Dissolved Organic Matter Composition Drives the Marine Production

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Dissolved Organic Matter Composition Drives the Marine Production of Brominated Very Short-Lived Substances Yina Liu,*,†,‡,⊗ Daniel C. O. Thornton,† Thomas S. Bianchi,†,§ William A. Arnold,∥ Michael R. Shields,†,§ Jie Chen,†,⊥ and Shari A. Yvon-Lewis† †

Department of Oceanography, Texas A&M University, College Station, Texas 77843, United States Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, United States § Department of Geological Sciences, University of Florida, Gainesville, Florida 32611, United States ∥ Department of Civil, Environmental, and Geo-Engineering, University of Minnesota, 500 Pillsbury Drive SE, Minneapolis, Minnesota 55455, United States ⊥ South China Sea Marine Engineering and Environment Institution, Guangzhou, Guangdong 510310, China ‡

S Supporting Information *

ABSTRACT: Brominated very short-lived substances (BrVSLS), such as bromoform, are important trace gases for stratospheric ozone chemistry. These naturally derived trace gases are formed via bromoperoxidase-mediated halogenation of dissolved organic matter (DOM) in seawater. Information on DOM type in relation to the observed BrVSLS concentrations in seawater, however, is scarce. We examined the sensitivity of BrVSLS production in relation to the presence of specific DOM moieties. A total of 28 model DOM compounds in artificial seawater were treated with vanadium bromoperoxidase (V-BrPO). Our results show a clear dependence of BrVSLS production on DOM type. In general, molecules that comprise a large fraction of the bulk DOM pool did not noticeably affect BrVSLS production. Only specific cell metabolites and humic acid appeared to significantly enhance BrVSLS production. Amino acids and lignin phenols suppressed enzyme-mediated BrVSLS production and may instead have formed halogenated nonvolatile molecules. Dibromomethane production was not observed in any experiments, suggesting it is not produced by the same pathway as the other BrVSLS. Our results suggest that regional differences in DOM composition may explain the observed BrVSLS concentration variability in the global ocean. Ultimately, BrVSLS production and concentrations are likely affected by DOM composition, reactivity, and cycling in the ocean.

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per trillion of Bry to the stratosphere (BryVSLS), which is equivalent to ∼4 to 36% of the total stratospheric bromine.1 Naturally emitted CHBr3 and CH2Br2 account for a large fraction of the BryVSLS.5 CHBr3, CH2Br2, CHClBr2, and CHBrCl2 are mainly derived from natural sources in seawater, and are thought to be associated with macro- and microalgal production by an enzyme-mediated pathway. It has been suggested that haloperoxidases, such as the vanadium bromoperoxidases (VBrPO), catalyze the oxidation of bromine and iodine in the presence of hydrogen peroxide (H2O2) and form a variety of reactive oxidized halogen species,6−8 with hypobromous acid (HOBrenz) as the primary enzymatic product.8 The resulting HOBrenz halogenates a range of organic matter (OM)

INTRODUCTION Bromoform (CHBr3), dibromomethane (CH2Br2), chlorodibromomethane (CHClBr 2 ), and bromodichloromethane (CHBrCl2) constitute a substantial fraction of atmospheric brominated very short-lived substances (BrVSLS), which are defined as brominated trace gases with atmospheric lifetimes CHClBr2 > CHBrCl2 (Figure S3 and Tables S1 and S2 of the Supporting Information). This concentration order is consistent with that in seawater chlorination treatments, in which hypochlorous acid (HOCl) rapidly converts to HOBr yielding CHBr3 as a major trihalomethane product.27 This observation may suggest that while V-BrPO is not capable of catalyzing chlorine oxidation, a trace amount of HOCl was formed from excess amounts of HOBrenz. The resulting HOCl subsequently chlorinated the brominated intermediates to form CHClBr2 and CHBrCl2. Although previous studies have suggested that CHClBr2 and CHBrCl2 are formed as the results of chlorine substitution of CHBr3,28 the rate of substitution is too slow to be considered here.29 Our results are consistent with the observation reported by Liu et al.,14 who suggested that CHClBr2 and CHBrCl2 in the euphotic zone and aged deep-water masses may have originated from disparate sources. The authors suggested that CHClBr2 and CHBrCl2 in aged deep-water masses are the results of chlorine substitution of CHBr3; but in the euphotic zone, they are likely produced in situ by enzyme-mediated halogenation of DOM.14 Production of CH2Br2, which is often significantly correlated with CHBr3 in the ocean,14,30 was not observed in any experiments. This finding further suggests that the mechanisms of V-BrPO-mediated production of CHBr3, CHClBr2, and 3369

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acid, glycolic acid, and urea. Enolizable carboxylic acids, such as citric acid, are known to be effective trihalomethane precursors in water chlorination processes.44 The halogenation of citric acid is initiated with HOCl-induced decarboxylation and chloroform is released after subsequent serial chlorination reactions.44 It is not surprising, therefore, that citric acid significantly enhanced CHBr3 production in the presence of HOBrenz. We hypothesize that halogenation of glycolic acid and alginic acid may occur via similar mechanisms as citric acid, although not as efficiently. Based on this hypothesis, pyruvic acid should be able to produce trihalomethanes as well, but it may be a slow or low yield producer that was out competed by the background DOM. Glycolic acid was one of the model DOM compounds that slightly enhanced CHBr3 production upon V-BrPO induced halogenation. This particular metabolite is produced during photorespiration by phytoplankton.45−47 H2O2, which is required for V-BrPO to generate HOBrenz, is also produced in the light via photolysis of DOM and phytoplankton photosynthesis.48,49 A strong correlation between H2O2 and CHBr3 concentrations was observed from several algal species isolated from the Baltic Sea under photo-oxidative stress.50 Our experiments suggest that CHBr3 production is enhanced during conditions conducive to photorespiration not only because more H2O2 is available for HOBrenz formation, but also because glycolic acid enhanced CHBr3 production. Urea, an important metabolite produced by organisms, showed significant enhancement of CHBr3 production. The mechanism of urea bromination and the resulting enhancement is not clear. We speculate that a portion of urea rapidly formed tribromamine (NBr3),51 which could then form HOBr via further oxidation. Thus, urea served as a reservoir of HOBr capacity, allowing a higher probability for HOBr to encounter CHBr3 precursors after other highly reactive, non-CHBr3 forming precursors were consumed. In the field, a substantially elevated BrVSLS concentration was observed near the Canary Islands with low chlorophyll a concentrations.14,52 Elevated heterotrophic bacteria abundance and urea concentrations were also observed in this area.14 Liu et al.14 speculated that the presence of reactive DOM led to elevated BrVSLS concentrations in this area. Based on the results presented in this study, we postulate that urea played an important role in regulating CHBr3 formation. Urea has been used as an indicator of amino acid cycling by bacteria53,54 and is both excreted and utilized by bacteria.54 Because bacteria play an important role in regulating DOM composition in seawater, they may also play an important role, albeit indirect, in BrVSLS production. Alginic acid, an acidic polysaccharide that is widely distributed in brown algae,55 also enhanced CHBr3 production. It is well-known that brown algae are prolific producers of CHBr3.30 The prolific CHBr3 production from macroalgae has long been explained by the presence of abundant V-BrPO, for V-BrPO activity has been observed in a diverse range of macroalgae.6,10,49 Here, we showed that in addition to V-BrPO, brown algae also possess suitable substrates for enzymemediated CHBr3 formation. Humic acid was able to substantially enhance CHBr3 production though present at a lower concentration than other model DOM compounds, which is consistent with results reported in drinking water treatment studies.56,57 Humic acid is a known substrate for CHBr3 formation upon halogenation with HOBr, which is formed either via an enzymatic pathway or NaOCl conversion in seawater.56−58 This finding suggests that

Carbohydrates are one of the dominant forms of extracellular organic carbon produced by phytoplankton and encompass a significant fraction of the marine DOM pool.34−36 In the surface ocean, polysaccharides account for as much as 50% of the high molecular weight DOM.37 Multiple processes, however, likely affect whether these important components of DOM are effective precursors for CHBr3. First, they are competing with other more reactive DOM constituents, such as the fast reacting precursors (e.g., compounds with resorcinol structures38). Second, due to the slow reacting nature of carbohydrates in trihalomethane formation, halogenation of carbohydrates in the environment may be subject to other competing processes, such as uptake by bacteria. This is particularly important for monosaccharides that are rapidly cycled, such as glucose. Among the model DOM compounds tested in this study, we found more compounds were capable of suppressing CHBr3 production than enhancing it. Substituting V-BrPO and H2O2 with NaOCl, the active ingredient in water chlorination, yielded the same result, which confirmed that the reduction in CHBr3 production was not caused by competitive inhibition of the enzyme. Ascorbic acid has been shown to scavenge HOCl to protect lipoprotein oxidation.39 Ascorbate undergoes a fast reaction with bromine,40 and thus, inhibited halogenation of other DOM molecules and CHBr3 production. Aliphatic amino acids have been shown to be poor trihalomethane precursors in water chlorination experiments.41 In contrast, phenolic structures are expected to be effective trihalomethane precursors, but the kinetics of trihalomethane formation can be slow.25,42 The fact that aromatic and aliphatic amino acids and phenols suppressed CHBr3 formation relative to the background indicates these model DOM moieties are more reactive than the background DOM with HOBrenz, but the products observed after 4 h were not the trace gases we monitored in this study. In the case of aliphatic amino acids, halogenation reactions may preferentially form nonvolatile compounds such as the haloacetic acids (HAAs) and haloamines. On the other hand, phenols may rapidly form halophenol intermediates via electrophilic substitution reactions,43 but the incubation time was not long enough for CHBr3 to be released, because further halogenation is required.42 It is likely that nonvolatile halogenated phenols were formed as an end product due to H2O2 limited HOBrenz formation. For example, phenol red has been shown to suppress CHBr3 production in this and other studies. Instead of forming CHBr3, phenol red is brominated to bromophenol blue (Figure S4 of the Supporting Information).22 Similarly, halogenation of aromatic amino acids is expected to occur at the aromatic rings, and hence halogenated tryptophan and tyrosine are expected as the end products in our experiments. For compounds with aromatic rings to release CHBr3 and other trihalomethanes, repeated exposure to halogenating agents like HOBrenz is required to achieve the eventual ring opening and subsequently C−C bond cleavage.43 It should be noted that the reaction rate decreased with increasing halide substitution.43 Thus, we propose that although aromatic compounds are known precursors for trihalomethanes in water chlorination treatments, these compounds may not be as important in the surface ocean. Although only a few of the model DOM compounds examined in this study enhanced CHBr3 production relative to HASW, most of these compounds are important metabolites produced by phytoplankton and other organisms, such as citric 3370

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Figure 2. CHBr3 concentrations observed from dual model DOM compound experiment. (a) Tryptophan, (b) vanillin, (c) phenol red, (d) Dglucose, and (e) ultrapure water were mixed with urea at relative fractions of 50%, 10%, 0.5%, and 0% (i.e., 100% urea), to make up a total DOM concentration of ∼1.0 mM C. Gray bars depicted CHBr3 concentration observed from V-BrPO treated ASW (i.e., HASW).

even small amounts of reactive DOM have a significant impact on CHBr3 production. Dual Substrate Experiments. Three model DOMsuppressed compounds (tryptophan, vanillin, and phenol red) were chosen for the dual DOM experiments. Each compound was mixed at ratios defined in the Experimental Section with urea, a DOMenhanced compound. In addition, D-glucose, which belongs to the DOMno effect group, and ultrapure water were individually mixed with urea. Mixtures containing tryptophan, vanillin, and phenol red at the relative proportions of 50%, 10%, and 0.5% of the added DOM concentration resulted in significant reductions in CHBr3 concentrations, relative to 0% addition of these compounds (i.e., 100% added urea) (Figure 2). D-Glucose mixed with urea in various proportions exhibited a similar trend as ultrapure water mixed with urea. Such a consistency between D-glucose and ultrapure water mixed with urea experiments confirmed that the CHBr3 production trends observed in these experiments were the result of dilution of urea. These experiments with dual model DOM compounds represent a highly simplified scenario compared with the broad array of molecules that comprise DOM under in situ conditions. Nonetheless, this

work clearly shows that CHBr3 production is governed by more complex processes than previously thought, such as the composition of the DOM pool. The presence of DOMsuppressed, even at trace relative concentrations (0.5%), substantially reduces CHBr3 production, and these compounds may or may not ultimately release CHBr3 via repeated exposure to HOBrenz after the fast reacting precursors are exhausted. Ultimately, CHBr3 production is driven by the relative concentrations of different compounds within the complex DOM pool in seawater and their reactivity. Implications for BrVSLS Biogeochemistry in the Ocean. CHBr3 concentration in seawater follows a broad trend with chlorophyll a concentration.14,19,52 In the water column, the CHBr3 tends to be elevated near the subsurface chlorophyll maximum depth.15,59 These observations suggest that the involvement of phytoplankton, and presumably VBrPO activity, is essential for CHBr3 and the other BrVSLS production. CHBr3 concentration, however, usually does not significantly correlate with chlorophyll a concentration. Even though CHBr3 concentrations tend to be elevated with elevated chlorophyll a, significant variability in productive waters is observed.15,31 Several explanations have been suggested, 3371

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Environmental Science & Technology including effects of sea-to-air fluxes of CHBr3, different turnover rates between CHBr3 and chlorophyll a, phytoplankton species specificity for V-BrPO production, physical mixing, the influence of anthropogenic input, and DOM specificity for CHBr3 production.14,31,60 Although these processes can, to some extent, alter the relationship between CHBr3 and chlorophyll a, a factor that is more directly linked to the enzyme-mediated pathway is suggested in a recent study, namely variability of V-BrPO activity in seawater.9 Only a small fraction of HOBrenz, however, ultimately turns into CHBr3, as observed by Hill and Manley,61 which suggests V-BrPO induced HOBrenz and hence V-BrPO activity may not be a limiting factor for CHBr3 production in seawater. Moreover, HOBrenz is unlikely the only reactive bromine species that is capable of brominating DOM in seawater. Results from Leri et al.62 and Méndez-Dı ́az et al.63 show that halogenation of DOM is also achieved abiotically. In fact, the pseudocorrelations between CHBr3 and phytoplankton taxa may be due to different proportion of organic moieties produced by different phytoplankton groups. Phytoplankton that produce higher proportion of lipids and proteins have been found to be more effective trihalomethane precursors.33 This is particularly important in the open ocean because phytoplankton and associated bacteria control the composition of the bulk DOM pool.64 In the coastal ocean, the relationship between CHBr3 and photosynthetic biomass exhibit no significant correlation, which has been attributed to complex coastal circulation and anthropogenic sources of CHBr3.31 We speculate that such an insignificant relationship is, in fact, due to a supply of allochthonous DOM, which contains effective CHBr3 precursors, such as the humic and fulvic acids. These nonalgal DOM sources likely out-compete algal-derived DOM in CHBr3 formation. Our findings here are consistent with Karlsson et al.,65 who proposed that elevated concentrations of brominated volatile compounds observed in sea ice brine and upper waters were attributable to high concentration of riverine dissolved organic matter discharged to the Arctic Ocean. Thus, results from this study offer another plausible explanation for the relationship between CHBr3 production and photosynthetic biomass. We hypothesize that the variability in CHBr3 production is affected by DOM type, interactions between different DOM compounds, as well as DOM fate in seawater. These processes will affect the relative abundance and reactivity of DOMsuppressed and DOMenhanced compounds in seawater. Moreover, different turnover rates and degradation processes of various DOM moieties likely affect CHBr3 formation potential. For the slow reacting precursors, they are subject to various competing processes such as microbial utilization and photodegradation, in addition to chemical competition for halogenating species like HOBrenz. Thus, despite the relatively short reaction time used in this study, our results are environmentally relevant. We suggest that to better understand BrVSLS biogeochemistry, it is important to better understand the driving factors that are more directly related to the final products, such as organic matter (OM) characterization of both the dissolved and particulate fraction, for halogenation of marine particulate organic matter (POM) was also observed by Leri and colleagues.62,66 BrVSLS are only a subset of compounds produced by organic matter halogenation. Halogenation reactions with organic matter can potentially create stable compounds that are preserved in the sediment.66 As more

powerful analytical tools become available for the characterization of OM in seawater,67,68 it will be possible to start to investigate BrVSLS biogeochemistry in relation to OM chemical characterization and also to investigate the role of halogenation in the cycling of organic carbon.

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ASSOCIATED CONTENT

S Supporting Information *

Additional experimental details, figures, and tables as noted in the text. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Y. Liu. Phone: 508-289-3834. Fax: 508-457-2164. E-mail: yina. [email protected]. Present Address ⊗

Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, United States Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Dr. Steven L. Manley at California State University− Long Beach for his generous donation of some of the vanadium bromoperoxidase used in this study. Dr. Lisa Campbell and Dr. Gunnar Schade at Texas A&M University and the anonymous reviewers provided insightful comments on the paper.

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DOI: 10.1021/es505464k Environ. Sci. Technol. 2015, 49, 3366−3374