Efficient Atmospheric Cleansing of Oxidized Organic Trace Gases by Vegetation

Volatiles Versus Vegetation Plants act as both global sources and sinks of highly reactive volatile organic compounds (VOCs). Models typically treat the uptake and degradation of these compounds as if they are mostly unreactive, like other more commonly studied biogenic gases such as ozone. A study by Karl et al. (p. 816, published online 21 October) suggests that VOCs may be more reactive than expected. By monitoring six field sites representing a range of deciduous ecosystems, several oxidized VOCs were found to have high deposition fluxes. Fumigation experiments in the laboratory confirmed that leaves are capable of oxidizing these compounds, and do so through an enzymatic detoxification or stress-response mechanism. Budgets for VOC flux in the atmosphere suggests that, on a global scale, plants may take up significant levels of VOCs in polluted regions, especially in the tropics. Deciduous trees enzymatically remove oxygenated volatile organic compounds from the atmosphere. The biosphere is the major source and sink of nonmethane volatile organic compounds (VOCs) in the atmosphere. Gas-phase chemical reactions initiate the removal of these compounds from the atmosphere, which ultimately proceeds via deposition at the surface or direct oxidation to carbon monoxide or carbon dioxide. We performed ecosystem-scale flux measurements that show that the removal of oxygenated VOC via dry deposition is substantially larger than is currently assumed for deciduous ecosystems. Laboratory experiments indicate efficient enzymatic conversion and potential up-regulation of various stress-related genes, leading to enhanced uptake rates as a response to ozone and methyl vinyl ketone exposure or mechanical wounding. A revised scheme for the uptake of oxygenated VOCs, incorporated into a global chemistry-transport model, predicts appreciable regional changes in annual dry deposition fluxes.


Efficient Atmospheric Cleansing of Oxidized Organic Trace Gases by Vegetation
T. Karl, 1 * P. Harley, 1 L. Emmons, 1 B. Thornton, 2 A. Guenther, 1 C. Basu, 2 A. Turnipseed, 1 K. Jardine 3 The biosphere is the major source and sink of nonmethane volatile organic compounds (VOCs) in the atmosphere. Gas-phase chemical reactions initiate the removal of these compounds from the atmosphere, which ultimately proceeds via deposition at the surface or direct oxidation to carbon monoxide or carbon dioxide. We performed ecosystem-scale flux measurements that show that the removal of oxygenated VOC via dry deposition is substantially larger than is currently assumed for deciduous ecosystems. Laboratory experiments indicate efficient enzymatic conversion and potential up-regulation of various stress-related genes, leading to enhanced uptake rates as a response to ozone and methyl vinyl ketone exposure or mechanical wounding. A revised scheme for the uptake of oxygenated VOCs, incorporated into a global chemistry-transport model, predicts appreciable regional changes in annual dry deposition fluxes.
L arge quantities of nonmethane volatile organic compounds (NMVOCs) enter the atmosphere via biogenic, pyrogenic, and anthropogenic sources. The annual production of NMVOCs [~1200 to 1350 teragrams of carbon (TgC)/year) probably exceeds that of methane and carbon monoxide (CO) (~500 TgC/year each) (1,2). Together, these gases fuel tropospheric chemistry. Oxidation of NMVOCs leads to the formation of aerosols (3)(4)(5) and modulates the oxidation ca-pacity of the atmosphere (6), creating important climate feedbacks (7). One large uncertainty in constraining budgets of NMVOCs is the amount of deposition to vegetation, which acts as a major source and sink for organic trace gases on a global scale. This has consequences for constraining secondary species produced in the gas phase, which will either oxidize to CO and carbon dioxide (CO 2 ), condense onto or form organic aerosol (OA) and be rained out, or directly deposit to the surface via dry and wet deposition. Two recent bottom-up assessments of the tropospheric organic aerosol budget (1, 3), on the basis of different assumptions for wet and dry deposition of organic vapors, resulted in different predictions of global production rates for secondary organic aerosol (SOA).
Dry deposition schemes parameterize the deposition flux according to where F represents the deposition flux, C is the ambient concentration, and v d is the deposition velocity. Deposition velocities are usually treated in analogy to Ohm's Law, where v d can be expressed as three resistances in series: R a represents the aerodynamic resistance above the surface and has the same value for all constituents. The term R b is the quasi-laminar resistance to transport through the thin layer of air in contact with surface elements and varies with the diffusivity of a substance. Standard micrometeorological methods and modeling approaches are available to calculate R a and R b (8). R c represents the resistance to uptake by surface elements and has been extensively parameterized for ozone (O 3 ) and sulfur dioxide (SO 2 ) (9). Because O 3 immediately decomposes inside plants by reduction, a relative measure of reactivity ( f 0 = 0 to 1) accounts for its loss (9). Stomatal resistance (R s ) primarily controls the deposition of highly reactive compounds (10). Because of the lack of observational constraints, accounting for the uptake of organic gases occurs in analogy to O 3 and SO 2 solely on the basis of their physiochemical properties (solubility and reactivity) in the mesophyll. As a consequence, all models treat NMVOCs as nonreactive or only slightly reactive species ( f 0 = 0 to 0.1), leading to large estimates of R c (10).
In this report, we combine field observations with laboratory experiments and transport modeling in order to investigate the influence of vegetation on the deposition of oxygenated VOCs (oVOCs). oVOCs represent the most abundant class of organic carbon and profoundly affect the chemical composition in Earth's oxidizing atmosphere. In six field experiments across a range of ecosystems ( fig. S1), oVOCs deposited at high rates. The sum of methyl vinyl ketone (MVK) and methacrolein (MAC), which account for about 80% of the carbon in the initial stage of isoprene oxidation, exhibits the fastest deposition rates. R c for deciduous ecosystems is much smaller than predicted and falls along a trend that would be expected for O 3 ( f 0 = 1) (Fig. 1). This suggests that oVOCs, like O 3 , are immediately lost once they enter a leaf through stomata. Tropical ecosystems exhibit the fastest deposition rates (R c s are 2.6 to 3.5 times smaller than predicted), and the observed deposition velocities for MVK+MAC are as large as for O 3 (up to 2.4 cm/s). We measured similarly high-deposition fluxes for other oVOCs, including acetaldehyde, MVK+MAC, hydroxyacetone, glycolaldehyde, C 5 carbonyls, and nopinone (Fig. 2). All oVOCs deposited on the vegetation except acetaldehyde, which exhibited net emissions during a hot period at the beginning of the study because it is also produced by vegetation (11). Because of the bidirectional exchange of acetaldehyde, v d should be regarded as a net deposition velocity. All oVOCs investigated here form during the photochemical oxidation of isoprene and certain monoterpenes. The vertical profiles suggest that deposition mainly occurs via uptake by vegetation elements, with the upper 70% of the canopy (Fig. 2) accounting for more than~97% of the total de-position flux for all measured oVOCs. After correction for different molecular diffusivities in air, the corresponding R c s of oVOCs (except acetaldehyde) fall within 25% of O 3 . Because of the bidirectional exchange, R c for acetaldehyde is 60% higher than that of O 3 (Fig. 2). Large deposition fluxes imply that the internal concentration (C i ) of these oVOCs is small compared with the ambient concentration (C a ).
To investigate mechanisms that can potentially influence the uptake of oVOCs-in particular, MVK and MAC-we performed a series of leaf cuvette experiments with Populus trichocarpa x deltoides. We observed a linear flux-concentration relationship between the uptake (the flux) of oVOCs by a leaf as a function of oVOC concentration (figs. S3 and S5), which is indicative of enzymatic reactions metabolizing oVOCs. The compensation point (C p ) of a compound, defined as the concentration at which the net uptake is zero, typically followed an exponential increase with leaf temperature ( fig. S6). When oVOCs form or decompose inside a leaf, the C p is typically greater than zero, resulting in emission below and uptake above the C p . The mesophyll resistance (R m ), expressed as a deposition velocity (v m = 1/R m ), was highest between 15°and 20°C, dropping substantially above a narrow temperature range between 25°and 28°C ( fig. S6). The light response curves of v m exhibited a functional form similar to electron transport.
Plants possess the ability to detoxify through various mechanisms [via oxidative stress or conversion by the aldehyde dehydrogenase (ALDH) family]. As an example, ALDHs are a protein superfamily of nicotinamide adenine dinucleotide phosphate (NADP + )-dependent enzymes known to oxidize a wide range of carbonyls. ALDH enzymes play an important role in the detoxification of aldehydes by oxidizing these to their corresponding carboxylic acids (12). Stress-induced up-regulation of these and potentially other enzymes (such as various peroxidases) could help reduce concentrations of aldehydes and other oVOCs that would otherwise build up to toxic levels.
On the basis of exposure experiments with P. trichocarpa x deltoides, we suggest that chemical and mechanical stress affects uptake rates of acetaldehyde and MVK (Fig. 3). For both plants, v m for acetaldehyde dropped during fumigation with MVK but changed little for MVK. The corresponding C p for acetaldehyde increased during the fumigation period, suggesting increased internal production occurring as a response to oxidative or metabolic stress. During MVK fumigation, conversion rates of aldehydes may have also decreased through enzyme saturation or depletion of reactive oxygen species (ROSs), which would explain the relatively small change of v m for MVK during fumigation as opposed to a large increase immediately after fumigation. For the MVK experiment, the post-exposure v m drastically increased for acetaldehyde (approximately twofold) and MVK (~20-fold), suggesting short-term up-regulation of metabolic activity in response to MVK exposure during the previous days; however, v m decreased The dotted line shows R C with a dry deposition that would be conventionally used (f 0 = 0). LAI data are plotted as mean T SD (n = 10 LAI measurements); the SD for R C was calculated as the sum of systematic and random errors associated with turbulent flux measurements (14) and the errors associated with instrument precision for wind measurements through use of a sonic anemometer. www.sciencemag.org SCIENCE VOL 330 5 NOVEMBER 2010 after one day in both cases. The v m for MVK increasing direct or indirect enzymatic reactions, rather than purely nonenzymatic reactions (such as Michael addition), probably regulated the metabolic consumption. MVK fumigation also resulted in physiological changes. After a certain exposure period, stomatal conductance (G s ) and photosynthesis dropped by 30 to 50% and 20 to 50%, respectively, each day. G s and photosynthesis, however, recovered every morning. This corroborates the finding that MVK actively goes through stomata, inducing a biological response in the mesophyll.
We did not observe any physiological changes (G s and photosynthesis) for plant B during the course of the O 3 fumigation experiment. v m for MVK increased by~70% immediately after we exposed plant B to O 3 and gradually increased by another~25% during the course of the fumigation, where it remained after we turned off the O 3 supply (Fig. 3). We observed similar behavior for acetaldehyde. For both compounds, v m remained high for 2 days after stopping the fumigation. A set of experiments inducing mechanical wounding resulted in increased uptake of MVK, which is qualitatively similar to the chemical exposure experiments. The uptake of acetaldehyde decreased and occurred in parallel with an increasing C p . This is consistent with the idea that mechanical wounding increases the internal production of acetaldehyde (11). Upon recovery, the uptake rates (v m ) for acetaldehyde increased subsequently and at times exceeded the pre-wounding values.
The increase of v m for acetaldehyde and MVK after (plant A and B) and during (plant B) fumigation imply that these plants responded to acute chemical exposure by up-regulating the activity of processes responsible for detoxification. Quantitative polymerase chain reaction identified changes in several characteristic genes indicative of enhanced metabolic activity as a response to chemical and mechanical stress (table S3). All chemical treatments (MVK and O 3 ) showed elevated gene expression patterns related to ROS (superoxide dismutase and ascorbate peroxidase). Mechanical wounding and chemical exposure experiments (MVK and O 3 ) resulted in up-regulation of aldehyde oxidase (AAO2) and aldehyde dehydrogenase (ALDH2). We observed elevated levels of p450 cytochrome, which is typically associated with the oxidation of organic substances, for all chemical treatments along with increases in WRKY transcription factors, encoding proteins involved in plant responses to biotic and abiotic stresses. These changes in gene-expression patterns support the gas-exchange measurements, showing that plants can adjust their metabolism (meaning, their v m ) and increase oVOC decomposition as a response to environmental factors.
The presented laboratory and field observations show that oVOCs can be efficiently metabolized by plants through constitutive and induced detoxification mechanisms. Because the general route of atmospheric photooxidation of NMVOCs goes through the formation of carbonyls and hydroxycarbonyls, these findings have consequences for understanding the atmospheric evolution of these oVOCs. To place these findings on a broader scale, we modified the dry deposition scheme for oVOCs in a comprehensive global chemistry and transport model (13,14). Fast metabolic conversion of oVOCs was incorporated, according to our field observations, by setting f 0 to 1 (9). The total dry deposition flux of organics on a carbon basis increases (by up to 110%) relative to previous estimates (Fig. 4). Large changes especially occur in tropical regions such as the Amazon, where the annual dry deposition flux increases between 65 and 85%. Globally, dry deposition of organics increases by about 36%. More importantly, deposition fluxes are substantially altered because of increases (50 to 100%) in dry deposition of relatively insoluble species [for example, carbonyls with Henry's Law Constant (HLC) of <50 M/atm] leading to decreases (up to 30%) in wet deposition of certain soluble species [for example, peroxides with HLCs of >300 M/atm ( fig. S8)]. Higher dry deposition of relatively insoluble species also leads to a decrease in dry deposition of certain peroxides because of lower atmospheric concentrations in the gas phase. Modeled oVOC concentrations in the surface layer change substantially (30 to 60%). These results have consequences for capturing the dynamic behavior and repartitioning between NMVOC oxidation products and SOA (5,14,15). The modifications change OH radical concentrations by up to 15% above the land surface layer (fig. S11). Tropospheric O 3 concentrations are slightly reduced (by 1 to 3%) in the Northern Hemisphere and enhanced (by 0.5 to 1.5%) in the tropical land regions (fig. S10).  Dry deposition of organic trace gases addresses a poorly quantified process in the atmosphere (3,10). We estimate a lower and upper bound for the annual deposition flux of gas phase oVOCs between 37 and 56% relative to the annual NMVOC emission flux on a carbon basis (table S4). It is conceivable that oVOC deposition fluxes to vegetation could increase as a consequence of acute or chronic exposure to high O 3 concentrations in polluted regions (16).

Transient Middle Eocene Atmospheric CO 2 and Temperature Variations
Peter K. Bijl, 1 * † Alexander J. P. Houben, 1 * † Stefan Schouten, 2 Steven M. Bohaty, 3 Appy Sluijs, 1 Gert-Jan Reichart, 4 Jaap S. Sinninghe Damsté, 2,4 Henk Brinkhuis 1 The long-term warmth of the Eocene (~56 to 34 million years ago) is commonly associated with elevated partial pressure of atmospheric carbon dioxide (pCO 2 ). However, a direct relationship between the two has not been established for short-term climate perturbations. We reconstructed changes in both   (2), with a globally uniform 4°to 6°C warming of both surface and deep oceans withiñ 400,000 years, as derived from foraminiferal stable oxygen isotope records (3). A decrease in carbonate mass accumulation rates during the MECO argues for ocean acidification induced by a rise in pCO 2 (3). Application of paleo-pCO 2 proxies across the MECO has yet to confirm whether pCO 2 changes are indeed associated with this interval of transient warming.
We investigated a sedimentary succession spanning the MECO recovered from the East Tasman Plateau at Ocean Drilling Program (ODP) Site 1172, which at that time was situated on the shelf (~65°S paleolatitude; Fig. 1 and figs. S1 and S2) (4,5). To fully capture the magnitude of the sea surface temperature (SST) change associated with the MECO at this site, we applied two independent temperature proxies: the alkenone unsaturation index (U K3 7 ) (6) and the index of tetraethers consisting of 86 carbon atoms (TEX 86 ) (5, 7) ( fig. S3). At the onset of the MECO, U K3 7 and TEX 86 indicate a rise in SST of 3°C and 6°C, respectively, which, also at this location, stands out as an interruption of long-term middle Eocene cooling (Fig. 2). Bulk carbonate oxygen isotope values (d 18 O) decrease by 1.0 to 1.2 per mil (‰), which, if controlled by SST only, also indicate a SST rise of~4°to 5°C (5).
Additional evidence of warming is derived from assemblages of hypnozygotic organic cysts of surface-dwelling dinoflagellates (dinocysts) (5). Whereas the middle Eocene dinocyst record at ODP Site 1172 is dominated by taxa that are endemic to the Southern Ocean (8), an incursion of low-latitude dinocyst taxa characterizes the MECO (Fig. 2 and fig. S4). A SST increase of 3°to 6°C is consistent with inferences from benthic foraminiferal and fine-fraction carbonate oxygen isotope records at other sites (1,3). The U K3 7 and TEX 86 proxies are independent of seawater d 18 O. Hence, the consistent magnitude of warming between the proxies suggests that the carbonate d 18 O records were not affected by a change in d 18 O of seawater, and that global ice volume did not change considerably during the MECO.
Absolute SSTs as indicated by U K3 7 and TEX 86 are consistent, with 26°C or 24°C just below the onset of the MECO for the two proxies, respective-ly, and peak MECO SSTs exceeding 28°C. These SSTs are much (~10°C) higher than those derived from fine-fraction carbonate oxygen isotope measurements from elsewhere in the Southern Ocean (1, 3). At least part of this large discrepancy is most likely the result of diagenetic alteration of calcite (9).
We assessed pCO 2 changes by determining the stable carbon isotopic composition (d 13 C) of alkenones, long-chained ketones exclusively synthesized by specific haptophyte algae. Carbon isotopic fractionation during carbon fixation (e p ) by haptophyte algae varies as a function of dissolved CO 2 [CO 2(aq) ] (10, 11), specific cell physiological parameters (which show good correspondence to the surface-water concentrations of soluble phosphate), and other environmental parameters, primarily light intensity (5). The carbon isotopic composition of diunsaturated alkenones (d 13 C C37:2 ) ranges between -32.5 and -35.5‰ (fig. S3). We used bulk carbonate d 13 C to estimate the d 13 C value of the dissolved inorganic carbon (DIC) pool in seawater (5) to determine e p . The data show background e p values of 21 to 22‰ rising up to 24.5‰ during MECO (Figs. 2 and 3 and fig. S3). The relationship between e p and pCO 2 is exponential, which results in a relatively large uncertainty in reconstructed pCO 2 levels with high e p values (Fig. 3). Temperature variations, however, play a minor role in the range of temperatures indicated by TEX 86 and U K3 7 (Fig. 2) and cannot explain the high e p values (Fig. 3). It seems unlikely that changes in light intensity (12) influenced e p substantially at ODP Site 1172 (5). The soluble phosphate concentration exerts a strong influence on the relation between e p and pCO 2 , particularly if e p values are high (5).
To evaluate all possible absolute pCO 2 estimates from our record, we applied the full range of present-day surface-water phosphate concentrations. These vary between 0 mmol liter −1 in the oligotrophic gyres to >2 mmol liter −1 in the Southern Ocean (5) (fig. S5). Yet even when phosphate concentrations of 0 mmol liter −1 are assumed, e p values between 21.2‰ and 24.5‰ yield pCO 2 estimates between 600 parts per million by volume (ppmv) before the MECO and 6400 ppmv during the MECO (Figs. 2 and 3). Hence, elevated levels of pCO 2 must in part be responsible for the high e p values, with middle Eocene pCO 2