Nature | Article

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Filamentous bacteria transport electrons over centimetre distances

Journal name:
Nature
Volume:
491,
Pages:
218–221
Date published:
DOI:
doi:10.1038/nature11586
Received
Accepted
Published online

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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  1. Filamentous Desulfobulbaceae in current-producing sediments.
    Figure 1: Filamentous Desulfobulbaceae in current-producing sediments.

    a, Microprofiles of O2, pH and ΣH2S (ΣH2S = ([H2S] + [HS−] + [S2−]). b, Tuft of filamentous Desulfobulbaceae collected from the sulphide-free zone. c, Filamentous Desulfobulbaceae identified by fluorescence in situ hybridization targeting 16S rRNA. Filament cells appear yellow from overlay of images obtained with probe DSB706 (labelled green) and probe ELF654 (labelled red); other cells appear blue from DNA-staining with 4′,6-diamidino-2-phenylindole (DAPI). d, Phylogenetic affiliation (by maximum likelihood) of the filaments based on 16S rRNA sequences. Scale bar, 10% estimated sequence divergence; filled and open circles show bootstrap support >80% and >60%, respectively (by maximum parsimony; 1,000 iterations); the specificity of the probes used for FISH is indicated by the green and yellow shading. Accession numbers are given in Supplementary Table 1.

  2. Biogeochemical impacts of filament cutting.
    Figure 2: Biogeochemical impacts of filament cutting.

    a–c, Microprofiles of oxygen, sulphide and pH measured in undisturbed sediment cores (a), 10–60 min (b) and 1 day (c) after passing a thin tungsten wire (50 µm diameter) horizontally through the sediment near the oxic–anoxic interface. Data are presented as mean values ± s.e.m. (oxygen and pH, n = 9; sulphide, n = 6). Volume-specific rates of oxygen consumption rates (grey areas) are calculated from numerical modelling of the measured oxygen concentration profiles.

  3. Biogeochemical effects of filter pore size.
    Figure 3: Biogeochemical effects of filter pore size.

    a–c, Depth distributions of oxygen concentrations (red circles) and pH (blue circles) measured after 20 days of incubation in sediment cores containing polycarbonate filters with different pore sizes: 2.0 µm (a), 0.8 µm (b) and 0.22 µm (c). The filter position is indicated by the dashed line. Volume-specific rates of oxygen consumption (grey bars) were estimated from numerical modelling of the oxygen concentration profiles. Data are presented as mean values ± s.e.m. (n = 6).

  4. Effect of layer of glass beads intercalated in the sediment.
    Figure 4: Effect of layer of glass beads intercalated in the sediment.

    a, Oxygen concentrations (red lines), pH (blue lines) and sulphide concentrations (black lines) in three sediment cores with an intercalated layer of electrically inert glass microspheres reaching from 3 mm down to 8 mm sediment depth (hatched area). b, Micrograph showing filamentous Desulfobulbaceae extracted from a glass bead section and hybridized with the specific ELF654 FISH probe. DAPI-stained chromosomes are visible in some cells of the filament.

  5. AFM, SEM, TEM and EFM micrographs of the filamentous Desulfobulbaceae.
    Figure 5: AFM, SEM, TEM and EFM micrographs of the filamentous Desulfobulbaceae.

    a, SEM image of four cells. b, c, Thin-section TEM images of filament cross sections. d, e, Longitudinal section including a cell–cell junction (d) and oblique section of cell–cell junction (e). f, Height AFM image of cell–cell junction with inserted topographic curve along 500 nm line with the same scaling of x, y and z axes. g, 1 × 1 µm EFM image above cell–cell junction with lighter contrast closely following the ridge topography mapped in the preceding AFM scan (not shown).

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

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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

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 financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

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

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Supplementary information

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  1. Supplementary Information (452K)

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

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