NEWS & VIEWS
NATURE|Vol 464|25 March 2010
a
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Carbon input to soils
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Carbon lost from soils from fresh carbon inputs
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Carbon lost from decomposition of old carbon in soils
Figure 1 | Possible mechanisms driving increased soil respiration (RS) in a warming climate. a, An increase in RS could occur through a rise in the decomposition rate of old soil organic carbon, leading to a net loss from the global pool of soil carbon to the atmosphere. b, If carbon inputs to the soil increase, higher RS could derive from enhanced release of fresh carbon. In this second case, there would be no net loss of carbon from the global soil pool. The findings of Bond-Lamberty and Thomson4 leave open which of these processes — if not a combination of them — is likely to dominate.
content of soil organic carbon (its state) within a reasonable time period. A third is measur ing the components of carbon output, particu larly in distinguishing between output due to increased respiration from plant roots and the immediate root environment, and output due to respiration from free-living microbes in the bulk soil. These have often been referred to as autotrophic and heterotrophic respiration (RA and RH, respectively), but the distinction between them is blurred because of the close association of plants and soil organisms. BondLamberty and Thomson’s findings show that total RS has increased, and suggest that both RA and RH have also risen. A barrier to reliably pre dicting the future of global fluxes of soil organic carbon to the atmosphere is the uncertainty associated with measuring all three components of soil carbon cycling (input–state–output). Bond-Lamberty and Thomson’s analysis4
also throws up a curiosity in northern soils. The authors fit a single global model to all of the RS data from 1989 to 2008, which gives a positive global relationship between RS and tempera ture. An unexpected result, however, is that the RS data from the boreal and Arctic regions, when examined in isolation, show a significant negative relationship with temperature, which is unexpected from previous studies6–10. This finding adds an intriguing aspect to the debate about how northern soils will respond to climate change, in which the following fac tors have to be taken into account. The boreal and Arctic regions are projected to experience greater than average climate warming1; they contain some of the largest soil carbon stocks on Earth11; the permafrost experiences seasonal temperatures either side of 0 °C such that small levels of warming could have profound effects on biological activity and carbon fluxes9; and
BIOGEOCHEMISTRY
NO connection with methane Ronald S. Oremland Microorganisms that grow by oxidizing methane come in two basic types, aerobic and anaerobic. Now we have something in between that generates its own supply of molecular oxygen by metabolizing nitric oxide. On page 543 of this issue, Ettwig et al.1 report their discovery of a new type of methaneoxidizing (methanotrophic) bacterium, pro visionally dubbed Methylomirabilis oxyfera. As its name suggests, this microbe does something quite unexpected: the process involved could provide another angle on our understanding of the biology and chemistry of the early Earth, and perhaps even extend to the possibility of 500
life on other methane-rich bodies in the Solar System. Methylomirabilis oxyfera conducts what seems to be an anaerobic, nitrite-linked oxi dation of methane (CH4) via a denitrification pathway to yield nitogen and carbon diox ide. But Ettwig et al. show that this organism defies convention and, by means of a putative nitric oxide (NO) dismutase enzyme, reacts to
permafrost processes and highly organic soils such as peats are relatively poorly described in current coupled carbon-cycle–climate (C4) models12,13. For all these reasons, the response of northern soils to climate change is a fertile area for future research. At the global level, however, Bond-Lamberty and Thomson’s elegant analysis lends strong support to the hypothesis that soil carbon fluxes will increase in a warming climate. The outcomes of their meta-analysis should further drive efforts to develop methods to disaggre gate the underlying processes contributing to RS. Without understanding these processes, it will not be possible to accurately predict the net response of soil carbon stores to climate change — and that is a central question for determin ing the biospheric feedbacks between the carbon cycle and climate. ■ Pete Smith is at the Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Aberdeen AB24 3UU, UK. Changming Fang is at the Coastal Ecosystems Research Station of Yangtze River Estuary, Institute of Biodiversity Science, Fudan University, Shanghai 200433, China. e-mails:
[email protected];
[email protected]
1. Batjes, N. H. Eur. J. Soil. Sci. 47, 151–163 (1996). 2. Smith, P., Fang, C., Dawson, J. J. C. & Moncrieff, J. B. Adv. Agron. 97, 1–43 (2008). 3. Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Nature 408, 184–187 (2000). 4. Bond-Lamberty, B. & Thomson, A. Nature 464, 579–582 (2010). 5. IPCC Working Group I Climate Change 2007: The Physical Science Basis (Cambridge Univ. Press, 2007). 6. Shaver, G. R. et al. J. Ecol. 94, 740–753 (2006). 7. Tarnocai, C. Glob. Planet. Change 53, 222–232 (2006). 8. Ström, L. & Christensen, T. R. Soil Biol. Biochem. 39, 1689–1698 (2007). 9. Zimov, S. A., Schuur, E. A. G. & Chapin, F. S. Science 312, 1612–1613 (2006). 10. Dorrepaal, E. et al. Nature 460, 616–619 (2009). 11. Gorham, E. Ecol. Appl. 1, 182–195 (1991). 12. Friedlingstein, P. et al. J. Clim. 19, 3337–3353 (2006). 13. Ostle, N. J. et al. J. Ecol. 97, 851–863 (2009).
produce N2 and oxygen. The intracellular O2 produced is used to metabolize methane via the well-described pathway of aerobic meth anotrophy initiated by the enzyme methane monooxygenase (Fig. 1a). NO dismutase is one of just a handful of enzymes that are known to evolve molecular oxygen. Hence, M. oxyfera can consume methane in anoxic environ ments that are rich in nitrogen oxides, such as the freshwater sloughs contaminated with nitrogenous fertilizer run-off investigated by Ettwig and colleagues. Nevertheless, the bac terium is at heart a cryptic aerobe, but rather than getting its O2 from the atmosphere, it gen erates its own from the ambient nitrite. Essen tially, it contains its own little scuba tank that allows it to ‘breathe’ oxygen while immersed in methane-rich anoxic muck, thereby accessing the methane that conventional methanotrophs cannot reach.
NEWS & VIEWS
NATURE|Vol 464|25 March 2010
Methane is nature’s simplest hydrocarbon. It first endeared itself to me when I was an under graduate slogging through my first semester of organic chemistry. One simple carbon atom surrounded by four hydrogen atoms: ah, but an entire course could be structured around this deceptively simple molecule and its relevance to such topics as basic microbiology, planetary evolution, geochemistry, petroleum geology, energy economics, global warming and even astrobiology. The basic fact here is that methane burns well and has economic value. It is the prime component of natural gas, and is also renew able via the degradation of fermentable organic molecules in concert with microbes referred to as methanogenic archaea (Fig. 1b). Moreover, it exists as enormous deposits on the sea floor in solid form as a clathrate2, in principle offer ing a way to solve our energy problems. But here lies the rub. After water vapour and CO2, methane is the most important greenhouse gas in Earth’s troposphere (the lowest 10 kilome tres or so of the atmosphere). If massive release
a Methylomirabilis oxyfera
of methane comes from the breakdown of sea bed clathrates, as may have occurred in the distant past3, there would be a rapid and highly disruptive pattern of global change. Enter the methanotrophs, which make a living by consuming methane, either by inter ception on its upward transit from sites of biological production or geological storage, or by uptake from the troposphere. By oxidizing methane to CO2 they reduce its outward flux to the atmosphere and, along with reaction with hydroxyl radicals, help to regulate methane abundance in the troposphere4. There are two known routes by which meth ane can be oxidized and support the growth of microorganisms: aerobic and anaerobic. The aerobic pathway has been well studied and is characterized by Methylococcus capsulatus, which oxidizes methane with molecular oxy gen, forming CO2, water and biomass (Fig. 1c). These bacteria are isolated by classic means, and their cellular workings have been unrav elled by standard biochemistry, now greatly aided by the progress made in DNA sequencing
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Nitrate reducers
Methanogenesis Complex organics
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O2 Oxic Anoxic CH4
SRB ANME
CO2 + 2H2O
CH4 + 2O2 Methylococcus capsulatus
SO42– + 2H+
H2S CH4
[?]
CO2 + 2H2O
Figure 1 | Four modes of methane metabolism by microorganisms. a, Nitrite-linked methane (CH4) oxidation by Methylomirabilis oxyfera1. Nitrate (NO3–) is reduced to nitrite (NO2–) by other microbes; M. oxyfera reduces the nitrite to nitric oxide (NO), after which it undergoes a dismutative reaction to yield N2 and O2. This intracellular oxygen is the ultimate oxidant for a conventional ‘aerobic’ pathway of methane oxidation (c) initiated by particulate methane monooxygenase. b, Methanogenesis by anaerobic processing of organic matter, yielding fermentation products, and then H2 and CO2, which serve as substrates for consumption by methanogenic archaea. c, Aerobic oxidation of methane, as displayed by bacteria such as Methylococcus capsulatus that can exploit the interfaces between methane-rich anoxic environments and oxygen-rich aerobic environments to obtain supplies of both gases. d, Reverse methanogenesis: anaerobic oxidation of methane (AOM) involving an archaeon (designated ANME) related to the methanogens. The ANME microbe oxidizes the methane in a sequence opposite to that of methane formation in b. An unknown intermediate [?] is exchanged between the ANME and sulphate-reducing bacteria (SRB). The sulphate-reducers act in a relationship that ultimately allows the carbon in methane to be oxidized to CO2, and the electrons generated by that reaction reduce sulphate (SO42–) to hydrogen sulphide (H2S).
and genetics, and with computer databases. Anaerobic oxidation of methane is a more complicated story. It was first postulated by marine geochemists, who observed verti cal profiles of methane abundance in anoxic marine systems that suggested in situ biologi cal consumption, with sulphate acting as the ultimate oxidant, or terminal electron accep tor. This is analogous to how O2 works in the aerobic pathway, but sulphate is a much weaker oxidant than O2 and hence the reaction does not yield much energy for bacterial growth. The fact that these microbes could not be cul tivated made microbiologists (myself included) discount the phenomenon. But technological advances have changed the game: recalcitrant microbes need not be cultivated to support astonishing findings. Thus, it emerged that a specialized group of anaerobic microorgan isms, closely related to the methanogenic archaea (‘ANMEs’), conduct the reverse reac tion, and make a living by oxidizing methane back to CO2, with sulphate-reducing bacteria acting in a mutually beneficial relationship5 (Fig. 1d). Ettwig and colleagues’ studies1 involved detailed metagenomic analyses and bio chemical assays of cultures that were highly enriched in M. oxyfera, and with their dis covery we have something that lies in the grey area between aerobic and anaerobic methane oxidation (Fig. 1a). The broader question is what importance a process such as that medi ated by M. oxyfera has beyond the confines of anoxic agricultural streams. Is it a biologi cal adaptation responding to environmental niches created by human-induced pollution? Is it something more significant with respect to Earth’s history, harking back to the times before the great oxidation event (about 2.45 billion years ago), when our planet’s atmosphere was devoid of oxygen and was presumably meth ane-rich? Or maybe it was a means to harness the abundant methane of Earth’s middle years, when a still-limited oxygen tension allowed for the oxidation of ammonium and the accumu lation of ‘suboxic’ anions such as nitrite to serve as electron acceptors. Such concepts go beyond the realm of Earth, and can be extrapolated to Mars (where meth ane is present as an atmospheric trace gas) or even Titan (where it occurs as liquid precipi tation and shallow lakes). Do alien, anaero bic microbes exist somewhere on these orbs to take advantage of the abundant supply of carbon and energy that methane supplies? ■ Ronald S. Oremland is in the National Research Program, Water Resources Division, US Geological Survey, Menlo Park, California 94025, USA. e-mail:
[email protected] 1. Ettwig, K. F. et al. Nature 464, 543–548 (2010). 2. Kvenvolden, K. A. Chem. Geol. 71, 41–51 (1988). 3. Kennett, J. P., Cannariato, K. G., Hendy, I. L. & Behl, R. J. Science 288, 128–133 (2000). 4. Reeburgh, W. S. Chem. Rev. 107, 486–513 (2007). 5. Thauer, R. K. & Shima, S. Ann. NY Acad. Sci. 1125, 158–170 (2008).
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