Environ. Sci. Technol. 2010, 44, 8403–8408
Photochemical Production and Consumption Mechanisms of Nitric Oxide in Seawater EMMANUEL F. OLASEHINDE, KAZUHIKO TAKEDA, AND HIROSHI SAKUGAWA* Graduate School of Biosphere Science, Department of Environmental Dynamics and Management, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521, Japan
Received May 2, 2010. Revised manuscript received September 23, 2010. Accepted September 30, 2010.
Nitric oxide (NO•) is an active odd-nitrogen species that plays a critical role in determining the levels of ozone (O3) and other nitrogen species in the troposphere. Here, we provide experimental evidence for photochemical formation of NO• in seawater. Photoproduction rates and overall scavenging rate constants were measured by irradiation of surface seawater samples collected from the Seto Inland Sea, Japan. Photoproduction rates of NO• ranged from 8.7 × 10-12 M s-1 to 38.8 × 10-12 M s-1 and scavenging rate constants were 0.05-0.33 s-1. The steady state concentrations of NO• in seawater, which were calculated from the photoproduction rates and scavenging rate constants were in the range 2.4-32 × 10-11 M. Estimation from the scavenging rate constant showed that the NO• lifetime in seawater was a few seconds. Our results indicate that nitrite photolysis plays a crucial role in the formation of NO•, even though we cannot exclude minor contributions from other sources. Analysis of filtered and unfiltered seawater samples showed no significant difference in NO• photoformation rates, which suggests a negligible contribution of NO• produced by photobiological processes. Using an estimated value of the Henry’s law constant (kH ≈ 0.0019 M atm-1), a supersaturation of surface seawater of 2 to 3 orders of magnitude was estimated. On the basis of the average values of the surface seawater concentration and the atmospheric NO• concentration, a sea-to-air NO• flux was estimated.
Introduction Nitric oxide (NO•) plays a key role in regulating atmospheric concentrations of ozone (O3) and hydroxyl radicals (•OH) in the Earth’s troposphere. When the atmosphere is in a pseudophotostationary state, NO• reacts with O3 to form nitrogen dioxide and oxygen (1). The balance between ozone formation and destruction in the remote troposphere is largely dependent on the ambient NO• concentration (2). Previous studies have shown that NO• concentrations (low pptv mixing ratio) typical of the marine boundary layer and midtroposphere may influence radical imbalance and thus stimulate depletion of the tropospheric ozone (3, 4). However, the mechanisms which control the concentration and distribution of NO• in the marine boundary layer are poorly understood, particularly in areas distant from primary sources * Corresponding author phone: +81 82 424 6504; fax: + 81 82 424 6504; e-mail:
[email protected]. 10.1021/es101426x
2010 American Chemical Society
Published on Web 10/18/2010
of nitrogen oxides. Primary emissions of NO• from fossil combustion, biomass burning and other anthropogenic sources are not sufficiently long-lived in the atmosphere to be transported long distances (2). Thus, this process might not be the dominant factor controlling the supersaturation of NO• in the marine boundary layer. Although atmospheric NO• has largely been attributed to anthropogenic sources, it has been speculated that oceans are a likely source of this radical (5, 6). Several studies in the oceanological field indicate that NO• is produced biologically as an intermediate in nitrification and denitrification processes (7, 8). However, nitrification and denitrification are not expected to occur in sunlit surface waters because they are inhibited by light and high oxygen concentration, respectively (8). Further, marine phytoplankton such as red tide algae can produce NO• from nitrite through nitrate reductase (NR) (9). Photochemical formation of nitric oxide via nitrite photolysis in seawater has also been documented (5, 6, 10). Over the past decades, researchers have focused on the effects of NO• on plants. Studies have shown that NO• acting as a signaling molecule can control plant metabolism, regulate growth, development, maturation and senescence, prevent infection, and so on (7). However, oceanological research on NO• has been largely neglected, partly due to the low concentration of NO• in natural seawater and/or because of the lack of suitable analytical methods for NO• measurement in natural seawater. To date, there is only one report of photochemically generated NO• in natural seawater (5). Relatively little is known about the sources of NO•, the reactions in seawater are poorly understood, and the direction and magnitude of the global NO• flux from sea to air remains unknown. Recently, we reported a new analytical method for the measurement of the photoformation rates of NO• in natural waters (10). Here, we present a series of such measurements conducted on seawater samples from the Seto Inland Sea, Japan. The primary objectives of this study were as follows: (1) to determine the photoformation rates, overall scavenging rate constants, steady-state concentrations, and lifetime of NO• in seawater; (2) to identify the sources and sinks of NO• in seawater; and (3) to estimate the flux of NO• from sea to air.
Experimental Section Study Area and Sample Collection. The Seto Inland Sea is located in Western Japan and is one of the largest semienclosed seas in the country (Supporting Information (SI) Figure S1). It is about 450 km from east to west (130°40-135°30′ E) and 15-55 km north to south (32° 55′-34° 50′ N). It consists of several smaller seas and bays, among which are HarimaNada, Bingo-Nada, Aki-Nada, Osaka Bay, Bisan-Seto, and Hiroshima Bay. The sea has an area of about 23 000 km2 and a maximum depth of 50 m (average depth, 38 m) (11). Seawater (salinity 31.3-33.7%, pH 8.0-8.2) samples from various depths and locations were collected from the Seto Inland Sea using Niskin sampling bottles and a Sea-Bird CTD carousel multi sampling system (SBE-9plus). Sampling was conducted during the cruise of Hiroshima University’s R/V Toyoshio Maru between October 20-24, 2008 and October 5-9, 2009. Samples were immediately transferred to clean 1 L amber glass bottles. Water samples were filtered through a precleaned glass fiber filter (Advantech, 0.45 µm nominal rating) and stored in the dark at 4 °C until analysis. Analyses were completed within 2 weeks of sample collection. VOL. 44, NO. 22, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
8403
Chemicals, HPLC Instrumentation and Conditions. All chemicals and reagents used in this study are provided in the SI. Photoproduced nitric oxide was determined in seawater by trapping it with added 4,5-diaminofluorescein (DAF-2), and measuring the triazolofluorescein (DAF-2T) product by RP-HPLC (10). The HPLC system consisted of a JASCO PU-2089 plus pump, a Rheodyne injection valve with a 100 µL sample loop, and a JASCO FP-2020 plus intelligent fluorescence detector interfaced with a Shimadzu C-R6A Chromatopac integrator. DAF-2 and DAF-2T were separated on an RP-18 GP column (150 × 4.6 mm I.D., 5 µm) from Kanto Kagaku. The mobile phase consisted of 10 mM phosphate buffer solution (PBS) at pH 7.4 with 6% acetonitrile. The flow rate was 1 mL min-1 and the column was at ambient temperature. The detector was operated at wavelengths of 495 and 515 nm for excitation and emission, respectively. Ancillary Measurements. Nitrate was determined spectrophotometrically by the previously reported method (12). The nitrite ion concentration was determined by a colorimetric method following the diazotization of sulfanilamide and coupling with N-1-naphthylethylenediamine. The absorbance spectra were acquired using a Shimadzu UV-2400 PC UV-vis scanning spectrophotometer. The purification of oxyhemoglobin (HbO2) from bovine hemoglobin has been described elsewhere (13). Hydroxyl radicals in seawater were determined using the method described by Arakaki et al. (14) with few modifications as mentioned in the SI. Reaction Rate Constant of DAF-2 with NO• in AirSaturated Solution. Procedural details for the determination of the reaction rate constant of DAF-2 with NO• in airsaturated solution can be found in the SI. Briefly, the competition kinetics method was employed to determine the rate constant for the reaction of DAF-2 with NO• in airsaturated aqueous solution. Using different ratios of HbO2 and DAF-2, the reaction rate constant of DAF-2 with NO• in air-saturated aqueous solution was estimated to be (6.28 ( 0.45) × 10 6 M-1s-1. It should be noted that the rate constant determined in this study is only valid provided that the formation rate of NO• in the system is very low (∼pM/s level or less than as typical of this study), which would allow the reaction of DAF-2 with NO• to predominate over the nitrosonium addition of N2O3 (15). Our findings are in agreement with the previous report suggesting that nitrosonium addition of N2O3 leading to the formation of DAF-2T (see SI eqs S6-S8) is controlled by the local concentration of NO• and that N2O3 would form quantitatively only when the concentration of NO• rises to the micromolar range (16). Details of the DAF-2sNO and DAF-2sN2O3 pathways are provided in the SI. Irradiation Experiments and General Procedures for NO• Determinations. The method for the determination of the NO• photoformation rates is essentially that described by Olasehinde et al. (10). This involved addition of an aliquot of 50 µM DAF-2 solution prepared in phosphate buffer (0.1 M phosphate, pH 7.4) to a water sample (5.0 mL) in an airtight 6.5 mL quartz glass cell, giving a final concentration of 5 µM DAF-2. The solution was irradiated in the quartz glass cell with solar simulator, gently stirred with a Teflon stirring bar, and maintained at about 20 °C using a Neslab RTE 111 recirculating water bath. The daily actinic flux of the solar simulator was determined by measuring the degradation rate of an 8 µM standard solution of 2-nitrobenzaldehyde (2-NB). The apparent first order photolysis rate constant for the degradation of 2-NB for the solar simulator ranged from 0.0057-0.0064 s-1. However, all data relating to photochemical reactions were normalized to a 2-NB degradation rate of 0.0093 s-1, which was determined at noon under clear sky conditions in Higashi-Hiroshima (34° 25′ N) on May 1, 1998 (17). 8404
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 22, 2010
As shown in our previous report, OH radicals cannot oxidize DAF-2 to DAF-2T, and the transformation of DAF-2 into DAF-2T is not potentiated by light within the time frame of illumination in this study (10). DAF-2T formation was not observed under dark controls. Previous studies have also shown that stable oxidized forms of NO•, such as NO2- and NO3-, and other reactive oxygen species, such as O2•-, H2O2, and ONOO-, do not react with DAF-2 to yield any fluorescent products (10, 18). Furthermore, during photolysis of DAF-2 in Milli-Q water without a NO• source, no loss of DAF-2 was detected and formation of DAF-2T was negligible. Hence, the transformation of DAF-2 into DAF-2T mediated by the reaction of NO• with DAF-2 in air-saturated solution is a fairly selective process. It should be pointed out that the photodegradation rate of DAF-2T is negligible, compared to the formation rate of DAF-2T. Photoformation rates of NO• (RNO•) in water samples were calculated using the following formula: RNO· ) RD /(YD × FD)
(1)
where RD is the photoformation rate of DAF-2T in water samples (M s-1), YD the yield of DAF-2T formed per DAF-2 reacted with NO• in air-saturated solution, and FD the fraction of NO• that reacts with DAF-2. Our previous study showed that FD in seawater ranged from 0.92-0.99 at 5 µM DAF-2. For the purpose of calculating RNO•, it was assumed that FD )1. The mean value of YD determined over a pH range of 4.0-8.8 was 0.042 (10). To determine the overall scavenging rate constant of NO• Σ(ks, NO• [S]), NO• photoformation rates of seawater with different DAF-2 concentrations (0.05-0.4 µM) were measured. In water samples containing natural scavengers of NO• in addition to DAF-2, the FD is given as follows: FD ) {kD[DAF - 2]}/{(kD[DAF - 2]) +
∑ (k
s,NO·[S])}
(2)
where kD is the reaction rate constant of DAF-2 with NO• in air-saturated solution (M-1s-1), and Σ (ks, NO• [S]) is the summation of the scavenging rate of NO• with natural NO• scavengers [S] in the water samples. Substituting (eq 2) into (eq 1), provides: RD ) RNO· × YD{kD[DAF - 2]}/{(kD[DAF - 2]) +
∑ (k
s,NO·[S])}
(3)
The inverse of eq 3, and then rearrangement gives: 1/RD ) {1/(RNO· × YD)} +
{ ∑ (k
s,NO·[S])/(RNO·
}
× YD × kD) × {1/[DAF - 2]}
(4)
Plotting 1/RD against 1/[DAF-2], a straight line is obtained (See Figure S2 of the SI). With a known kD, Σ (ks, NO• [S]) can be calculated from the y-intercept and the slope of Figure S2 by the following:
∑ (k
s,NO·[S])
) slope × kDAF-2 /intercept
(5)
The NO• lifetimes (τNO) in water samples were estimated using eq 6: τNO· ) 1/
∑ (k
s,NO·[S])
(6)
Results and Discussion NO• Photoformation Rates. The Photoformation rates of NO• in surface seawater (0-5 m) ranged from 8.7 × 10-12 to 38.8 × 10-12 Ms1- (Table 1). Meanwhile, NO• photoformation rates varied among sites, with the highest rates (38.8 × 10-12
TABLE 1. NO• Photoformation Rates (RNO•) in Seawatera RNO• (10-12 Ms-1) sampling locations
min
max
average
Osaka bay Harima-nada Bisan-seto Bingo-nada Aki-nada
24.6 12.5 13.6 8.7 12.2
38.8 18.8 20.4 15.2 19.1
29.5 14.9 16.3 12.4 14.5
a
Number of samples (n g 7) in each sampling location.
FIGURE 2. Dependence of NO• photoformation rates on nitrate concentrations (regression equation: y ) 0.029 x + 19.03; r2 ) 0.8258).
FIGURE 1. Correlation plots of NO• photoformation rates versus (a) NO2- (regression equation: y ) 30.263 x + 1.994; r2 ) 0.979) and (b) NO3- (y ) -2.620 + 30.224; r2 ) 0.01) in the seawater samples. Ms1-) in Osaka Bay and the lowest (8.7 × 10-12 Ms1-) in the Bingo Nada. The elevated NO• photoformation rates observed in Osaka Bay are attributed to the exceptionally high concentration of NO• precursors (presumably NO2- and NO3-) in this region. The photoformation rates in this study are comparable to that previously reported (∼ 10-12 Ms1-) (5). To identify the photochemical sources of NO• in seawater, correlation plots of NO• photoformation rates versus NO2and NO3- concentrations in the samples were used to examine the relationship between the photoformed NO• and its photochemical precursors. A positive linear correlation (Figure 1a) was observed between NO• photoformation rates and NO2- (r2 ) 0.97, n ) 60), which suggests that NO2- could be a major photochemical source of NO• in seawater. However, there was a lack of correlation between the NO• photoformation rates and nitrates in the samples (Figure 1b). To further clarify the role of NO3- as a NO• photochemical source, experiments were conducted to determine the
dependence of NO• photoformation rates on nitrate concentrations. In these experiments, filtered seawater samples were spiked with nitrates to concentrations of up to 100 µM. Samples were irradiated for 30 min and analyzed for NO• photoformation rates prior to and after addition of nitrates. The addition of nitrates did not significantly increase the NO• photoformation rates (Figure 2), even though a slight increase was observed with increasing NO3- concentrations. The ratio of the slopes of regression lines of Figures 1a and 2 showed that less than 1% of the photoformed NO• is generated from NO3- photolysis under our experimental conditions, indicating that NO• is predominantly generated from NO2- photolysis in seawater. This is expected because nitrate photolysis results in the formation of nitrite and NO2, which require further photolysis or reaction to produce NO• (19). This result corroborated the report of Smith et al. (20) who found that NO• production is more closely correlated with NO2- concentration than NO3- concentration. Sinks and Lifetime of NO• in Seawater. In the present work, the overall scavenging rate constants of NO• Σ(ks, NO• [s]) in the surface seawater samples ranged from 0.05 to 0.33 s-1 (mean 0.24 s-1, n ) 20). The low scavenging rate constant of NO• in seawater could be attributed to the relatively low reactivity of NO• with the major dissolved compounds in seawater. As observed by Zafiriou et al. (21), altering several trace constituents that vary widely in seawater did not produce major changes in NO•aq yields or decay rates. This suggested that sea salts have little or no effect on the scavenging rate constant of NO• in seawater. In our previous report, we postulated that the reaction of NO• with the photochemically generated reactive oxygen species (ROS), such as hydroxyl radicals (•OH), superoxide anion (O2•-), and alkyl peroxyl radicals (ROO•), could be one of the pathways for NO• loss in natural waters (10). To test this hypothesis, the concentrations of •OH were determined in the same seawater samples used for the determination of the scavenging rate constant of NO•. Procedural details for the determination of •OH have been reported elsewhere (14, 17). The photoformation rates, scavenging rate constants, and steady-state concentrations of •OH in the Seto Inland Sea are shown in Supporting Information Table S1. The steady-state concentrations of •OH in the water samples ranged from 4.8 × 10-18 to 19 × 10-18 M, which are similar to those reported for Biscayne Bay seawater (8.5 -11.4 × 10-18 M) (22) and Temperate Coastal waters (10.6 × 10-18 M) (23). Although no measurements of O2•- and ROO• were made during this cruise, the steadystate concentrations of O2•- in coastal and open ocean waters have been well documented, and are in the range 2-55 × 10-11 and 2-16 × 10-11 M, respectively (24, 25). However, VOL. 44, NO. 22, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
8405
measurement of ROO• concentrations in seawater have not been reported (26). The percentage contributions of •OH, O2•- and ROO• to the observed scavenging rate constants of NO• in seawater were estimated using eq 7: % ) Si, NO· × 100/
∑ (k
s,NO·[S])
(7)
where Si, NO• is the reaction rate of each NO• scavenger with NO• (i ) •OH, O2•-, ROO•) and Σ (ks, NO• [s]) is the observed scavenging rate constant of NO•. Thus, Si, NO• can be calculated by: Si, NO· ) ki, NO· × [i]
(8)
where ki, NO• is the rate constant for the reaction with the individual scavenger (M-1s-1), and [i] is the concentration of a given individual NO• scavenger in seawater. The reaction rates of O2•-, •OH and ROO• with NO• are well established (27-31), and they have second-order rate constants ranging from 5.6 × 107 to 6.7 × 109, 1.0 × 1010 and 2 × 109 M-1s-1, respectively. Using the published rate constant (30) and the average steady-state concentration of •OH determined in this study (Table S1 of the SI), the scavenging rate of NO• by •OH accounted for 0.45 µm) while the second portion remained unfiltered. The samples were analyzed in triplicate for NO• photoformation rates following the procedure described in this paper. There was no significant difference between the formation rates of NO• in the filtered and unfiltered seawater samples (See Figure S3 of the SI). This is reasonable, because nitrification and denitrification processes are not expected to occur in sunlit surface waters due to light inhibition and high oxygen concentration, respectively 8406
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 22, 2010
(8). Our results suggest that particulate matter (>0.45 µm) does not appear to be a major source or sink of the photochemically formed NO• in seawater. Therefore, we conclude that photobiological processes are insignificant, and that homogeneous photochemical processes dominate NO• production in sunlit surface waters. Steady-State Concentration of NO• in Seawater. The assessment of NO• steady-state concentrations ([NO•]ss) in the seawater is crucial to understanding its biogeochemical role and also for the determination of the NO• flux from seawater to the atmosphere. Steady-state concentrations of NO• can be estimated using eq 9: [NO·]ss ) RNO· /
∑ (k
s,NO·[S])
(9)
Using this approach, the measured NO• steady state concentrations of the surface seawater samples ranged from 2.4 × 10-11 to 32 × 10-11 M, with an average concentration of 12 × 10-11 M. The steady-state concentrations of NO• in surface waters are calculated based on the light flux representative of noon solar radiation intensity (under clear sky conditions) on May 1, 1998. Therefore, [NO]ss tends toward the upper limit and the time-weighted average NO• concentrations are less because of the variations in the solar irradiance by the time of the day. Previous work by Zafiriou and McFarland showed that the steady state concentration of NO• in the central equatorial Pacific was ∼10-11 M (5). In a separate study by Liu et al. (32), the NO• concentration in Qingdao coastal waters was 12 × 10-11 M, which agrees with the result in this study. Estimation of the Sea-to-Air Flux of NO•. The sea-to-air flux of NO• (FNO in molm-2 s-1) was estimated as in previous studies (33-35) using the following formula: FNO ) KL(Cw - KHPNO)
(10)
where KL is the liquid phase transfer velocity; Cw, KH and PNO are defined as the concentrations in surface seawater, Henry’s law constant and partial pressure of NO•, respectively; and KL was calculated as a function of wind speed and the Schmidt number using the relationship established by Wanninkhof (34). KL ) 2.778 × 10-6(0.31U2(Sc/660)-1/2)
(11)
The Schmidt number for NO• was taken as Sc ) (µ/D), where µ is the kinematic viscosity of seawater, and D is the diffusion coefficient of NO• in seawater. The kinematic viscosity (0.994 × 10-6 m2s-1) and diffusion coefficient (3.07 × 10-9 m2 s-1) were adapted from Andreas (36) and Zhou et al. (37), respectively. In this work, we computed the KL value using in situ wind speed data, which were measured on board at about 10 m elevation from the surface with an average value of 5 m s-1. Thus, the estimated value of KL was 3.0 × 10-5 m s-1. Meanwhile, the atmospheric concentration of NO• was needed to calculate the sea-to-air fluxes. Unfortunately, due to time limitations, the atmospheric NO• concentration in the Seto Inland Sea was not measured during this cruise. However, atmospheric NO• concentrations in the ranges of 10-11 to 10-12 atm have been widely reported in the marine boundary layer and marine free troposphere (6, 38-40). If we assume that the atmospheric NO• concentrations in the Seto Inland Sea are as high as 10-10 atm, (1 to 2 orders of magnitude higher than the reported values for marine boundary layers), and the average value of the surface seawater concentration determined in this study (12 × 10-11 M, corresponding to pNO (sea) of 6.3 × 10-8 atm), then the bulk surface seawater was thus supersaturated with NO• by factors up to 102.
On the basis of the average value of the surface seawater concentration, the assumed atmospheric NO• concentration (10-10 atm), and the transfer velocity (KL), the flux of NO• from sea-to-air was estimated to be 3.55 × 10-12 mol m-2 s-1. This is comparable to the NO• flux reported previously for the central equatorial Pacific (-2.2 × 10-16 mol cm-2 s-1; FNO ) kl (Cair/H-Csea) (5)). Therefore, the annual flux over the 23 000 km2 of the Seto Inland Sea was estimated to be 7.6 × 107 g N yr-1. From these results, we infer that this region may serve as a net source of NO• to the atmosphere. Future studies are targeted at the simultaneous determination of the atmospheric and seawater NO• concentrations in the Seto Inland Sea. Environmental Significance of NO•. Although NO• may only be present in extremely small concentrations in seawater, the results of our studies indicate that NO• generation in natural surface seawater is large enough to cause strong supersaturation of the surface seawater, which are in excellent agreement with the conclusions of the previous investigator (5). As recognized by Jacob and Hilker (41), NO• could be transferred to the gas phase because of its low solubility in aqueous solution. In the atmosphere, NO• is a key species involved in the photochemistry of ozone and acidic precipitation. The concentration of NO• relative to ozone and the rate of oxidation of carbon monoxide and methane determine whether photochemistry results in a net source or net sink of ozone in the troposphere (2-4). Further, the reaction of NO• with volatile organic compounds (VOCs) could lead to the formation of HNO3 which is often a major component of acidic precipitation. In addition to the effects on the atmosphere, it is conceivable that NO• has a biological impact. Studies have shown that NO• influences the growth of phytoplankton in the marine environment (42). Although NO• can increase the growth of red tide alga at low concentrations, it can also inhibit it at high NO• concentrations. Therefore, understanding the distribution of NO• in seawater may help explain the formation and disappearance mechanisms for phytoplankton blooms in seawater. Also, nitric oxide in aqueous solution reacts with a variety of free radicals at diffusion controlled rates (28-31), thereby changing their concentrations and altering their fates in seawater. However, whether NO• influences the redox chemistry of trace metals in seawater or not is subject to further investigation.
Acknowledgments The authors gratefully acknowledge the Japan Society for the Promotion of Science for financial support through a Grant-in-Aid for Scientific Research (B) (18310010).The financial support received from Kurita Water and Environment Foundation is also appreciated.
Supporting Information Available A map showing the sampling stations (Figure S1), chemicals and a detailed description of experimental procedures for the determination of reaction rate constant of DAF-2 with NO• in air-saturated solution at neutral pH and procedure for the determination of hydroxyl radicals in seawater. This material is available free of charge via the Internet at http:// pubs.acs.org.
Literature Cited (1) Aneja, V. P.; Robarge, W. P.; Sullivan, L. J.; Moore, T. C.; Pierce, T. E.; Geron, C.; Gay, B. Seasonal variations of nitric oxide flux from agricultural soils in the Southeast United States. Tellus 1996, 48B, 626–640. (2) Atlas, E. L.; Ridley, B. A.; Hubler, G.; Walega, J. G.; Carroll, M. A.; Montzka, D. D.; Huebert, B. J.; Norton, R. B.; Grahek, F. E.; Schauffler, S. Partitioning and budget of NOy species during the Mauna Loa observatory photochemistry experiment. J. Geophys. Res. 1 992, 97 (D10), 449–462.
(3) Ridley, B. A.; Carroll, M. A.; Dunlap, D. D.; Trainer, M.; Sachse, G. W.; Gregory, G. L.; Condon, E. P. Measurements of NOx over the eastern Pacific Ocean and southwestern United States during the spring 19984 NASA GTE aircraft program. J. Geophys. Res. 1989, 94, 5043–5057. (4) Crutzen, P. J. The role of NO• and NO2 in the chemistry of the troposphere and stratosphere. Annu. Rev. Earth Planet. Sci. 1979, 7, 443–472. (5) Zafiriou, O. C.; McFarland, M. Nitric oxide from nitrite photolysis in the central equatorial pacific. J. Geophys. Res. 1981, 86, 3173– 3182. (6) Zafiriou, O. C.; McFarland, M.; Bromund, R. H. Nitric oxide in seawater. Science 1980, 207, 637–639. (7) Zhang, Z. B.; Liu, C. Y.; Wu, Z. Z.; Xing, L.; Li, P. F. Detection of nitric oxide in culture media and studies on nitric oxide formation by marine microalgae. Med. Sci. Monit. 2006, 12 (2), BR75–85. (8) Ward, B. B.; Zafiriou, O. C. Nitrification and nitric oxide in the oxygen minimum of the eastern tropical North Pacific. Deep Sea Res. 1988, 35 (7), 1127–1142. (9) Zhang, Z.; Xing, L.; Wu, Z.; Liu, C.; Lin, C.; Liu, L. Discovery of nitric oxide in marine ecological system and the chemical characteristics of nitric oxide. Sci. China Ser. B-Chem 2006, 49 (5), 475–480. (10) Olasehinde, E. F.; Takeda, K.; Sakugawa, H. Development of an analytical method for nitric oxide radical determination in natural waters. Anal. Chem. 2009, 81 (16), 6843–6850. (11) Yamamoto, T. The Seto Inland Sea--eutrophic or oligotrophic. Mar. Pollut. Bull. 2003, 47, 37–42. (12) Zhang, J. Z.; Fischer, C. J. A simplified resorcinol method for direct spectrophotometric determination of nitrate in seawater. Mar. Chem. 2006, 99, 220–226. (13) Herold, S.; Rock, G. Reaction of deoxy-, oxy-, and methmoglobin with nitrogen monoxide: Mechanistic studies of the s-nitrosothiol formation under different mixing conditions. J. Biol. Chem. 2003, 278, 6623–6634. (14) Arakaki, T.; Faust, B. C. Sources, sinks, and mechanisms of hydroxyl radical ( · OH) photoproduction and consumption in authentic acidic continental cloud waters from Whiteface Mountain, New york: The role of the Fe(r) (r ) II, III) photochemical cycle. J. Geophys. Res. 1998, 103 (D3), 3487– 3504. (15) Espey, M. G.; Thomas, D. D.; Miranda, K. M.; Wink, D. A. Focusing of nitric oxide mediated nitrosation and oxidative nitrosylation as a consequence of reaction with superoxide. Proc Natl. Acad. Sci. U.S.A. 2002, 99, 11127–11132. (16) Jourd’heuil, D.; Jourd’heuil, F. L.; Feelisch, M. Oxidation and nitrosation of thiols at low micromolar exposure to nitric oxide. J. Biol. Chem. 2003, 278 (18), 15720–15726. (17) Arakaki, T.; Miyake, T.; Shibata, M.; Sakugawa, H. Photochemical formation and scavenging of hydroxyl radical in rain and dew waters. J. Chem. Soc. Jpn. 1998, 619–625. (18) Gomes, A.; Fernandes, E.; Lima, J. L. Use of fluorescence probes for detection of reactive nitrogen species: A review. J. Fluoresc. 2006, 16, 119–139. (19) Loegager, T.; Sehested, K. Formations and decay of peroxynitric acid: a pulse radiolysis study. J. Phys. Chem. 1993, 97 (25), 6664– 6669. (20) Smith, R. L.; Yoshinari, T. Occurrence and Turnover of nitric oxide in nitrogen -impacted sand and gravel aquifer. Environ. Sci. Technol. 2008, 42 (22), 8245–8251. (21) Zafiriou, O. C.; Mcfarland, M. Determination of trace levels of nitric oxide in aqueous solution. Anal. Chem. 1980, 52 (11), 1662–1667. (22) Zhou, X.; Mopper, K. Determination of photochemically produced hydroxyl radicals in seawater and fresh water. Mar. Chem. 1990, 30, 71–88. (23) Mopper, K.; Zhou, X. Hydroxyl radical photoproduction in the sea and its potential impact on marine processes. Science 1990, 250, 661–664. (24) Hansard, S. P.; Vermilyea, A. W.; Voelker, B. M. Measurements of superoxide radical concentration and decay kinetics in the Gulf of Alaska. Deep Sea Res. Part 1 2010, 05, 007, doi: 10.10116/j.dsr. (25) Rose, A. L.; Webb, E. A.; Waite, T. D.; Moffett, J. W. Measurement and implications of nonphotochemically generated superoxide in the equatorial Pacific Ocean. Environ. Sci. Technol. 2008, 42, 2387–2393. (26) Dahl, E. E.; Saltzman, E. S. Alkyl nitrate photochemical production rates in North Pacific seawater. Mar. Chem. 2008, 112, 137–141. (27) Huie, R. E.; Padmaja, S. The reaction of NO• with superoxide. Free Rad. Res. Commun. 1993, 18 (4), 195–199. VOL. 44, NO. 22, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
8407
(28) Saran, M.; Michel, C.; Bors, W. Reaction of NO• with O2•-. Implications for the action of endothelium-derived relaxing factor (EDRF). Free Rad. Res. Cornms. 1990, 10, 221–226. (29) Padmaja, S.; Huie, R. E. The reaction of nitric oxide with organic peroxyl radicals. Biochem. Biophys. Res. Commun. 1993, 195 (2), 539–544. (30) Buxton, G. V.; Greenstock, C. L.; Helman, W. P.; Ross, A. B. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (•OH/O•-) in aqueous solution. J. Phys. Chem. Ref. Data 1988, 17, 513– 886. (31) Mack, J.; Bolton, J. R. Photochemistry of nitrite and nitrate in aqueous solution: A review. J. Photochem. Photobiol. A: Chem. 1999, 128, 1–13. (32) Liu, C.; Zhao, M.; Ren, C.; Yang, G.; Li, P.; Han, Y. Direct measurement of nitric oxide in seawater medium by fluorometric method. Chinese J. Anal. Chem. 2009, 37 (10), 1463– 1467. (33) Matsunaga, S.; Mochida, M.; Saito, T.; Kawamura, K. In situ measurement of isoprene in the marine air and surface seawater from the western North Pacific. Atmos. Environ. 2002, 36, 6051– 6057. (34) Wanninkhof, R. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 1992, 97 (C5), 7373– 7382. (35) Zhang, G.; Zhang, J.; Xu, J.; Zhang, F. Distributions, sources and atmospheric fluxes of nitrous oxide in Jiaozhou Bay. Est. Coast. Shelf Sci. 2006, 68, 557–566.
8408
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 22, 2010
(36) Andreas, E. L. A Handbook of Physical Constants and Functions for Use in Atmospheric Boundary Layer Studies; ERDC/CRREL M-05-1, U.S. Army Cold Regions Research and Engineering Laboratory: Hanover, NH, 2005, 55. (37) Zhou, Z.; Todd, B. D.; Travis, K. P.; Sadus, R. J. A molecular dynamics of study of nitric oxide in water: Diffusion and structure. J. Chem. Phys. 2005, 123 (5), 054505. (38) Ridley, B. A.; Carroll, M. A.; Gregory, G. L. Measurements of nitric oxide in the boundary layer and free troposphere over the Pacific Ocean. J. Geophys. Res. 1987, 92 (D2), 2025–2047. (39) Carroll, M. A.; Ridley, B. A.; Montzka, D. D.; Hubler, G.; Walega, J. G.; Norton, R. B.; Huebert, B. J.; Grahek, F. E. Measurements of nitric oxide and nitrogen dioxide during the Mauna Lao Observatory Photochemistry Experiment. J. Geophys. Res. 1992, 97 (10), 361–374. (40) Carsey, T. P.; Churchil, D. D.; Farmer, M. L.; Fischer, C. J.; Pszenny, A. A.; Ross, V. B.; Saltzman, E. S.; Springer-Young, M.; Bonsang, B. Nitrogen oxides and ozone production in the North Atlantic marine boundary layer. J. Geophys. Res. 1997, 102 (D9), 10653–10665. (41) Jacobi, H.-W.; Hilker, B. J. A mechanism for the photochemical transformation of nitrate in snow. Photochem. Photobiol. A: Chem. 2007, 185, 371–382. (42) Zhang, Z.; Lin, C.; Liu, C.; Xing, L.; Wu, Z.; Sun, F. Studies on pattern and chemical features of NO• effect on marine phytoplankton growth. Sci. China, Ser. B: Chem 2005, 48 (4), 376–384.
ES101426X
