Figure 2: Biogeochemical impacts of filament cutting.
Figure 3: Biogeochemical effects of filter pore size.
Figure 4: Effect of layer of glass beads intercalated in the sediment.
Figure 5: AFM, SEM, TEM and EFM micrographs of the filamentous Desulfobulbaceae.

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GenBank/EMBL/DDBJ

Data deposits

All sequences are deposited in GenBank/EMBL/DDBJ under accession numbers JX091023–JX091073.

References

  1. Jørgensen, B. B. in Marine Geochemistry (eds Schulz, H. D. & Zabel, M. ) 173–207 (Springer, 2000)

    Book  Google Scholar 

  2. Nielsen, L. P., Risgaard-Petersen, N., Fossing, H., Christensen, P. B. & Sayama, M. Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463, 1071–1074 (2010)

    Article  ADS  CAS  Google Scholar 

  3. Risgaard-Petersen, N., Revil, A., Meister, P. & Nielsen, L. P. Sulfur, iron-, and calcium cycling associated with natural electric currents running through marine sediment. Geochim. Cosmochim. Acta 92, 1–13 (2012)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  6. Mariscal, V., Herrero, A. & Flores, E. Continuous periplasm in a filamentous, heterocyst-forming cyanobacterium. Mol. Microbiol. 65, 1139–1145 (2007)

    Article  CAS  Google Scholar 

  7. Lu, W., Wang, D. & Chen, L. W. Near-static dielectric polarization of individual carbon nanotubes. Nano Lett. 7, 2729–2733 (2007)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  10. Holmes, D. E., Bond, D. R. & Lovley, D. R. Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl. Environ. Microbiol. 70, 1234–1237 (2004)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  12. Cologgi, D. L., Lampa-Pastirk, S., Speers, A. M., Kelly, S. D. & Reguera, G. Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc. Natl Acad. Sci. USA 108, 15248–15252 (2011)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. Sayama, M., Risgaard-Petersen, N., Nielsen, L. P., Fossing, H. & Christensen, P. B. Impact of bacterial NO3− transport on sediment biogeochemistry. Appl. Environ. Microbiol. 71, 7575–7577 (2005)

    Article  CAS  Google Scholar 

  17. Jeroschewski, P., Steuckart, C. & Kuhl, M. An amperometric microsensor for the determination of H2S in aquatic environments. Anal. Chem. 68, 4351–4357 (1996)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  19. Revsbech, N. P. & Jorgensen, B. B. Microelectrodes: their use in microbial ecology. Adv. Microb. Ecol. 9, 293–352 (1986)

    Article  Google Scholar 

  20. Cherniavskaya, O., Chen, L. W., Weng, V., Yuditsky, L. & Brus, L. E. Quantitative noncontact electrostatic force imaging of nanocrystal polarizability. J. Phys. Chem. B 107, 1525–1531 (2003)

    Article  CAS  Google Scholar 

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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.).

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Authors and Affiliations

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

    Christian Pfeffer, Kasper Urup Kjeldsen, Lars Schreiber, Andreas Schramm, Nils Risgaard-Petersen & Lars Peter Nielsen

  2. Department of Bioscience, Section for Microbiology, Aarhus University, Aarhus C, 8000, Denmark

    Steffen Larsen, Rikke Louise Meyer, Andreas Schramm & Lars Peter Nielsen

  3. Centre for DNA Nanotechnology (CDNA), Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus C, 8000, Denmark

    Jie Song, Mingdong Dong, Flemming Besenbacher & Rikke Louise Meyer

  4. Department of Biological Sciences, University of Southern California, Los Angeles, 90089, California, USA

    Yuri A. Gorby & Kar Man Leung

  5. Department of Physics and Astronomy, University of Southern California, Los Angeles, 90089, California, USA

    Mohamed Y. El-Naggar & Kar Man Leung

Authors
  1. Christian Pfeffer
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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.

Corresponding authors

Correspondence to Nils Risgaard-Petersen or Lars Peter Nielsen.

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The authors declare no competing financial interests.

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This file contains Supplementary Methods, Supplementary Figure 1, Supplementary Table 1 and Supplementary References. (PDF 452 kb)

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Pfeffer, C., Larsen, S., Song, J. et al. Filamentous bacteria transport electrons over centimetre distances. Nature 491, 218–221 (2012). https://doi.org/10.1038/nature11586

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