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Hydrogen peroxide production in marine bathing waters: Implications for fecal indicator bacteria mortality
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Marine Pollution Bulletin 56 (2008) 397–401 www.elsevier.com/locate/marpolbul
Review
Hydrogen peroxide production in marine bathing waters: Implications for fecal indicator bacteria mortality Catherine D. Clark a,*, Warren J. De Bruyn a, Scott D. Jakubowski a, Stanley B. Grant b b
a Department of Chemistry, Chapman University, One University Drive, Orange, CA 92866, USA Henry Samueli School of Engineering, Department of Chemical Engineering and Materials Science, University of California, Irvine, CA 92697, USA
Abstract Hydrogen peroxide concentrations [H2O2] have been measured over the last two decades in multiple studies in surface waters in coastal, estuarine and oceanic systems. Diurnal cycles consistent with a photochemical production process have frequently being observed, with [H2O2] increasing by two orders of magnitude over the course of the day, from low nM levels in the early morning to 102 nM in late afternoon. Production rates range from <10 for off-shore ocean waters to 20–60 nM h1 for near-shore coastal and estuarine environments. Slow night-time loss rates (<10 nM h1) have been attributed to biological and particle mediated processes. Diurnal cycles have also frequently been observed in fecal indicator bacteria (FIB) levels in surf zone waters monitored for microbial water quality. Measured peak peroxide concentrations in surface coastal seawaters are too low to directly cause FIB mortality based on laboratory studies, but likely contribute to oxidative stress and diurnal cycling. Peroxide levels in the surf zone may be increased by additional peroxide production mechanisms such as deposition, sediments and stressed marine biota, further enhancing impacts on FIB in marine bathing waters. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Peroxide; Fecal indicator bacteria; Coastal waters
1. Introduction In recent years there has been increased concern over the microbial quality of marine recreational bathing waters. Public beaches in the USA with >50,000 visitors per year are mandated to participate in water quality monitoring programs. Microbial water quality is assessed from the concentration of fecal indicator bacteria (FIB) (US EPA, 2000), based on epidemiological evidence linking measurements of these indicators to adverse health outcomes (Cabelli et al., 1979; Wade et al., 2003). In California, beaches are posted with warning notices if the state’s single sample standards for FIB are exceeded (US EPA, 1986). For example, Huntington State Beach in Southern California has experienced frequent FIB contamination episodes *
Corresponding author. Tel.: +1 714 628 7341; fax: +1 714 532 6048. E-mail address: [email protected] (C.D. Clark).
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in the surf zone, resulting in multiple beach closures and postings (Boehm et al., 2002). Previous studies at this site suggest a complex interplay of FIB contributions from non-point sources, including urban runoff from the watershed and birds in the coastal marshes, and potential point sources from the Orange County Sanitation District sewage outfall system (Grant et al., 2001; Boehm et al., 2004; Kim et al., 2004; Reeves et al., 2004; Grant et al., 2005). Diurnal cycles in FIB have been observed in the surf zone (Boehm et al., 2002), and attributed to UV radiationinduced mortality, biological predation and/or oxidative stress from natural photochemically-produced oxidizing agents like hydrogen peroxide. Elevated levels of hydrogen peroxide have previously been shown to cause damage and cell lysis in microorganisms (Gonzalez-Flecha and Demple, 1997; Weinbauer and Suttle, 1999), and implicated as a cause of FIB mortality in marine sewage fields (Mitchell and Chamberlin, 1975).
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Here we review peroxide concentrations, production and loss rates reported in near- and off-shore surface seawater studies in the literature, and discuss the implications for FIB levels in the surf zone. 2. Peroxide production and loss mechanisms in seawater Hydrogen peroxide is a key intermediate in aquatic redox processes in chemical and biological systems, acting as a strong oxidizing agent that reacts with trace metals and pollutants (O’Sullivan et al., 2005 and references therein). It is a common transient in natural waters, with surface maxima on the order of 102 nM in a variety of marine environments. The primary production process in seawater involves photochemical reactions that occur when colored dissolved organic matter (CDOM) absorbs UV radiation (Lean et al., 1994). CDOM is a highly complex colored material that contains humic substances. Most CDOM in coastal waters comes from riverine or wetland inputs of terrestrially derived materials from plant degradation, but may also be produced from grazing phytoplankton and viral-induced lysis in the ocean (Hessen and Tranvik, 1998). The reaction of oxygen molecules with photo-excited CDOM generates superoxide O 2 and its conjugate acid HO2, which dismutate to form hydrogen peroxide and oxygen (O’Sullivan et al., 2005): CDOM þ O2 ! CDOMþ þ O 2
ð1Þ
O 2
ð2Þ
þ H2 O ! HO2 þ OH
HO2 þ HO2 ! H2 O2 þ O2 HO2 þ O 2 þ H2 O ! H2 O2 þ O2 þ OH
ð3Þ ð4Þ
As one of the most stable CDOM photoproducts with a half-life of several to one hundred hours, hydrogen peroxide has been used as an indicator of photochemical activity in aquatic ecosystems (Szymczak and Waite, 1991; Miller, 1994; Herut et al., 1998) and as a tracer for vertical water movements (Johnson et al., 1989). Increased levels have been measured in coastal environments with high CDOM inputs from rivers (Zika et al., 1985a; Moore et al., 1993; Amouroux and Donard, 1995; Kieber and Heltz, 1995; Cooper et al., 2000; O’Sullivan et al., 2005; Miller et al., 2005). Additional possible sources of hydrogen peroxide to surface seawater include atmospheric input via dry and wet deposition (Gunz and Hoffmann, 1990; Sakugawa et al., 1990) and biological production by algae (Palenik and Morel, 1988; Moffett and Zafiriou, 1990; Collen et al., 1995). These sources are insignificant compared to in situ abiotic photochemical production (Thompson and Zafiriou, 1983; Zika et al., 1985b; Cooper et al., 1989; Petasne and Zika, 1997). However, wet deposition has been shown to be an intermittent significant source over localized areas during rain events (Kieber et al., 2001; Avery et al., 2005), with peroxide concentrations in rainwater over the ocean ranging from 10 to 80 lM (Yuan and Shiller, 2000 and references therein).
Diurnal cycling in hydrogen peroxide has been previously observed, with high concentrations during the day when photochemical production is occurring and low concentrations at night when loss processes dominate. The dominant removal process in seawater has been attributed to biological decomposition involving peroxidase enzymes from marine plankton and bacteria (Cooper and Zepp, 1990; Moffett and Zafiriou, 1993; Petasne and Zika, 1997). Other potential sinks include catalytic decomposition mediated by transition metals, halides and particles, photochemical decomposition and physical mixing dynamics (Moffett and Zafiriou, 1993; Petasne and Zika, 1997). 3. Peroxide seawater measurements Peroxide concentrations have being measured in many previous surface seawater measurements using an enzyme-mediated fluorescence peroxidase technique developed by Zika and Saltzman (1982). Other early studies used a fluorometric method adapted to measurements in seawater by Miller and Kester (1988), based on the dimerization of (p-hydroxyphenyl)acetic acid (POHPAA) by hydrogen peroxide in the presence of peroxidase. A more recently developed chemiluminescence method involving the reaction of peroxide with an acridinium ester does not suffer from background fluorescence matrix effects in organic rich environments, making it more useful in fresher waters with higher DOM inputs (Cooper et al., 2000). These three methods have similar H2O2 detection limits of 5 nM in seawater. Although these are non-selective techniques which cannot separate hydrogen peroxide from other organic peroxides, a recent intercomparison showed that other organic peroxides comprise an insignificant fraction of the total peroxide load in seawater and inferred that previous measurements made with non-selective techniques measured only H2O2 in seawater (Miller et al., 2005). O’Sullivan et al. (2005) recently adapted a gas-phase hydroperoxide method for analyses in surface waters with HPLC separation, followed by post-column derivitization with POHPAA to produce a fluorescent dimmer. This technique is less sensitive than earlier methods (H2O2 detection limit 30 nM), but differentiates between hydrogen peroxide and other short chain organic peroxides. Table 1 summarizes field measurements of hydrogen peroxide concentrations in surface seawater over the last two decades. Concentrations range from <10 to 440 nM, with higher levels associated with higher CDOM inputs from rivers. Well defined diurnal cycles in peroxide, consistent with a dominant photochemical production process and a relatively constant destruction process, have often been observed. A time lag of 4 h between sunrise and increasing peroxide concentration has been previously noted (Miller and Kester, 1994). Diel changes of 25– 60 nM have been previously measured in most surface seawaters. The net production rate of hydrogen peroxide between the low early morning levels and maximum concentrations in the afternoon can be estimated from the ini-
C.D. Clark et al. / Marine Pollution Bulletin 56 (2008) 397–401 Table 1 Hydrogen peroxide concentrations (in nM) in surface seawater [H2O2]
Location
100–240 Gulf of Mexico – coastal 8–70 Peru – coast and off-shore estuarine 125–154 Sargasso Sea 100–150 Western Mediterranean 15–110 Great Barrier Reef 60–120 Eastern Caribbean – Spring 95–420 Eastern Caribbean – Fall <10–400 Coastal Seto Inland Sea 11–350 Estuarine, off Patuxent River, USA 138–186 Bay of Biscay, France 22–256 Gironde estuary, France 10–80 Mediterranean Sea 8–100 Red Sea 20–80 Baltic Sea 110–260 Coastal seawater 25–200 Subtropical Atlantic Ocean 25–80 Atlantic Ocean 440 Estuarine, Chesapeake Bay 37 Grizzly Bay, California 60–280 Coastal seawater off Rhode Island
Reference Zika et al. (1985a) Zika et al. (1985b) Palenik and Morel (1988) Johnson et al. (1989) Szymczak and Waite (1991) Moore et al. (1993) Moore et al. (1993) Fujiwara et al. (1993) Kieber and Heltz (1995) Amouroux and Donard (1995) Amouroux and Donard (1995) Herut et al. (1998) Herut et al. (1998) Herut et al. (1998) Cooper et al. (2000) Obernosterer et al. (2001) Avery et al. (2005) O’Sullivan et al. (2005) O’Sullivan et al. (2005) Miller et al. (2005)
tial and final surface concentrations. A summary of net peroxide production rates in seawater from the literature is given in Table 2. Net production rates of 2–10 nM h1 have been reported for off-shore surface seawaters, with higher production rates of 17–56 nM h1 in estuarine and coastal waters with riverine inputs (Table 2). Formation
Table 2 Net hydrogen peroxide production rates (NHPPR) in nM h1 in surface seawater NHPPR a
3.3 24 8.3a 2.7–3.4 7.1a 3.3a 17a 25a 33a 6–50a 4±1 20–30a 5.6a 8.9a 2.4–3.5 5.5 2.2–9.4 56a
Location
Reference
Sargasso Sea Canal waters, Florida Western Mediterranean Vineyard Sound Great Barrier Reef Eastern Caribbean, oligotrophic off-shore Eastern Caribbean, coastal Eastern Caribbean, estuarine Eastern Caribbean, in Orinoco River Coastal Seto Inland Sea Sargasso Sea Estuarine, off Patuxent River, USA Mediterranean Sea Red Sea Antarctic waters Subtropical Atlantic Ocean Atlantic Ocean Coastal seawater off Rhode Island
Palenik and Morel (1988) Cooper et al. (1988) Johnson et al. (1989) Moffett and Zafiriou (1990) Szymczak and Waite (1991) Moffett and Zafiriou (1993) Moffett and Zafiriou (1993) Moffett and Zafiriou (1993) Moffett and Zafiriou (1993) Fujiwara et al. (1993) Miller and Kester (1994) Kieber and Heltz (1995) Herut et al. (1998) Herut et al. (1998) Yocis et al. (2000) Obernosterer et al. (2001) Avery et al. (2005) Miller et al. (2005)
a Estimated from published diurnal cycle (maximum–minimum concentration)/(hours from sunrise to peak concentration).
399
rates are much higher in lakes and rivers, ranging from 81 to 2120 nM h1 (Scully et al., 1996); this increase in fresher waters corresponds to higher levels of CDOM and enhanced photochemical production. The overall net night-time loss rate of peroxide is low. Estimated dark loss rates in coastal surface waters range from 0.5 to 5.5 nM h1 (Great Barrier Reef – Szymczak and Waite, 1991) and 3.6 nM h1 (Vineyard Sound – Moffett and Zafiriou, 1990), to higher values of 7.2 nM h1 (Western Mediterranean – Johnson et al., 1989) and 10 nM h1 measured in highly productive coastal waters (Biscayne Bay, Florida – Petasne and Zika, 1997). The dark decomposition of hydrogen peroxide has been primarily attributed to biologically mediated processes by marine microorganisms <1 lM in diameter, since filtering dramatically reduces loss rates (Petasne and Zika, 1997) and a positive relationship between bacteria abundance and peroxide decay rates has been shown (Petasne and Zika, 1997). Other loss pathways include particle mediated processes (Petasne and Zika, 1997). 4. Implications for FIB mortality and cycling Elevated levels of hydrogen peroxide have been shown to cause damage and cell lysis in microorganisms (Gonzalez-Flecha and Demple, 1997; Weinbauer and Suttle, 1999), and implicated as a cause of FIB mortality in marine sewage fields (Mitchell and Chamberlin, 1975). Sunlight inactivates bacteria in seawater (Fujioka et al., 1981), indicating a photochemical or photo-oxidative process is occurring. Based on laboratory studies showing that an exogenous hydrogen peroxide concentration of 105 M activated the expression of catalase (Gonzalez-Flecha and Demple, 1997), the peroxide levels measured in coastal seawater, while high, are still too low to directly cause cell lysis. However, these laboratory experiments were conducted in the dark, and it is possible that cells exposed to sunlight may be sensitized to lower concentrations of peroxide. In one study, Weinbauer and Suttle (1999) found reduced bacterial abundances in coastal waters with as little as 100 nM hydrogen peroxide, but concluded that peroxide-induced lysogenic phage production was not an important source of bacterial mortality. Low levels of 100 nM hydrogen peroxide caused oxidative stress to bacteria in coastal waters based on increasing catalase enzyme concentration (Angel et al., 1999), and the diurnal periodicity in catalase activity matched the diurnal changes in hydrogen peroxide. This suggests that oxidative stress caused by hydrogen peroxide may become important above the 102 nM level in sunlit surface seawaters. In a general sense, the peroxide concentrations on the order of 200–300 nM measured in near-shore waters are too low to directly cause cell lysis but would likely contribute to oxidative stress and increased UV-induced mortality rates of FIB. However, hydrogen peroxide production and destruction mechanisms and therefore overall levels may be different in the dynamic surf zone environment where FIB
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levels are monitored and regulated. Sources could thus be larger in marine bathing waters than sources in near shore or open ocean waters. An increase in atmospheric peroxide concentrations at ebb tide during daylight has previously been observed at a coastal site (Morgan and Jackson, 2002), and was attributed to the formation of hydrogen peroxide under stress from seaweed (Collen and Pedersen, 1996) and aquatic plants in the intertidal zone, followed by diffusion of the peroxide through the biological membranes and cell walls into the layer of air above the tidal region (Morgan and Jackson, 2002). Another possible ebb tide source is the formation of peroxide via reduction of oxygen by Fe(II) in beach sediments containing high levels of reduced iron (Cooper et al., 2000). Dry deposition from the gas phase has frequently being cited as an insignificant source of peroxide to surface seawaters in the ocean (Zika et al., 1985a,b; Palenik and Morel, 1988; Szymczak and Waite, 1991; Fujiwara et al., 1993; Kieber et al., 2001; Avery et al., 2005), based on early estimates by Thompson and Zafiriou (1983). However, these previous calculations were based on open ocean deposition velocities and typical atmospheric concentrations (1–10 ppbv). Air-sea exchange should increase in the surf zone. Also, given that hydrogen peroxide is strongly partitioned into the liquid phase (Henry’s Law constant kh = 8.33 104 M atm1; O’Sullivan et al., 1996), gas phase concentrations could increase significantly in the surf zone in coastal areas with a substantial marine layer (like the west coast of the US) as the early morning fog layer burns off. In addition, a recent study in coastal Southern California showed that hydrogen peroxide concentrations associated with urban aerosol liquid particles were >2 orders of magnitude higher than predicted by Henry’s Law, suggesting increased in situ production in anthropogenically impacted atmospheres in urban areas (Arellanes et al., 2006). Peroxide levels could also be elevated in the surf zone due to production from local pollution sources. One previous study has shown elevated production rates in polluted coastal waters with substantial anthropogenic inputs (Herut et al., 1998), attributed to other organic material and metal inputs leading to additional photochemical pathways. The advection of water parcels with higher levels of peroxide into a sampling site by long-shore or rip cell currents could also increase local peroxide levels. While additional sources and production mechanisms may be active in the surf zone, this would not necessarily increase hydrogen peroxide levels since peroxide sinks may also increase in the surf zone due to turbulence and bacterial loading. For example, particle-mediated loss processes might be more significant in the surf zone than oligotrophic off-shore waters due to the higher sediment load and turbidity from wave action. If peroxide levels were significantly increased, this would enhance oxidative impacts on FIB in marine bathing waters. Clearly, more extensive studies are needed on peroxide concentrations and production mechanisms in the surf zone where FIB levels and
cycling are of major concern to regulatory agencies and recreational beach-goers. Acknowledgments C.D.C. thanks the Office of Naval Research for support (#N00014-01-1-0030). S.B.G. thanks the National Water Research Institute (#03-WQ-001). References Amouroux, D., Donard, O.F.X., 1995. Hydrogen peroxide determination in estuarine and marine waters by flow injection with fluorescence detection. Oceanol. Acta 18, 353–361. Angel, D.L., Fiedler, U., Eden, N., Kress, N., Adelung, D., Herut, B., 1999. Catalase activity in macro- and micro-organisms as an indicator of biotic stress in coastal waters of the eastern Mediterranean Sea. Helgoland Mar. Res. 53, 209–218. Arellanes, C., Paulson, S.E., Fine, P.M., Sioutas, C., 2006. Exceeding of Henry’s Law by hydrogen peroxide associated with urban aersols. Environ. Sci. Technol. 40, 4859–4866. Avery Jr., G. Brooks, Cooper, W.J., Kieber, R.J., Willey, J.D., 2005. Hydrogen peroxide at the Bermuda Atlantic Time Series Station: temporal variability of seawater hydrogen peroxide. Mar. Chem.. Boehm, A.B., Grant, S.B., Kim, J.H., Mowbray, S.L., McGee, C.D., Clark, C.D., Foley, D.M., Wellman, D.E., 2002. Decadal and shorter period variability of surf-zone water quality at Huntington Beach, California. Environ. Sci. Technol. 36, 3885. Boehm, A.B., Lluch-Cota, D.B., Davis, K.A., Winant, C.D., Monismith, S.G., 2004. Covariation of coastal water temperature and microbial pollution at interannual to tidal periods. Geophys. Res. Lett. 31, L06309. Cabelli, V., Dufour, A.P., Levin, M.A., McCabe, L.J., Harberman, P.W., 1979. Relationship of microbial indicators to health effects at marine bathing beaches. Am. J. Public Health 69, 690–695. Collen, J., Pedersen, M., 1996. Production, scavenging and toxicity of hydrogen peroxide in green seaweed Ulva rigida. Eur. J. Phycol. 31, 265–271. Collen, J., Del Rio, M.J., Garcia-Reiana, G., Pedersen, M., 1995. Photosynthetic production of hydrogen peroxide by Ulva rigida C. Ag. (Chlorophyta). Planta 196, 225–230. Cooper, W.J., Zepp, R.G., 1990. Hydrogen peroxide decay in water with suspended soils: evidence for biologically mediated processes. Can. J. Fish. Aquat. Sci. 47, 888–893. Cooper, W.J., Zika, R.G., Petasne, R.G., Plane, J.M.C., 1988. The photochemical formation of peroxide in natural waters exposed to sunlight. Environ. Sci. Technol. 22, 1156–1160. Cooper, W.J. et al., 1989. In: Suffet, J.H., MacCarthy, P. (Eds.), Aquatic Humic Substances, . In: Influence on Fate and Treatment of Pollutants, vol. 219. American Chemical Society, Washington, DC, pp. 333–362 (Chapter 22). Cooper, W.J., Moegling, J.K., Kieber, R.J., Kiddle, J.J., 2000. A chemiluminescence method for the analysis of H2O2 in natural waters. Mar. Chem. 70, 191–200. Fujioka, R.S., Hashimoto, H.H., Siwak, E.B., Young, R.H.F., 1981. Effect of sunlight on survival of indicator bacteria in seawater. Appl. Environ. Microbiol. 41, 690–696. Fujiwara, K., Ushiroda, T., Takeda, K., Kumamato, Y., Tsubota, H., 1993. Diurnal and seasonal distribution of hydrogen peroxide in seawater of the Seto Inland Sea. Geochem. J. 27, 103–115. Gonzalez-Flecha, B., Demple, B., 1997. Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli. J. Bacteriol. 47, 382–388. Grant, S.B., Sanders, B.F., Boehm, A.B., Redman, J.A., Kim, J.H., Mrse, R.D., Chu, A.K., Gouldin, M., McGee, C.D., Gardiner, N.A., Jones, B.H., Svejkovsky, J., Leipzig, G.V., Brown, A., 2001. Generation of
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Marine Pollution Bulletin 56 (2008) 397–401 www.elsevier.com/locate/marpolbul
Review
Hydrogen peroxide production in marine bathing waters: Implications for fecal indicator bacteria mortality Catherine D. Clark a,*, Warren J. De Bruyn a, Scott D. Jakubowski a, Stanley B. Grant b b
a Department of Chemistry, Chapman University, One University Drive, Orange, CA 92866, USA Henry Samueli School of Engineering, Department of Chemical Engineering and Materials Science, University of California, Irvine, CA 92697, USA
Abstract Hydrogen peroxide concentrations [H2O2] have been measured over the last two decades in multiple studies in surface waters in coastal, estuarine and oceanic systems. Diurnal cycles consistent with a photochemical production process have frequently being observed, with [H2O2] increasing by two orders of magnitude over the course of the day, from low nM levels in the early morning to 102 nM in late afternoon. Production rates range from <10 for off-shore ocean waters to 20–60 nM h1 for near-shore coastal and estuarine environments. Slow night-time loss rates (<10 nM h1) have been attributed to biological and particle mediated processes. Diurnal cycles have also frequently been observed in fecal indicator bacteria (FIB) levels in surf zone waters monitored for microbial water quality. Measured peak peroxide concentrations in surface coastal seawaters are too low to directly cause FIB mortality based on laboratory studies, but likely contribute to oxidative stress and diurnal cycling. Peroxide levels in the surf zone may be increased by additional peroxide production mechanisms such as deposition, sediments and stressed marine biota, further enhancing impacts on FIB in marine bathing waters. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Peroxide; Fecal indicator bacteria; Coastal waters
1. Introduction In recent years there has been increased concern over the microbial quality of marine recreational bathing waters. Public beaches in the USA with >50,000 visitors per year are mandated to participate in water quality monitoring programs. Microbial water quality is assessed from the concentration of fecal indicator bacteria (FIB) (US EPA, 2000), based on epidemiological evidence linking measurements of these indicators to adverse health outcomes (Cabelli et al., 1979; Wade et al., 2003). In California, beaches are posted with warning notices if the state’s single sample standards for FIB are exceeded (US EPA, 1986). For example, Huntington State Beach in Southern California has experienced frequent FIB contamination episodes *
Corresponding author. Tel.: +1 714 628 7341; fax: +1 714 532 6048. E-mail address: [email protected] (C.D. Clark).
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in the surf zone, resulting in multiple beach closures and postings (Boehm et al., 2002). Previous studies at this site suggest a complex interplay of FIB contributions from non-point sources, including urban runoff from the watershed and birds in the coastal marshes, and potential point sources from the Orange County Sanitation District sewage outfall system (Grant et al., 2001; Boehm et al., 2004; Kim et al., 2004; Reeves et al., 2004; Grant et al., 2005). Diurnal cycles in FIB have been observed in the surf zone (Boehm et al., 2002), and attributed to UV radiationinduced mortality, biological predation and/or oxidative stress from natural photochemically-produced oxidizing agents like hydrogen peroxide. Elevated levels of hydrogen peroxide have previously been shown to cause damage and cell lysis in microorganisms (Gonzalez-Flecha and Demple, 1997; Weinbauer and Suttle, 1999), and implicated as a cause of FIB mortality in marine sewage fields (Mitchell and Chamberlin, 1975).
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Here we review peroxide concentrations, production and loss rates reported in near- and off-shore surface seawater studies in the literature, and discuss the implications for FIB levels in the surf zone. 2. Peroxide production and loss mechanisms in seawater Hydrogen peroxide is a key intermediate in aquatic redox processes in chemical and biological systems, acting as a strong oxidizing agent that reacts with trace metals and pollutants (O’Sullivan et al., 2005 and references therein). It is a common transient in natural waters, with surface maxima on the order of 102 nM in a variety of marine environments. The primary production process in seawater involves photochemical reactions that occur when colored dissolved organic matter (CDOM) absorbs UV radiation (Lean et al., 1994). CDOM is a highly complex colored material that contains humic substances. Most CDOM in coastal waters comes from riverine or wetland inputs of terrestrially derived materials from plant degradation, but may also be produced from grazing phytoplankton and viral-induced lysis in the ocean (Hessen and Tranvik, 1998). The reaction of oxygen molecules with photo-excited CDOM generates superoxide O 2 and its conjugate acid HO2, which dismutate to form hydrogen peroxide and oxygen (O’Sullivan et al., 2005): CDOM þ O2 ! CDOMþ þ O 2
ð1Þ
O 2
ð2Þ
þ H2 O ! HO2 þ OH
HO2 þ HO2 ! H2 O2 þ O2 HO2 þ O 2 þ H2 O ! H2 O2 þ O2 þ OH
ð3Þ ð4Þ
As one of the most stable CDOM photoproducts with a half-life of several to one hundred hours, hydrogen peroxide has been used as an indicator of photochemical activity in aquatic ecosystems (Szymczak and Waite, 1991; Miller, 1994; Herut et al., 1998) and as a tracer for vertical water movements (Johnson et al., 1989). Increased levels have been measured in coastal environments with high CDOM inputs from rivers (Zika et al., 1985a; Moore et al., 1993; Amouroux and Donard, 1995; Kieber and Heltz, 1995; Cooper et al., 2000; O’Sullivan et al., 2005; Miller et al., 2005). Additional possible sources of hydrogen peroxide to surface seawater include atmospheric input via dry and wet deposition (Gunz and Hoffmann, 1990; Sakugawa et al., 1990) and biological production by algae (Palenik and Morel, 1988; Moffett and Zafiriou, 1990; Collen et al., 1995). These sources are insignificant compared to in situ abiotic photochemical production (Thompson and Zafiriou, 1983; Zika et al., 1985b; Cooper et al., 1989; Petasne and Zika, 1997). However, wet deposition has been shown to be an intermittent significant source over localized areas during rain events (Kieber et al., 2001; Avery et al., 2005), with peroxide concentrations in rainwater over the ocean ranging from 10 to 80 lM (Yuan and Shiller, 2000 and references therein).
Diurnal cycling in hydrogen peroxide has been previously observed, with high concentrations during the day when photochemical production is occurring and low concentrations at night when loss processes dominate. The dominant removal process in seawater has been attributed to biological decomposition involving peroxidase enzymes from marine plankton and bacteria (Cooper and Zepp, 1990; Moffett and Zafiriou, 1993; Petasne and Zika, 1997). Other potential sinks include catalytic decomposition mediated by transition metals, halides and particles, photochemical decomposition and physical mixing dynamics (Moffett and Zafiriou, 1993; Petasne and Zika, 1997). 3. Peroxide seawater measurements Peroxide concentrations have being measured in many previous surface seawater measurements using an enzyme-mediated fluorescence peroxidase technique developed by Zika and Saltzman (1982). Other early studies used a fluorometric method adapted to measurements in seawater by Miller and Kester (1988), based on the dimerization of (p-hydroxyphenyl)acetic acid (POHPAA) by hydrogen peroxide in the presence of peroxidase. A more recently developed chemiluminescence method involving the reaction of peroxide with an acridinium ester does not suffer from background fluorescence matrix effects in organic rich environments, making it more useful in fresher waters with higher DOM inputs (Cooper et al., 2000). These three methods have similar H2O2 detection limits of 5 nM in seawater. Although these are non-selective techniques which cannot separate hydrogen peroxide from other organic peroxides, a recent intercomparison showed that other organic peroxides comprise an insignificant fraction of the total peroxide load in seawater and inferred that previous measurements made with non-selective techniques measured only H2O2 in seawater (Miller et al., 2005). O’Sullivan et al. (2005) recently adapted a gas-phase hydroperoxide method for analyses in surface waters with HPLC separation, followed by post-column derivitization with POHPAA to produce a fluorescent dimmer. This technique is less sensitive than earlier methods (H2O2 detection limit 30 nM), but differentiates between hydrogen peroxide and other short chain organic peroxides. Table 1 summarizes field measurements of hydrogen peroxide concentrations in surface seawater over the last two decades. Concentrations range from <10 to 440 nM, with higher levels associated with higher CDOM inputs from rivers. Well defined diurnal cycles in peroxide, consistent with a dominant photochemical production process and a relatively constant destruction process, have often been observed. A time lag of 4 h between sunrise and increasing peroxide concentration has been previously noted (Miller and Kester, 1994). Diel changes of 25– 60 nM have been previously measured in most surface seawaters. The net production rate of hydrogen peroxide between the low early morning levels and maximum concentrations in the afternoon can be estimated from the ini-
C.D. Clark et al. / Marine Pollution Bulletin 56 (2008) 397–401 Table 1 Hydrogen peroxide concentrations (in nM) in surface seawater [H2O2]
Location
100–240 Gulf of Mexico – coastal 8–70 Peru – coast and off-shore estuarine 125–154 Sargasso Sea 100–150 Western Mediterranean 15–110 Great Barrier Reef 60–120 Eastern Caribbean – Spring 95–420 Eastern Caribbean – Fall <10–400 Coastal Seto Inland Sea 11–350 Estuarine, off Patuxent River, USA 138–186 Bay of Biscay, France 22–256 Gironde estuary, France 10–80 Mediterranean Sea 8–100 Red Sea 20–80 Baltic Sea 110–260 Coastal seawater 25–200 Subtropical Atlantic Ocean 25–80 Atlantic Ocean 440 Estuarine, Chesapeake Bay 37 Grizzly Bay, California 60–280 Coastal seawater off Rhode Island
Reference Zika et al. (1985a) Zika et al. (1985b) Palenik and Morel (1988) Johnson et al. (1989) Szymczak and Waite (1991) Moore et al. (1993) Moore et al. (1993) Fujiwara et al. (1993) Kieber and Heltz (1995) Amouroux and Donard (1995) Amouroux and Donard (1995) Herut et al. (1998) Herut et al. (1998) Herut et al. (1998) Cooper et al. (2000) Obernosterer et al. (2001) Avery et al. (2005) O’Sullivan et al. (2005) O’Sullivan et al. (2005) Miller et al. (2005)
tial and final surface concentrations. A summary of net peroxide production rates in seawater from the literature is given in Table 2. Net production rates of 2–10 nM h1 have been reported for off-shore surface seawaters, with higher production rates of 17–56 nM h1 in estuarine and coastal waters with riverine inputs (Table 2). Formation
Table 2 Net hydrogen peroxide production rates (NHPPR) in nM h1 in surface seawater NHPPR a
3.3 24 8.3a 2.7–3.4 7.1a 3.3a 17a 25a 33a 6–50a 4±1 20–30a 5.6a 8.9a 2.4–3.5 5.5 2.2–9.4 56a
Location
Reference
Sargasso Sea Canal waters, Florida Western Mediterranean Vineyard Sound Great Barrier Reef Eastern Caribbean, oligotrophic off-shore Eastern Caribbean, coastal Eastern Caribbean, estuarine Eastern Caribbean, in Orinoco River Coastal Seto Inland Sea Sargasso Sea Estuarine, off Patuxent River, USA Mediterranean Sea Red Sea Antarctic waters Subtropical Atlantic Ocean Atlantic Ocean Coastal seawater off Rhode Island
Palenik and Morel (1988) Cooper et al. (1988) Johnson et al. (1989) Moffett and Zafiriou (1990) Szymczak and Waite (1991) Moffett and Zafiriou (1993) Moffett and Zafiriou (1993) Moffett and Zafiriou (1993) Moffett and Zafiriou (1993) Fujiwara et al. (1993) Miller and Kester (1994) Kieber and Heltz (1995) Herut et al. (1998) Herut et al. (1998) Yocis et al. (2000) Obernosterer et al. (2001) Avery et al. (2005) Miller et al. (2005)
a Estimated from published diurnal cycle (maximum–minimum concentration)/(hours from sunrise to peak concentration).
399
rates are much higher in lakes and rivers, ranging from 81 to 2120 nM h1 (Scully et al., 1996); this increase in fresher waters corresponds to higher levels of CDOM and enhanced photochemical production. The overall net night-time loss rate of peroxide is low. Estimated dark loss rates in coastal surface waters range from 0.5 to 5.5 nM h1 (Great Barrier Reef – Szymczak and Waite, 1991) and 3.6 nM h1 (Vineyard Sound – Moffett and Zafiriou, 1990), to higher values of 7.2 nM h1 (Western Mediterranean – Johnson et al., 1989) and 10 nM h1 measured in highly productive coastal waters (Biscayne Bay, Florida – Petasne and Zika, 1997). The dark decomposition of hydrogen peroxide has been primarily attributed to biologically mediated processes by marine microorganisms <1 lM in diameter, since filtering dramatically reduces loss rates (Petasne and Zika, 1997) and a positive relationship between bacteria abundance and peroxide decay rates has been shown (Petasne and Zika, 1997). Other loss pathways include particle mediated processes (Petasne and Zika, 1997). 4. Implications for FIB mortality and cycling Elevated levels of hydrogen peroxide have been shown to cause damage and cell lysis in microorganisms (Gonzalez-Flecha and Demple, 1997; Weinbauer and Suttle, 1999), and implicated as a cause of FIB mortality in marine sewage fields (Mitchell and Chamberlin, 1975). Sunlight inactivates bacteria in seawater (Fujioka et al., 1981), indicating a photochemical or photo-oxidative process is occurring. Based on laboratory studies showing that an exogenous hydrogen peroxide concentration of 105 M activated the expression of catalase (Gonzalez-Flecha and Demple, 1997), the peroxide levels measured in coastal seawater, while high, are still too low to directly cause cell lysis. However, these laboratory experiments were conducted in the dark, and it is possible that cells exposed to sunlight may be sensitized to lower concentrations of peroxide. In one study, Weinbauer and Suttle (1999) found reduced bacterial abundances in coastal waters with as little as 100 nM hydrogen peroxide, but concluded that peroxide-induced lysogenic phage production was not an important source of bacterial mortality. Low levels of 100 nM hydrogen peroxide caused oxidative stress to bacteria in coastal waters based on increasing catalase enzyme concentration (Angel et al., 1999), and the diurnal periodicity in catalase activity matched the diurnal changes in hydrogen peroxide. This suggests that oxidative stress caused by hydrogen peroxide may become important above the 102 nM level in sunlit surface seawaters. In a general sense, the peroxide concentrations on the order of 200–300 nM measured in near-shore waters are too low to directly cause cell lysis but would likely contribute to oxidative stress and increased UV-induced mortality rates of FIB. However, hydrogen peroxide production and destruction mechanisms and therefore overall levels may be different in the dynamic surf zone environment where FIB
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levels are monitored and regulated. Sources could thus be larger in marine bathing waters than sources in near shore or open ocean waters. An increase in atmospheric peroxide concentrations at ebb tide during daylight has previously been observed at a coastal site (Morgan and Jackson, 2002), and was attributed to the formation of hydrogen peroxide under stress from seaweed (Collen and Pedersen, 1996) and aquatic plants in the intertidal zone, followed by diffusion of the peroxide through the biological membranes and cell walls into the layer of air above the tidal region (Morgan and Jackson, 2002). Another possible ebb tide source is the formation of peroxide via reduction of oxygen by Fe(II) in beach sediments containing high levels of reduced iron (Cooper et al., 2000). Dry deposition from the gas phase has frequently being cited as an insignificant source of peroxide to surface seawaters in the ocean (Zika et al., 1985a,b; Palenik and Morel, 1988; Szymczak and Waite, 1991; Fujiwara et al., 1993; Kieber et al., 2001; Avery et al., 2005), based on early estimates by Thompson and Zafiriou (1983). However, these previous calculations were based on open ocean deposition velocities and typical atmospheric concentrations (1–10 ppbv). Air-sea exchange should increase in the surf zone. Also, given that hydrogen peroxide is strongly partitioned into the liquid phase (Henry’s Law constant kh = 8.33 104 M atm1; O’Sullivan et al., 1996), gas phase concentrations could increase significantly in the surf zone in coastal areas with a substantial marine layer (like the west coast of the US) as the early morning fog layer burns off. In addition, a recent study in coastal Southern California showed that hydrogen peroxide concentrations associated with urban aerosol liquid particles were >2 orders of magnitude higher than predicted by Henry’s Law, suggesting increased in situ production in anthropogenically impacted atmospheres in urban areas (Arellanes et al., 2006). Peroxide levels could also be elevated in the surf zone due to production from local pollution sources. One previous study has shown elevated production rates in polluted coastal waters with substantial anthropogenic inputs (Herut et al., 1998), attributed to other organic material and metal inputs leading to additional photochemical pathways. The advection of water parcels with higher levels of peroxide into a sampling site by long-shore or rip cell currents could also increase local peroxide levels. While additional sources and production mechanisms may be active in the surf zone, this would not necessarily increase hydrogen peroxide levels since peroxide sinks may also increase in the surf zone due to turbulence and bacterial loading. For example, particle-mediated loss processes might be more significant in the surf zone than oligotrophic off-shore waters due to the higher sediment load and turbidity from wave action. If peroxide levels were significantly increased, this would enhance oxidative impacts on FIB in marine bathing waters. Clearly, more extensive studies are needed on peroxide concentrations and production mechanisms in the surf zone where FIB levels and
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