The Heat Is Online

An enzymic 'latch' on a global carbon store

Nature, Jan. 11, 2001

An enzymic 'latch' on a global carbon store

CHRIS FREEMAN*, NICK OSTLE*† & HOJEONG KANG*†

* School of Biological Sciences, University of Wales, Bangor LL57 2UW, UK
† Present addresses: Centre for Ecology and Hydrology, Grange-over-Sands LA11 6JU, UK (N.O.); Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706, USA (H.K.)

e-mail: c.freeman@bangor.ac.uk

A shortage of oxygen locks up carbon in peatlands by restraining a single enzyme.

Historically, northern peatlands have removed carbon dioxide from the atmosphere faster than it has been re-released, so they now contain 20–30% of the world's soil carbon stock1 (the equivalent of over 60% of the atmospheric carbon pool2). Here we show that the anaerobic conditions in peatlands prevent the enzyme phenol oxidase from eliminating phenolic compounds that inhibit biodegradation. This indicates that oxygen limitation on a single peatland enzyme may be all that prevents the re-release of a major store of global carbon into the atmosphere, with potentially serious implications for future global warming.

Mechanisms proposed to account for the slow decomposition rates in peatlands include the effects on microbial metabolism of low oxygen availability, low pH, low nutrient supply and low temperatures. But decomposition can be highly efficient in anaerobic environments such as the rumen or man-made sewage digesters. Likewise, it can remain relatively inefficient in fens that are nutrient-rich and whose pH is around neutral, or in mangrove systems that are far from cold3.

One feature common to all of these wetlands, however, is the ubiquity of phenolic compounds. These have attracted intense interest as potent inhibitors of enzymes4 and, with the exception of phenol oxidase, few enzymes are able to degrade these recalcitrant materials5. But the in situ activity of phenol oxidase is severely constrained6: it requires bimolecular oxygen, even though it exists in an essentially anaerobic environment. Also, the activity of all the major biodegradative hydrolase enzymes is depressed in peatlands7, although they normally retain high activity in anaerobic environments such as the rumen8 or anaerobic sludge digest9. We propose that the low rate of biodegradation in peatlands is due to oxygen constraints on phenol oxidase, which allow phenolic materials to accumulate and inhibit these pivotal hydrolase enzymes.

We compared enzyme activities under oxygen-saturated and oxygen-free conditions and found that phenol oxidase was the only enzyme to increase in activity under the more aerated conditions (7-fold increase in activity; Table 1). Evidence of a link between phenol oxidase activity and oxygen availability has been found in a Florida wetland, where phenol oxidase activity was detectable only under aerobic conditions5. Experimental supplementation with phenol oxidase resulted in a 27% drop in phenolic compound concentrations within 18 hours (Table 1). Lower water-tables, which are associated with increased aeration, also cause a sharp drop in phenolic concentrations10.

We determined the effect of reduced dissolved phenolic concentrations on hydrolase activities after removing them selectively by using crosslinked N-vinyl-2-pyrrolidone11. We found that the activity of hydrolases in peat samples exposed to phenolic-free waters was significantly higher than the corresponding activity in untreated waters containing phenolic compounds at just 2.40 mg l-1 (mean) (Table 1). It has been shown that hydrolases are strongly inhibited (over 80%) in the presence of higher phenolic concentrations12 or after longer exposure to phenolic materials4.

Supplementing aerobic peat samples with additional phenol oxidase led to a significant increase in the activity of hydrolase enzymes (Table 1) in response to the increased removal of inhibitory phenolic compounds. We also showed by doing a regression analysis of data from a 3-month field survey (r=0.61, P<0.05) that every doubling in phenol oxidase activity was accompanied by an approximate doubling in CO2 production.

Taken together, our findings support the idea that oxygen constraints on a single enzyme, phenol oxidase, can minimize the activity of hydrolytic enzymes responsible for peat decomposition. This has profound implications in the context of climate change as a feedback to the process of intensified carbon loss. Increased peat aeration, as a result of droughts predicted by certain climate-change models13, has the potential to eliminate a critical mechanism restricting the re-release of CO2 to the atmosphere. As such, phenol oxidase could be considered to represent a fragile 'latch' mechanism holding in place a vast carbon store of 455 gigatonnes.

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