Geochemical reactions in upper layers of marine sediments are coupled to those in deeper zones. It turns out that centimetre-long bacterial filaments acting as electrical cables are the metabolic link between the layers. See Article p.218
A few years ago, any suggestion that microbes could function as power cables to transmit electric currents across centimetre distances would have been met with scepticism. Yet this is exactly what Pfeffer et al.1 report report on page 218 of this issue. The authors provide compelling evidence linking the presence of long filaments of a previously unknown group of bacteria to the electric currents that couple spatially separated geochemical reactions in marine sedimentsFootnote 1.
In the oceans, atmospheric oxygen diffuses from the water into the upper layers of the underlying sediment. Here, it is rapidly consumed by microorganisms, which use the oxygen as the terminal acceptor of electrons that are generated during the metabolism of organic matter to gain energy for growth. As a result, oxygen concentrations drop sharply in the uppermost layer of the sediment (the oxic zone), leaving the deeper layers oxygen-free (anoxic). Microbes in the anoxic layers therefore rely on other electron-accepting molecules such as sulphate (SO42−) to fulfil their energy needs (Fig. 1). The transfer of electrons to sulphate, however, generates hydrogen sulphide (H2S), a gas that is toxic to oxygen-consuming organisms. Yet hydrogen sulphide levels can be controlled by microbes that convert it into sulphate or into other oxidized sulphur compounds.
Although the oxic and sulphide layers are typically separated by millimetres to centimetres of sediment, reductions in oxygen availability in the upper layer rapidly lead to the accumulation of hydrogen sulphide and the expansion of the sulphide region2. As soon as oxygen is available again, hydrogen sulphide consumption resumes and the sulphide layer recedes. The responses are so fast as to exclude mechanisms based on the diffusion of molecules, and they can be explained only by the action of electric currents.
Such electric currents might be mediated by bacterial conductive appendages (microbial nanowires)3,4,5, electron-shuttling solid phases (such as humic substances generated during the decomposition of organic matter)6 and/or conductive minerals7. However, evidence so far suggests that these mediators enable the flow of electrons only across nanometre to micrometre distances, whereas the oxic and sulphide sediment layers are typically separated by millimetre to centimetre distances.
Now Pfeffer et al. report that sulphidic marine sediments are densely colonized by long, multicellular bacterial filaments — some reaching lengths (up to 1.5 centimetres) that correspond well to the spatial separation of the oxic and sulphide layers. The authors provide experimental evidence that the filaments are required for the electrical coupling between sediment layers. For example, when they cut the filaments or used filters to prevent their passage, oxygen consumption in the upper region was reduced and the sulphide layer expanded.
The filamentous microbes belong to the family Desulfobulbaceae, a morphologically diverse group of bacteria with members previously shown8 to both generate and consume hydrogen sulphide; these reactions are localized to the space (periplasm) contained between the cytoplasmic (or inner) membrane and the outer membrane. Interestingly, the outer membrane of the filamentous microbes is structured as ridges, which define tubular channels of periplasm running along the cells, and continue as junctions between neighbouring cells. Furthermore, although the outer membrane of the ridges and junctions acts as an insulator, their internal content is highly charged. These unique structural and electrical properties hint at a potential mechanism for electron transfer involving the periplasmic conduits.
The authors propose a plausible model in which cells at one end of the filament oxidize hydrogen sulphide to supply electrons to the oxygen-consuming cells located at the opposite end (Fig. 1). However, the idea that the microbial filaments behave as living, centimetre-long power cords, presumably transporting electrons through continuous tubular channels, defies our understanding of biological electron transfer. Nevertheless, it is known that the periplasm of some bacteria that use metals as electron acceptors houses abundant metal-containing proteins, mostly of the cytochrome class, that allow electrons to flow from the inner to the outer membrane9. Cytochromes and microbial nanowires can transmit electric currents across micrometre-thick films formed by these bacteria. Therefore, similar mechanisms — but contained within tubular periplasmic ridges — might mediate long-range electron transfer in the Desulfobulbaceae filaments.
Pfeffer and colleagues' report raises questions about the ecological role of these bacteria as well. If widespread, the bacterial cables could constitute the main mechanism for the transport of electric currents in marine sulphidic sediments. However, it is unclear whether they act alone or in concert with other microbes. When the authors cut the filaments or prevented their permeation through the sediments with filters, they might have also disrupted other microbial electrical networks. Hence, to assess the exact contribution of the filaments to the electric currents of the sediments, it will be crucial to confirm that electrons can travel along the filaments and to measure the transport rates. Furthermore, the ability to consume the toxic hydrogen sulphide, if demonstrated, might allow the bacteria to outcompete other microbes, and promote metabolic interactions with others.
Finally, it should be noted that the bacterial cables might not simply provide a mechanism to cope with toxic hydrogen sulphide in sediments. Rather, they could enable a more widespread biological process for energy transfer and the coupling of spatially separated biogeochemical reactions. As noted in an earlier report2, hydrogen sulphide consumption in some subsurface sediments is not high enough to sustain the levels of oxygen consumption measured in the sediment's top layer. Thus, other biogeochemical reactions could be electrically coupled to the reduction of oxygen in sediments as well.
Pfeffer and colleagues' report adds to the growing body of evidence highlighting the crucial role that microbial electron transfer has in global geochemical processes and in the functioning of ecosystems. These are indeed exciting times for microbiologists, and the present work reminds us — one more time — just how much more awaits discovery.
*This article and the paper under discussion1 were published online on 24 October 2012.
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