Other ROS

"OH+ HCO3- -+H20 + C03-•OH+ C032- ->0H-+C03-

The carbonate radical will also form its conjugate acid, the bicarbonate radical:

The bicarbonate radical, HCO3', is more acidic than HC03~ (pKa = 10.3 vs. 106, respectively), but the pKa for equilibrium (16) is poorly constrained with reported values between 7.0-9.6 [150-152]. In many fresh water systems the predominant species will be the bicarbonate radical, while both the bicarbonate and carbonate radicals will be important in seawater. As may be expected, the reactivity of the carbonate radical with many organic and inorganic species will be pH dependent [153].

Huang and Mabury [154] used a radical trapping approach to determine steady state concentrations of the carbonate radical in a variety of fresh water environments. In their study, carbonate radical concentrations ranged from 5 x 10~15 to 10~13 M, and were a function of DOM and nitrate concentrations (which are the main sources of the 'OH radical in these waters), and alkalinity. The wavelength dependence and quantum yields for carbonate radical production are not known, but it is expected that they will mirror the action spectra for *OH radical production, and therefore will largely be confined to wavelengths in the UV-B extending out to approximately 330-340 nm [47],

The main fate of the carbonate radical is likely through reaction with DOM [155], This would not be surprising, since the carbonate radical behaves as a strong oxidant with a wide range of organic compounds including sulfides, phenols, aromatic anilines, amino acids and proteins. It primarily reacts through a one-electron oxidation pathway, although addition or H-atom abstraction pathways have also been reported [156,157], The one-electron oxidation pathway yields oxidized DOM and the carbonate anion:

Rate constants for reaction of the carbonate radical with a variety of organic compounds in aqueous solution range from less than 103 to 109 1 mol-1 s_1 (Table 5). A comprehensive tabulation of rate constants is given in Neta et al. [158]. Many of these reactions are temperature dependent characterized by an Arrhenius response [156]. Competing with DOM, the carbonate radical is fairly reactive towards inorganic species in aqueous solution (Table 5) including 02~ and H202 [159]:

H202 + C03- -»products fc = 8 x 1051 mol"1 s"1 (18)

02-+C03-^C032-+ 02 k = 4x lOMmol"1 s"1 (19)

At an 02~ and C03~ concentration of 10~9 M and 10-14 M, respectively, the carbonate radical loss rate is 4 x 10"15 Ms-1. This removal rate is comparable to some of the faster organic reactions noted above. However, when all of the organic reactants are considered together, it is likely that they will control the fate of the carbonate radical in the photic zone. The importance of these pathways will also depend on other factors such as the concentration of DOM, which indirectly controls the production and loss of H202 and 02~.

Table 5. Rate constants for the reaction of different organic compounds with the carbonate radical in aqueous solution at or near room temperature.

Compound

PH

molds')

Reference

Formate ion

6.4

1.1 x 105

[227]

Methanol

13.0

6.02 x 103

[157]

Acetate ion

12.1-12.7

6.0 x 102

[228]

Propanol

13.0

4.65 x 104

[157]

Acetone

12.1-12.7

1.6 x 102

[228]

Ascorbate ion

11.4

1.2 x 109

[156]

Glucose

7.0

7 x 104

[229]

Cyclohexanol

13.0

9.37 x 104

[157]

Tetrahydrofuran

13.0

1.00 x 105

[157]

Indole

7.0

4.1 x 10s

[230]

Benzene

7.0

3 x 103

[229]

Hydroquinone

11.4

1.9 x 109

[156]

Phenolate ion

11.4

1.3 x 109

[156]

Phenol

7.0

2.2 x 107

[229]

Aniline

9.0

4.6 x 108

[234]

Urea

7.0

< 1 x 103

[229]

Uracil

7.0

<1 x 104

[229]

Butylamine

11.5

4.0 x 105

[231]

Glutathione

7.0

5.3 x 106

[229]

Thioanisole

11.0

2.3 x 107

[155]

Dithiothreitol

10.5

4.1 x 108

[232]

Glycine

7.0

< 1 x 103

[229]

Alanine

7.0

< 1 x 103

[229]

Arginine

7.0

9 x 104

[229]

Methionine

7.0

3.6 x 107

[229]

Tryptophan

7.0

7.0 x 108

[230]

Glycylglycyltryptophan

7.0

7.0 x 108

[230]

Lysozyme

7.0

5.5 x 108

[229]

Trypsin

7.0

6.8 x 108

[229]

Carbonate radical

7.0-9.0

2.0 x 107

[227]

Nitrite ion

11.4

4.8 x 105

[156]

8.4 Impact of ROS on aquatic organisms

Intracellular production of ROS such as 02~, H202, *02 and the 'OH radical present some of the most pressing challenges to biological systems [37,90]. ROS react with biomolecules, such as proteins, lipids or DNA, modifying or destroying their intended functionality in a process known as oxidative stress. Organisms invest considerable cellular resources to prevent or repair oxidative damage and this is especially true for photosynthetic organisms, which generate ROS as part of the photosynthetic process [2]. While it is well documented that ROS produced inside the cell can adversely affect an organism, very little is known about the effect of externally generated ROS (i.e., species produced in the water surrounding the cell) on the growth and health of aquatic organisms.

In general, the impact of ROS on aquatic organisms should be inversely related to the reactivity of the ROS. For example, the direct effect of externally-generated *OH radicals on aquatic microorganisms is expected to be minimal because it is extremely reactive, which results in an extremely short lifetime that does not allow for significant transport to the cell surface [160]. However, production of the OH radical outside the cell may exert an indirect effect on cellular systems through the production of longer-lived free radical species such as the carbonate radical (which can potentially affect algal uptake of inorganic carbon) and the dibromide radical ion (Figure 1). These longer-lived free radical species are present at higher steady state concentrations in natural waters compared to the *OH radical (ca. 10~14 vs. 10-18 M) [4], and they are less reactive than the 'OH radical as indicated by their relatively long half-lives. As an example, the half-life of the carbonate radical is typically longer than 1.7 h in natural waters [154], which is more than enough time to allow for significant transport to the cell surface. Even though these ROS are less reactive than the 'OH radical they are nevertheless still quite reactive (vide supra) and have the potential to react at the surface of the cell, as will be discussed below.

Chemical reactivity is not the only factor to consider in assessing the impact of ROS on microorganisms. For a ROS to affect an organism it should be cell-permeable such that it reacts with and deactivates critical cellular functions. Charged radical species, including the dibromide anion, are unlikely to significantly affect cellular functions because they are not expected to diffuse through the cell membrane. Instead, these charged radicals will possibly react with extracellular surface proteins or carbohydrates, which may represent a chronic stress to microorganisms through inactivation of extracellular surface enzymes or transport proteins. Proteins with a high sulfhydryl content may be particularly susceptible, as the sulfur moieties should be highly reactive with a number of ROS such as the carbonate radical. Inactivation of transport proteins by ROS may partly explain the observed inhibition of amino acid uptake or inorganic nitrogen uptake in marine algae exposed to high UVR [161,162]. It is more likely, however, that these charged radicals will react with the much more abundant carbohydrates, which make up the cell wall or that are exuded by algae and bacteria [163]. Reaction with surface carbohydrates should result in minimal damage to the cell, and perhaps this explains why extracellular carbohydrates are produced in response to oxidative stress.

Hydrogen peroxide is not charged, unlike most of the other ROS, and therefore it will freely permeate through the cell membrane. However, it is not known whether ambient levels of H2O2 exert an acute or chronic stress on aquatic organisms. Studies conducted thus far point to an acute toxicological response of plankton to relatively high concentrations of H202. Barrion and Feuillade [164] found H202 to be an effective algicide in the treatment of the cyanobacteria Oscillatoria rubescens in lake water, but only at 10~3 M concentrations which are much greater than ambient concentrations. In contrast, relatively little inhibition in bacterial growth rates was observed when bacterioplankton were exposed to 10~9 to 10~6 M concentrations of H202 in humic-rich lake waters [137]. In a similar study, Mopper et al. [138] found that much higher concentrations of

H202 (2-3 x 10~6 M) were necessary to inhibit bacterial production in humicrich lake water. Indirect evidence for the negative biological impact of H202 has been provided by Hessen and VanDonk [165]. They demonstrated that, when water samples with high humic content were irradiated with an artificial UVR source and subsequently inoculated with a green algal culture, growth rates were inhibited in UVR-exposed samples compared to the dark controls. The authors attributed the reduction in growth rate to the photochemical production of long-lived products such as H202 in UVR-exposed samples.

The accumulation of H202 at the surface of lakes during periods of near surface water heating may adversely affect aquatic organisms. Recent studies revealed adverse effects of solar radiation on the near surface phytoplankton communities in stratified humic lakes [166,167], Although the negative impact may be attributed to the direct effects of UVR, the high concentrations of H202 at the surface caused by both stratification and high UVR absorbance may have also adversely influenced the phytoplankton. The evidence provided so far is inconclusive and points to a need for further research to study the chronic effects of ambient levels of H202 on plankton communities in lakes and marine systems. It is expected that the oxidative stress imposed by H202 is not due to its direct reaction with cellular constituents, but rather is the result of the production of the highly toxic 'OH radical inside the cell through the Fenton reaction [168],

ROS may also affect microorganisms through the production of toxic trace metal species. For example, the photolysis of organic Cu-complexes and interactions with 02~ may increase the Cu bioavailability and hence Cu toxicity to phytoplankton. This interaction with transition metals is likely to be one of the main processes through which photochemically produced 02-, or other charged ROS, can have an adverse affect on aquatic biota; but further studies are needed to ascertain the ecological impact of these types of reactions in natural waters.

8.5 Conclusions

ROS are ubiquitous in sunlit surface waters, and they are expected to play a pivotal role in the photooxidation of DOM. However, most of what we know regarding the fate of ROS is from chemical intuition or conjecture, based on related laboratory reactions reported in the literature. For example, the overall importance of ROS in intra-humic transformations is virtually unknown, but we expect that these transformations will be important in natural waters, based on photochemical studies with hydrophobic compounds that strongly bind to DOM [55,56].

Since ROS are formed from the absorption of UVR by DOM and its subsequent photochemical decay, any changes in the atmosphere such as tropospheric warming or stratospheric ozone depletion should affect steady state concentrations of ROS in the water column. Initial studies with H202 suggest that the formation of an ozone hole will increase production rates by 20-50%. Changes in atmospheric ozone levels are also expected to affect production rates of other

ROS, especially those species whose action spectra are largely confined to the UV-B (e.g., the 'OH radical [47]), but few systematic studies have been conducted to evaluate these changes.

Since many aspects of reactive oxygen chemistry are still poorly understood, it is suggested that future research should: (1) identify any significant interactions between ROS and DOM, particularly in the high molecular weight fraction; (2) determine the fate of the less reactive radicals, the dibromide radical, the carbonate radical, and alkoxy and peroxy radicals; (3) assess the impact of ROS on the health and growth of aquatic organisms as well as on ecosystem dynamics; and (4) develop models to predict the likely effect of climate change on the production and loss of ROS in the photic zone.

Acknowledgements

The authors gratefully acknowledge the National Science Foundation (OCE-0096413 and OPP-9610173, DJK) for their support of this work, Dr C. Osborn for discussions pertaining to this manuscript and G.R. Westby, Jr. for assisting with manuscript preparation.

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