geomicrobiology: methanotrophs in moss

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NATURE GEOSCIENCE | VOL 3 | SEPTEMBER 2010 | www.nature.com/naturegeoscience 595 news & views P eat bogs, prevalent in northern latitudes, store around a third of the Earth’s carbon 1 . Acidic, nutrient- depleted conditions in these bogs impede decomposition of organic matter, facilitating the formation of peat. Sphagnum mosses represent one of the dominant forms of vegetation in these systems. Anaerobic breakdown of these mosses produces large quantities of methane, a potent greenhouse gas. ere is growing concern that global warming will stimulate the anaerobic breakdown of peat mosses, and hence methane production. Writing in Nature Geoscience, Kip and colleagues 2 show that Sphagnum mosses form symbioses with methane-oxidizing bacteria — which have the potential to diminish methane release — in peat bog systems around the globe. Aerobic methane-oxidizing bacteria, known as methanotrophs, function as a terrestrial methane sink. Methanotrophs not only thrive as free-living bacteria in peatland soils, but also form symbioses with submerged Sphagnum mosses. Methanotrophs embedded in moss tissues collected from a peat bog in the Netherlands were found to convert methane to carbon dioxide, which was subsequently taken up by the plants 3 . However, the global extent of this symbiosis, together with its significance for attenuating methane emissions from peatland ecosystems, has remained uncertain. Kip and colleagues 2 collected Sphagnum mosses from the pools, lawns and hummocks of nine Sphagnum- dominated wetlands across the globe. ey observed significant rates of methane oxidation in all Sphagnum mosses; rates reached up to 80 μmol per day per gram dry weight in mosses sampled from northern Siberia. Oxidation was greatest in mosses collected from waterlogged pools and was lower in mosses collected from hummocks and lawns. e authors attribute the consumption of methane to a symbiotic association with methanotrophs, because in a laboratory experiment, methane oxidation ceased following the addition of acetylene, a compound that specifically inhibits methane oxidation by methanotrophs. Stable-isotope labelling experiments subsequently confirmed that methane-derived carbon was taken up by submerged mosses in the form of carbon dioxide (Fig. 1). e authors estimate that methane-derived carbon accounted for up to 35% of the carbon dioxide assimilated by Sphagnum mosses in these experiments. DNA-based microarray analyses revealed that the diversity of methanotrophs in the moss samples was surprisingly high for this specific ecological niche. One would expect a high diversity in the surrounding peat soils 4,5 , as the heterogeneous nature of soils creates different ecological niches, with differing concentrations of methane, oxygen and other essential nutrients. e symbiotic relationship seems to be mutually beneficial. Submerged Sphagnum is unable to access sufficient carbon dioxide from the atmosphere for photosynthesis owing to a lack of stomata, and would therefore benefit from a local, methanotrophic supply of carbon dioxide. Concomitantly, methanotrophs in submerged mosses would presumably benefit from a plant-derived supply of elevated oxygen concentrations, which would normally be supplied by diffusion from the atmosphere. Further findings from Kip et al. suggest that methanotrophic symbionts could help to counteract increased methane emissions from peat bogs in a warmer world. First, rates of methane oxidation almost doubled when the temperature of the incubations was raised from 10 °C to 20 °C. Second, methane emissions increased almost four-fold following removal of Sphagnum mosses from intact soil cores, suggesting that Sphagnum-associated methanotrophs — rather than free-living methanotrophs — are GEOMICROBIOLOGY Methanotrophs in moss Peat bogs release large quantities of methane to the atmosphere. A global survey of peat mosses reveals a ubiquitous symbiotic relationship with methane-oxidizing bacteria. Yin Chen and J. Colin Murrell Methane Oxygen Methane Mineralization of organic matter Symbiotic methanotrophs Other plants (e.g. Eriophorum) Rhizosphere methanotrophs Water Peat Methane Sphagnum Photosynthesis CO 2 Alternative carbon sources Figure 1 | Methane oxidation by methanotrophs in a peat bog. Kip et al. 2 reveal that Sphagnum mosses form symbioses with methane-consuming bacteria in Sphagnum-dominated peat bogs across the globe. Methane oxidation by the symbionts was greatest in submerged mosses. Carbon dioxide derived from methane oxidation — and potentially from methanotrophic utilization of alternative carbon sources — is taken up by the plants for photosynthesis. The symbiosis could help to explain why Sphagnum-dominated peatlands emit less methane than other peatland types that are dominated by vascular plants, which channel methane from the soil to the atmosphere. Free-living methanotrophs that inhabit the rhizosphere — the region of the soil influenced by roots — of peat-adapted plants also play an important role in methane oxidation. © 20 Macmillan Publishers Limited. All rights reserved 10

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nature geoscience | VOL 3 | SEPTEMBER 2010 | www.nature.com/naturegeoscience 595

news & views

Peat bogs, prevalent in northern latitudes, store around a third of the Earth’s carbon1. Acidic, nutrient-

depleted conditions in these bogs impede decomposition of organic matter, facilitating the formation of peat. Sphagnum mosses represent one of the dominant forms of vegetation in these systems. Anaerobic breakdown of these mosses produces large quantities of methane, a potent greenhouse gas. There is growing concern that global warming will stimulate the anaerobic breakdown of peat mosses, and hence methane production. Writing in Nature Geoscience, Kip and colleagues2 show that Sphagnum mosses form symbioses with methane-oxidizing bacteria — which have the potential to diminish methane release — in peat bog systems around the globe.

Aerobic methane-oxidizing bacteria, known as methanotrophs, function as a terrestrial methane sink. Methanotrophs not only thrive as free-living bacteria in peatland soils, but also form symbioses with submerged Sphagnum mosses. Methanotrophs embedded in moss tissues collected from a peat bog in the Netherlands were found to convert methane to carbon dioxide, which was subsequently taken up by the plants3. However, the global extent of this symbiosis, together with its significance for attenuating methane emissions from peatland ecosystems, has remained uncertain.

Kip and colleagues2 collected Sphagnum mosses from the pools, lawns and hummocks of nine Sphagnum-dominated wetlands across the globe. They observed significant rates of methane oxidation in all Sphagnum mosses; rates reached up to 80 μmol per day per gram dry weight in mosses sampled from northern Siberia. Oxidation was greatest in mosses collected from waterlogged pools and was lower in mosses collected from hummocks and lawns. The authors attribute the consumption of methane to a symbiotic association with methanotrophs, because in a laboratory experiment, methane oxidation ceased following the addition of acetylene, a compound that specifically inhibits methane oxidation by

methanotrophs. Stable-isotope labelling experiments subsequently confirmed that methane-derived carbon was taken up by submerged mosses in the form of carbon dioxide (Fig. 1). The authors estimate that methane-derived carbon accounted for up to 35% of the carbon dioxide assimilated by Sphagnum mosses in these experiments. DNA-based microarray analyses revealed that the diversity of methanotrophs in the moss samples was surprisingly high for this specific ecological niche. One would expect a high diversity in the surrounding peat soils4,5, as the heterogeneous nature of soils creates different ecological niches, with differing concentrations of methane, oxygen and other essential nutrients.

The symbiotic relationship seems to be mutually beneficial. Submerged Sphagnum is unable to access sufficient carbon dioxide from the atmosphere

for photosynthesis owing to a lack of stomata, and would therefore benefit from a local, methanotrophic supply of carbon dioxide. Concomitantly, methanotrophs in submerged mosses would presumably benefit from a plant-derived supply of elevated oxygen concentrations, which would normally be supplied by diffusion from the atmosphere.

Further findings from Kip et al. suggest that methanotrophic symbionts could help to counteract increased methane emissions from peat bogs in a warmer world. First, rates of methane oxidation almost doubled when the temperature of the incubations was raised from 10 °C to 20 °C. Second, methane emissions increased almost four-fold following removal of Sphagnum mosses from intact soil cores, suggesting that Sphagnum-associated methanotrophs — rather than free-living methanotrophs — are

geomICRobIology

methanotrophs in mossPeat bogs release large quantities of methane to the atmosphere. A global survey of peat mosses reveals a ubiquitous symbiotic relationship with methane-oxidizing bacteria.

yin Chen and J. Colin murrell

Methane Oxygen

Methane

Mineralization oforganic matter

Symbioticmethanotrophs

Other plants(e.g. Eriophorum)

Rhizospheremethanotrophs

WaterPeat

Methane

Sphagnum

PhotosynthesisCO2

Alternativecarbon sources

Figure 1 | Methane oxidation by methanotrophs in a peat bog. Kip et al.2 reveal that Sphagnum mosses form symbioses with methane-consuming bacteria in Sphagnum-dominated peat bogs across the globe. Methane oxidation by the symbionts was greatest in submerged mosses. Carbon dioxide derived from methane oxidation — and potentially from methanotrophic utilization of alternative carbon sources — is taken up by the plants for photosynthesis. The symbiosis could help to explain why Sphagnum-dominated peatlands emit less methane than other peatland types that are dominated by vascular plants, which channel methane from the soil to the atmosphere. Free-living methanotrophs that inhabit the rhizosphere — the region of the soil influenced by roots — of peat-adapted plants also play an important role in methane oxidation.

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© 20 Macmillan Publishers Limited. All rights reserved10

596 nature geoscience | VOL 3 | SEPTEMBER 2010 | www.nature.com/naturegeoscience

news & views

largely responsible for attenuating methane release from these soils.

However, it remains unclear why Sphagnum mosses that grow above the water table exhibit lower rates of methane oxidation than mosses growing beneath the water table, as the methanotrophic communities proved to be similar. Methanotrophic activity may have been diminished in hummock- and lawn-derived mosses owing to a lack of methane, or methanotrophs may start feeding on alternative carbon sources, such as acetate in these environments. Indeed, some methanotrophs isolated from acidic peatlands can use acetate6–8, one of the key intermediates in the breakdown of peat mosses. If the symbiotic methanotrophs are capable of feeding on alternative substrates, Kip and colleagues may have overestimated the contribution of methane-derived carbon to Sphagnum. Their estimation was based on incubations carried out in closed systems; in vivo, carbon dioxide may also be generated during the respiration of alternative carbon sources by methanotrophs.

Furthermore, the relative contribution of symbiotic versus free-living methanotrophs to methane oxidation in peatlands is uncertain. Submerged Sphagnum pools occupy a relatively small proportion of the peatland landscape, although their prevalence is likely to expand owing to permafrost thawing in a warmer world. At present it is difficult to assess the global significance of Sphagnum symbionts in attenuating peatland methane emissions. It has been well documented that peatlands covered with vascular plants, another principal peatland landscape, release more methane owing to the presence of vascular tissue, which channels methane directly to the atmosphere, bypassing the oxic zone of the soil that methanotrophs inhabit9,10.

Nevertheless, the study by Kip et al.2 highlights the ubiquitous nature of the Sphagnum–methanotroph symbiosis in submerged peatland mosses and could help to explain why Sphagnum-dominated peatlands generally emit less methane

than other peatland types10,11. Further investigation is now needed to determine the extent to which this symbiotic relationship could help to reduce methane emissions from peatlands in a warmer world. ❐

Yin Chen and J. Colin Murrell are in the Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK. e-mail: [email protected]

References1. Smith, L. C. et al. Science 303, 353–356 (2004).2. Kip, N. et al. Nature Geosci. 3, 617–621 (2010).3. Raghoebarsing, A. A. Nature 436, 1153–1156 (2005).4. Chen, Y. et al. Environ. Microbiol. 10, 446–459 (2008).5. Chen, Y. et al. Environ. Microbiol.

10, 2609–2622 (2008).6. Dedysh, S. N. et al. J. Bacteriol. 187, 4665–4670 (2005).7. Dunfield, P. F. et al. Int. J. Syst. Evol. Microbiol.

doi:10.1099/ijs.0.020149-0 (2010).8. Belova, S. E. et al. Environ. Microbiol. Rep.

doi:10.1111/j.1758-2229.2010.00180.x (2010).9. Frenzel, P. et al. Biogeochemistry 51, 91–112 (2000).10. Joabsson, A. et al. Trends Ecol. Evol. 14, 385–388 (1999).11. Whiting, G. J. et al. Nature 364, 794–795 (1993).

Satellite gravimetry has been playing an increasingly important role in monitoring the state of the polar ice

sheets since 2002. A suite of mass-balance studies1–3 based on the Gravity Recovery and Climate Experiment (GRACE) mission has revealed substantial losses of ice-sheet mass in Greenland and West Antarctica. What’s more, the contribution of the ice sheets to global mean sea-level rise has accelerated over the past few years2. Writing in Nature Geoscience, Wu and colleagues4 describe an innovative approach employed to derive ice-mass changes from GRACE data and suggest significantly smaller ice-mass loss overall than earlier GRACE-based estimates.

Variations in the mass of the polar ice sheets — and more generally in the storage of water or ice on land — affect the Earth’s gravitational field. This effect is detected by the twin GRACE satellites. However, other phenomena also contribute to the geodetic signal measured by GRACE. These further contributions comprise the response of the

lithosphere to past variations of the ice load at the Earth’s surface, termed glacial isostatic adjustment, as well as changes in the spatial distribution of the atmospheric and oceanic masses. Disentangling these different signals is key to accurately assessing ice-sheet mass balance.

The atmospheric and oceanic contributions are commonly derived from global reanalyses or other global climate models that assimilate observations. However, the contribution from glacial isostatic adjustment is more difficult to evaluate because the Earth’s mantle is viscoelastic and therefore responds to changes in surface loading with a long delay. Indeed, the variations of the mass and extent of the ice sheets since the Last Glacial Maximum, about 20,000 years ago, continue to affect present-day changes in bedrock elevation. Assessments of the glacial isostatic adjustment typically rely on deglaciation models — which simulate the evolution of the ice sheets since the Last Glacial

Maximum — together with assumptions about the viscosity profile of the mantle. Much is still unknown regarding the history of the ice sheets, and even less is known about the behaviour of the mantle in response to loading and unloading.

The originality of the method used by Wu and colleagues4 consists of estimating ice-mass changes and glacial isostatic adjustment simultaneously, as opposed to quantifying the latter separately from deglaciation models as had been done before. The problem is expressed in terms of a single matrix equation, with the observed surface-height changes decomposed into their different contributions. The equation is ultimately solved for ice-mass changes through matrix inversion. The glacial isostatic adjustment is thus not directly retrieved from deglaciation models, but the inversion method still requires a first-guess estimate of this value and the related statistical information. These are derived from deglaciation models. A similar approach has been previously applied to studying temporal

SeA-leVel RISe

Ice-sheet uncertaintyGravity measurements of the ice-mass loss in Greenland and Antarctica are complicated by glacial isostatic adjustment. Simultaneous estimates of both signals confirm the negative trends in ice-sheet mass balance, but not their magnitude.

david H. bromwich and Julien P. Nicolas

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© 20 Macmillan Publishers Limited. All rights reserved10