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Filamentous Bacteria Transport Electrons Over Centimetre Distances ARTICLE doi:10.1038/nature11586 Filamentous bacteria transport electrons over centimetre distances Christian Pfeffer1, Steffen Larsen2, Jie Song3, Mingdong Dong3, Flemming Besenbacher3, Rikke Louise Meyer2,3, Kasper Urup Kjeldsen1, Lars Schreiber1, Yuri A. Gorby4, Mohamed Y. El-Naggar5, Kar Man Leung4,5, Andreas Schramm1,2, Nils Risgaard-Petersen1 & Lars Peter Nielsen1,2 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. Marine sediments become anoxic because oxygen is consumed by micro- identity to any cultured member of this family (Fig. 1d). Almost bial processes at the surface. Without available oxygen the microorgan- identical (. 99%) 16S rRNA sequences were detected in the suboxic isms living below the surface are supposed to depend on energetically less zones of three replicate cores (Fig. 1d), whereas they were absent in the favourable, anaerobic processes1. Recently, however, electric currents subjacent sulphidic zones. The filaments were identified and quan- have been found to directly connect oxygen reduction at the surface with tified in the sediments by fluorescence in situ hybridization (FISH) sulphide oxidation in the subsurface2, even when oxygen and sulphide with specific 16S rRNA-targeting probes (Fig. 1c). The length density are separated by more than 1 cm. Half of the sediment oxygen consump- of filaments was at least 117 m cm23 in the oxic and suboxic sediment tion can be driven by electrons transported from below2,3. The spatial zone and no filaments were detected in the deeper sulphidic zone. separation of oxidation and reduction processes invokes steep pH gra- With an average cell length of 3 mm, this length density corresponded dients leading to distinct dissolutions and precipitations of minerals3. to 4 3 107 cells cm23. Individual filaments were difficult to dissect out Microbial activity apparently drives the electrochemical half-reactions without breaking them, however, fragments up to 1.5 cm long were and the establishment of electron-conducting structures through the recorded, supporting that the bacteria had the length to span the sediment2. Bacterial nanowires, humus particles and semi-conductive entire suboxic zone. mineral grains are known to conduct electrons over nanometre to micro- metre distances, and alone or in combination they have been proposed to Desulfobulbaceae filaments qualify as conductors facilitate electron transport over centimetre distances in marine sedi- We demonstrated experimentally that electron transport through the ment2,4,5. Experimental tests and observations have failed to confirm suboxic zone was mediated by a coherent structure like a bacterial these proposals so far, and instead we have unexpectedly found long, filament and not by diffusive electron shuttles or casual contact filamentous bacteria structured like electric cables as reported below. between conductive elements. Evidence for solid conductors was found by passing a very thin tungsten wire (50 mm diameter) hori- Filamentous Desulfobulbaceae in electric sediment zontally through sediment 1–2 mm below the oxic–anoxic interface, When sulphidic defaunated marine sediment was incubated in the thus transiently interrupting the sediment continuum (see Sup- dark with overlying oxic sea water, the porewater chemistry gradually plementary Information for details). The cut resulted in an immediate developed in accordance with the establishment of an electron trans- and lasting halt of the electron transport, as indicated by a significant port mechanism that coupled oxygen reduction at the sediment sur- drop in oxygen consumption (Tukey’s test under analysis of variance face to sulphide oxidation in deeper anoxic layers (Fig. 1a). As (ANOVA); P , 0.001; alpha 5 0.05; n 5 27), attenuation of the pH described previously2,3, the electric coupling of spatially segregated peak in the oxic zone and contraction of the suboxic zone (Fig. 2), the processes was evident from (1) the presence of a distinct pH peak latter being similar to the response to momentary oxygen removal demonstrating aerobic proton consumption—an indicator of electro- observed in a previous study2. The role of bacteria in establishing a chemical oxygen reduction2,3—and (2) the formation of a 12–15-mm centimetre-long electron transport mechanism was further investi- deep suboxic zone separating sulphide oxidation from the associated gated in incubations, where filters with defined pore sizes were oxygen reduction2,3. When sediment from the top 20 mm was gently inserted into sediment cores to selectively exclude or permit vertical washed, tufts of entangled filamentous bacteria appeared (Fig. 1b). growth or migration of bacteria. Manifestations of long-distance elec- Reverse transcription, cloning and sequencing of 16S ribosomal RNA tron transport appeared in cores containing filter barriers with pore from dissected filaments identified them as novel members of the sizes of 2.0 mm (Fig. 3), but did not appear in cores containing filter deltaproteobacterial family Desulfobulbaceae with , 92% sequence barriers with pore sizes # 0.8 mm as indicated from significantly lower 1Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark. 2Section for Microbiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark. 3Centre for DNA Nanotechnology (CDNA), Interdisciplinary Nanoscience Center (iNANO), Aarhus University, 8000 Aarhus C, Denmark. 4Department of Biological Sciences, University of Southern California, Los Angeles, California 90089, USA. 5Department of Physics and Astronomy, University of Southern California, Los Angeles, California 90089, USA. 00 MONTH 2012 | VOL 000 | NATURE | 1 ©2012 Macmillan Publishers Limited. All rights reserved RESEARCH ARTICLE O2 consumption rate O2 consumption rate O2 consumption rate a 0 b (μmol cm–3 d–1) (μmol cm–3 d–1) (μmol cm–3 d–1) 02040600 2040600 204060 μ μ μ O2 concentration ( M) O2 concentration ( M) O2 concentration ( M) 0 100 200 300 400 0 100 200 300 400 0 100 200 300 400 5 a b c 0 0 0 1 1 1 2 2 2 10 O2 Before cutting 10–60 minutes after cutting 1 day after cutting 3 3 3 pH 5678 Σ Depth (mm) 5 5 H2S pH Depth (mm) 15 c 10 10 O2 consumption rate O2 concentration 15 pH 15 Σ H2 S concentration Sediment surfaces 20 200 μm 20 Cut line 20 5678 5678 pH pH 0 1020304050 0 1020304050 25 Σ μ Σ μ H2S ( M) H2S ( M) 678 pH 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 mm diameter) 0 100 200 300 horizontally through the sediment near the oxic–anoxic interface. Data are Σ μ [O2] or H2S ( M) presented as mean values 6 s.e.m. (oxygen and pH, n 5 9; sulphide, n 5 6). 5 μm Volume-specific rates of oxygen consumption rates (grey areas) are calculated from numerical modelling of the measured oxygen concentration profiles. Structure of Desulfobulbaceae filaments d Desulfobulbaceae DSB706 The multicellular Desulfobulbaceae filaments showed a unique struc- ture with uniform ridges running along their entire length (Fig. 5a). Desulfocapsa sulfexigens Transmission electron microscopy of thin sections showed two types Desulfonema Desulfurivibrio alkaliphilus of filaments that either had 15 ridges and were about 400 nm wide or magnum Desulfobacter had 17 ridges and were about 700 nm wide (Fig. 5b, c). Each ridge Desulfobulbus japonicus postgatei Desulfobulbus propionicus contained a filled, 70–100 nm wide channel between the cytoplasmic and the outer membrane. The adjacent cells within the filaments were Desulfovibrio Filament DNA separated by 200 nm wide gaps bridged by the ridge filling and tightly desulfuricans Filament RNA Sediment RNA wrapped up by the outer membrane, which seemed to encase the 0.10 Glass microsphere DNA entire filament (Fig. 5d, e). A similar collective outer membrane of ELF645 the filamentous multicellular cyanobacterium Anabaena sp. has been suggested to ease exchange of nutrients between cells without leakage Figure 1 | Filamentous Desulfobulbaceae in current-producing sediments. 6 2 22 to the surroundings . It is possible that the outer membrane of the a, Microprofiles of O2, pH and SH2S(SH2S 5 ([H2S] 1 [HS ] 1 [S ]). Desulfobulbaceae filaments has a similar function with respect to b, Tuft of filamentous Desulfobulbaceae collected from the sulphide-free zone. c, Filamentous Desulfobulbaceae identified by fluorescence in situ electrons. On the basis of all the morphological data, we propose that hybridization targeting 16S rRNA. Filament cells appear yellow from overlay of O2 consumption rate O2 consumption rate O2 consumption rate images obtained with probe DSB706 (labelled green) and probe ELF654 (μmol cm–3 d–1) (μmol cm–3 d–1) (μmol cm–3 d–1) (labelled red); other cells appear blue from DNA-staining with 49,6-diamidino- 020406002040600204060
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