GEOMICROBIOLOGY

Sediment reactions defy dogma Kenneth H. Nealson

Redox reactions in widely spatially separated layers of marine sediments are coupled to each other. This suggests that bacteria mediate the flow of electrons between the layers — an idea that would previously have been dismissed.

To a human, 12 millimetres doesn’t seem like much of a distance. But to a bacterium it amounts to 10,000 body lengths — equiva-lent to about 20 kilometres in human terms. With this in mind, the report by Nielsen et al.1 on page 1071 of this issue is truly astonish-ing. The authors show that microbes can

respond to chemical changes across millimetre distances in marine sediments, thus altering the subsurface chemistry of those sediments. The phenomenon is initiated so quickly that it can’t involve molecular diffusion — the usual means by which chemical changes are transmitted through sedimentary layers.

Figure 1 | The tropical-cyclone heat pump. a, In this satellite image of Typhoon Kirogi (year 2000), a cold wake can be seen that has been created by cool water brought to the surface by enhanced vertical mixing. b, Simulation in an ocean-circulation model of the wake forced by tropical-cyclone winds at the ocean’s surface. c, The vertical structure of the modelled wake (boxed area in b) shows warming below the cold anomaly owing to heat from the surface that has been pumped down into the ocean interior, where it can be

transported by the large-scale circulation. In regions such as the subtropical central Pacific, cyclone mixing may influence the shallow wind-driven ‘overturning’ circulation, which flows towards the Equator at depth and feeds into the equatorial undercurrent. The warm water returns to the surface in the eastern equatorial Pacific. Fedorov et al.2 argue that increased tropical-cyclone activity in the Pacific, and the heat pump produced by vertical mixing, contributed to permanent El Niño-like conditions during the early Pliocene.

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that pumps heat from the surface down into the oceanic interior (Fig. 1).

This scenario sets up a possible feedback mechanism able to sustain El Niño-like temperature patterns in the equatorial Pacific, as follows. Extreme tropical-cyclone surface winds vigorously stir the normally well-strati-fied waters of the upper ocean, bringing cold water up to the surface and pumping warm surface water downwards (Fig. 1). In the central Pacific, much of the heat pumped down-wards is carried by the shallow wind-driven ‘overturning’ circulation towards the Equator, where it eventually returns to the surface in the equatorial upwelling regions in the eastern Pacific. The net result is warmer surface waters in the equatorial Pacific and, more generally, warmer ocean surface temperatures through-out the tropics. These conditions contribute to sustaining the increased tropical-cyclone activ-ity and the associated vertical ocean mixing, thus closing the feedback loop.

Using a fully coupled ocean–atmosphere general circulation model, Fedorov et al.2 include an idealized representation of tropical cyclones by prescribing additional ocean mix-ing along latitudes at which tropical cyclones occur. In doing so, they are able to simulate a climate state very similar to that thought to have occurred during the early Pliocene — including the permanent El Niño-like surface-temperature structure.

These results are promising but repre-sent only a preliminary step in including the effects of tropical cyclones in climate models. Tropical cyclones trigger short episodes of extremely vigorous ocean mixing. The tran-sient and extreme nature of these events cannot be captured using prescribed mixing values that are constant in space and time. Furthermore, it is not yet clear how much ocean mixing is done by tropical cyclones on a global scale. The authors use mixing esti-mates from previous work based on the global surface-temperature response to cyclones4,8, but those findings were largely exploratory and are first-order estimates at best. Additional

insight into the question could be provided by using, for example, a more sophisticated ocean-modelling approach that incorporates tropical-cyclone wind-forcing on a global scale.

Tropical cyclones may be transient, but they can modify the large-scale atmospheric and oceanic environments. Thus, feedbacks may occur that limit their intensity and formation. Idealized modelling approaches that prescribe the effects of cyclones cannot capture such feedbacks, which could influence the amount of ocean mixing, and the eventual heat transport. Further work is needed to reflect the full extent of ocean–atmosphere feedbacks associated with tropical cyclones.

As to the future, much of what we presume to understand about oceanic responses to global warming rests on the assumption that a warmer (and therefore more strongly stratified) tropi-cal ocean will undergo less mixing1,9. Fedorov and colleagues’ findings2 challenge this idea: they suggest that warmer tropical oceans will actually mix more because warmer climates will experience more tropical cyclones. If they are correct, a fundamental shift will be needed in our perception of processes in the tropical

ocean in the context of a changing climate. Furthermore, given the strong evidence

that there will be a substantial increase in the frequency of intense tropical cyclones over the next century10, and the fact that the strongest cyclones cause the largest amount of ocean mixing8, the results of Fedorov et al. may have implications for the future incidence of El Niño events. Such events could become a much more prevalent feature of Earth’s climate. ■

Ryan L. Sriver is in the Department of

Meteorology, The Pennsylvania State University,

University Park, Pennsylvania 16802-5013, USA.

e-mail: rsriver@psu.edu

1. Fedorov, A. V. et al. Science 312, 1485–1489 (2006).

2. Fedorov, A. V., Brierley, C. M. & Emanuel, K. Nature 463, 1066–1070 (2010).

3. Emanuel, K. J. Geophys. Res. 106, 14771–14781 (2001).

4. Sriver, R. L. & Huber, M. Nature 447, 577–580 (2007).

5. Korty, R. L. et al. J. Clim. 21, 638–654 (2008).

6. Jansen, M. & Ferrari, R. Geophys. Res. Lett. 36, doi:10.1029/2008GL036796 (2009).

7. Wunsch, C. & Ferrari, R. Annu. Rev. Fluid Mech. 36, 281–314

(2004).

8. Sriver, R. L., Huber, M. & Nusbaumer, J. Geochem. Geophys.

Geosyst. 9, doi:10.1029/2007GC001842 (2008).

9. Philander, S. G. & Fedorov, A. V. Paleoceanography 18, doi:10.1029/2002PA000837 (2003).

10. Bender, M. A. et al. Science 327, 454–458 (2010).

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Marine sediments typically become anoxic because the bacteria within them consume oxygen as it diffuses down from the overlying water. This process establishes a series of sedi-mentary layers, within which a different kind of molecule (or ion) accepts electrons from oxygen and is consumed to form a chemi-cally reduced product (Fig. 1). In one of the lower layers, sulphate (SO4

2–) is converted to highly toxic hydrogen sulphide (H2S), which accumulates and poisons the environment for most oxygen-consuming microorganisms. The hydrogen sulphide can, in turn, be converted into sulphate or other oxidized forms of sul-phur by bacteria that use inorganic material as an energy source.

Nielsen et al.1 worked with sediments in which oxygen could diffuse to a depth of a couple of centimetres. When they replaced oxygenated water in this region (the oxic zone) with anoxic water, they observed a rapid chemical response in the underlying sediments: within an hour, the sulphide layer began to move upward, most probably because less hydrogen sulphide was being consumed by bacteria than before. By contrast, when the authors replenished the water overlying the sediments with oxygen, creating a new oxic zone, the sulphide layer began to recede within an hour as more hydro-gen sulphide was consumed. In concert with this increase in sulphide consumption, Nielsen and colleagues recorded a rise in pH near the oxic–anoxic interface. This is consistent with a reaction taking place in the zone in which oxy-gen reacts to produce water, consuming protons in the process (and so increasing the pH).

The authors argue1 that the only explanation for these results is that some mechanism oper-ates in which bacteria allow electrons to flow from deeper sediments to the surface, coupling redox reactions in the sulphide layer with those in the oxic zone (Fig. 1). What’s more, they pro-pose that this unknown mechanism allows not only chemical communication, but also the transport of energy (in the form of electrons) across distances normally regarded as being far greater than any distance-scale associated with bacterial metabolism. They argue convincingly that the rapidity of these responses requires nearly real-time connections, which can’t be explained by diffusive processes across such distances. They also contend that the rise in pH in the oxic zone is not caused by the direct reaction of oxygen with other chemical species found in anoxic sediments, as such reactions would not consume protons.

Instead, the authors propose three possi-ble mechanisms to account for the observed electron flow: enzymes on bacterial outer membranes might transport electrons to solid substrates in the subsurface; conductive ‘nanowires’ might connect microbial cells, creating a network of bacteria that spans large distances in sediments; or other sedimen-tary components might be responsible, such as metallic conductors or the mineral pyrite. Such hypotheses would at one time have been

considered heretical to those in the field, but discoveries made in the past few years now make these arguments tenable.

Let’s start with the first proposed mecha-nism. Two groups of bacteria, Geobacter2 and Shewanella3, have well-characterized enzymes in their outer membranes that are capable of extra cellular electron transport — the bact-eria use the enzymes for the respiration of solid substrates, such as metal oxides. In support of the second hypothesis, the same two groups of bacteria also have conductive nanowires, either in the form of pilins4 (hair-like appendages) or pilin-like proteins that are associated with multi-haem cytochrome enzymes5,6 (which are capa-ble of electron transport). Although pilins and pilin-like proteins contain conductive materials, to date, no one has demonstrated that they can actually conduct electrons along their lengths.

As for the third suggested mechanism (that sedimentary components mediate electron flow), Nielsen and colleagues1 note several lines of evidence in support of this idea, including conductivity measurements of sediments7,8, and demonstrations of electric-current pro-duction by sediment batteries9–11 (which exploit naturally occurring voltage differences between anoxic sedimentary layers and the overlying

Figure 1 | Coupled reactions in marine sediments. Marine sediments typically consist of several layers. Oxygen from overlying water diffuses into the top layer of sediment (the oxic zone), where it is reduced by bacteria to form water. Lower sedimentary layers are anoxic, and are characterized by different reaction cycles in which nitrate, manganese(iv) or iron(iii) ions are reduced and re-oxidized by microbial activity. Nielsen et al.1 report that a reaction in one of the anoxic layers, in which hydrogen sulphide (H2S) is oxidized by bacteria to produce sulphur, is coupled to the oxygen-reduction reaction in the oxic layer. The coupling of these reactions can be explained only if electrons (e–) produced from the oxidation are rapidly transported to the oxic layer, to be used in the reduction. The authors propose that bacteria mediate the electron flow.

oxic zone). No mechanism for the con-ductivity recorded in these studies7–11 has been established, however.

So why should we care about Nielsen and colleagues’ findings? One rea-son is that their data may be relevant to energy transfer and electron flow through many different environments, not just the sediments studied1. If so, the microbe-mediated, electronic coupling of distant regions might act as much more than just a rapid mechanism for removing toxic hydrogen sulphide from subsurface sediments.

In fact, the authors note1 that even if all of the subsurface hydrogen sul-

phide was consumed, it would account for only part of the electron flow measured

at the oxic surface of the sediments. This might mean that a variety of other reactions in anoxic sediments are also mediated by rapid electron flow to the surface, such as the oxida-tion of organic carbon, or of inorganic electron acceptors found in such environments. This in turn would implicate electron flow in processes such as bioremedia tion, corrosion and carbon sequestration in sediments.

Finally, one of the tenets of anaerobic microbiology is that of ‘interspecies hydrogen exchange’ — a mechanism in which hydrogen is consumed by one microorganism to drive an otherwise slow or thermodynamically unfavourable reaction performed by another. Pro cesses such as anaerobic methane oxidation are thought to use such a mechanism, although no hydrogen transfer has yet been proved. Microbial electron transfer could accomplish the same catalytic feat, perhaps faster and more specifically (so that electrons are trans-ferred directly between only the right kinds of organisms) than hydrogen transfer. If so, new paradigms will emerge in the fields of micro-bial energetics and metabolism, and perhaps also in ecology and evolution. As Nielsen and colleagues’ study1 has shown, the time is ripe for microbiologists to open themselves up to unusual ideas. ■

Kenneth H. Nealson is in the Department of Earth

Sciences, University of California, Los Angeles,

Los Angeles, California 90089-0740, USA.

e-mail: knealson@usc.edu

1. Nielsen, L. P., Risgaard-Petersen, N., Fossing, H.,

Christensen, P. B. & Sayama, M. Nature 463, 1071–1074

(2010).

2. Lovley, D. R. Nature Rev. Microbiol. 4, 497–508 (2006).

3. Fredrickson, J. K. et al. Nature Rev. Microbiol. 6, 592–603

(2008).

4. Reguera, G. et al. Nature 435, 1098–1101 (2005).

5. Gorby, Y. A. et al. Proc. Natl Acad. Sci. USA 103, 11358–11363

(2006).

6. El-Naggar, M. Y., Gorby, Y. A., Xia, W. & Nealson, K. H.

Biophys. J. 95, L10–L12 (2008).

7. Sato, M. & Mooney, H. M. Geophysics 25, 226–249 (1960).

8. Ntarlagiannis, D., Atekwana, E. A., Hill, E. A. & Gorby, Y.

Geophys. Res. Lett. 34, L17305 (2007).

9. Rabaey, K. et al. ISME J. 1, 9-18 (2007).

10. Reimers, C. E., Tender, L. M., Fertig, S. & Wang, W. Environ.

Sci. Technol. 35, 192–195 (2001).

11. Ryckelynck, N., Stecher, H. A. & Reimers, C. E.

Biogeochemistry 76, 113–139 (2005).

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