Oceanography and Marine Biology: An Annual Review (Volume 42) - Chapter 2 pot

In marine biogeochemistry, interest in the distribution of DMSO focuses around the idea thatDMSO could be a key compound in the marine biogeochemical cycle of DMS, which is considered to

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Oceanography and Marine Biology: An Annual Review 2004 42, 29–56

THE ROLE OF DIMETHYLSULPHOXIDE IN THE MARINE BIOGEOCHEMICAL CYCLE OF DIMETHYLSULPHIDEANGELA D HATTON,1* LOUISE DARROCH2 & GILL MALIN2

Oban, Argyll, PA37 1QA, U.K.

Norwich, NR4 7TJ, U.K.

*E-mail: Angela.Hatton@sams.ac.uk

Abstract Dimethylsulphoxide ((CH3)2SO; DMSO) occurs naturally in marine and freshwaterenvironments, rainwater, and the atmosphere It is thought to be an environmentally significantcompound due to the potential role it plays in the biogeochemical cycle of the climatically activetrace gas, dimethylsulphide (DMS) Generally it has been assumed that the photochemical andbacterial oxidations of DMS to DMSO represent major sources of this compound and significant sinksfor DMS in the marine environment Conversely, it has also been suggested that DMSO may be apotential source for oceanic DMS Recent research has improved understanding of the origin and fate

of DMSO in sea water, although it seems likely that the full role this compound may play in themarine sulphur cycle has still to be elucidated The methods available for determining DMSO inaqueous samples and current knowledge of the distribution of DMSO in marine waters are reviewed.Mechanisms for DMSO production and loss pathways are also considered, as well as the possiblerole this compound may play in the cycling of DMS and global climate

dini-is widely used in cell biology and dini-is well known as a cryoprotectant for the preservation of livingcells and tissues (Yu & Quinn 1994) DMSO has also been widely used for diverse medicalapplications Pharmaceutical interest is mainly due to its analgesic and anti-inflammatory properties(Evans et al 1993, Shimoda et al 1996) and its ability to deliver drugs through the skin (Anigbogu

et al 1995) There is also some evidence that DMSO may reduce the development of cancer because

of its free-radical scavenging properties (Bertelli et al 1993, Diamond et al 1997), and it has beensuggested that DMSO has an antibacterial action, may act as a sedative (David 1972) and can bothreduce the infectivity of HIV in vitro and bring about the systematic improvement in advancedAIDS patients (Aranda-Anzaldo et al 1992)

DMSO occurs naturally in a wide range of beverages and foodstuffs, including fruits, vegetables,wine, and beer (Pearson et al 1981, de Mora et al 1993, Yang & Schwarz 1998) In addition, ithas been detected in freshwater lakes and streams (Andreae 1980a, Richards et al 1994), Antarctic

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30 A Hatton, L Darroch & G Malin

glacial meltwater ponds (de Mora et al 1996), Arctic coastal sea ice (Lee et al 2001), sea water(Gibson et al 1990, Kiene & Gerard 1994, Simó et al 1995, 1997, 1998b, 2000, Lee & de Mora

1996, Hatton et al 1996, 1998, 1999, Lee et al 1999a, Bouillon et al 2002), rainwater (Harvey &Lang 1986, Ridgeway et al 1992, Hatton 1995, Lee et al 2001) and the atmosphere (Berresheim et

al 1993, Sciare & Mihalopoulos 2000)

In marine biogeochemistry, interest in the distribution of DMSO focuses around the idea thatDMSO could be a key compound in the marine biogeochemical cycle of DMS, which is considered

to be one of the most important biogenic sulphur compounds in the marine environment It hasbeen suggested that DMS could be both chemically and biologically oxidised within the marineenvironment, leading to the formation of DMSO, and as such, DMSO is expected to play an importantrole in DMS biogeochemistry However, until recently the few available measurements for DMSO

in sea water were thought to be unreliable due to analytical difficulties (Hatton et al 1994b) Thedevelopment of a new sensitive technique (Hatton et al 1994b) and the refinement of previouslyestablished methods (Kiene & Gerard 1994, Simó et al 1996, 1998b) have now shown that DMSO

is present in sea water at concentrations equal to or higher than DMS (Hatton et al 1996, 1999,Simó et al 2000) Additional progress has been made regarding the origin and fate of this compound,although its role in the marine sulphur cycle has still to be fully established In this paper the globalimportance of DMS, its marine biogenic origin and the potential role DMSO may play in thebiogeochemical cycle of this important trace gas are briefly discussed

The global significance of DMS

All models for the biogeochemical cycle of sulphur require volatile or gaseous compounds toprovide a vehicle for the transfer of sulphur from the sea to land surfaces In past considerations

of the marine sulphur cycle it was the inorganic sulphur compounds that received the most attention.Consequently, the oxidation–reduction circuit between sulphate and sulphide, with hydrogen sul-phide as the gaseous link, was for a long time considered to explain most of the biologically drivenflow of sulphur in the natural environment (Kelly & Baker 1990) In 1972, however, Lovelock et

al published evidence for the ubiquity of DMS in surface sea water and proposed that marine DMSwas the natural sulphur compound filling the role originally assigned to H2S At that time it wasalready known that many living systems, including marine algae, produced DMS, and biochemicaldata were available that suggested that dimethylsulphoniopropionate (DMSP) might be the precur-sor of DMS in marine ecosystems (Challenger 1951, Cantoni & Anderson 1956, Tocher & Ackman

1966, Ishida 1968, Kadota & Ishida 1968) It is now well established that DMS is the major volatilesulphur species in the oceans and this fact, along with the suggestion that DMS may play animportant role in climate and atmospheric chemistry (Charlson et al 1987, Andreae 1990, Bates

et al 1992), has led to a great deal of research focusing on this compound Since the early 1980s,DMS measurements have been made throughout the Pacific, Atlantic, Arctic, Indian, and SouthernOceans (see Kettle et al 1999 and references therein) These studies have shown that DMS isnormally restricted to the upper 200 m of the water column, with higher concentrations found oncontinental shelves and in high productivity regions

Relative to concentrations of DMS in the atmosphere, the surface oceans have been shown to

be typically two orders of magnitude supersaturated, implying a net flux of the gas from the oceans

to the atmosphere (Liss & Slater 1974, Andreae 1986, Liss et al 1993) In the atmosphere, therapid oxidation of DMS leads to the production of sulphur dioxide (SO2), sulphate, and methanesulfonate (MSA), with sulphate and MSA present in the atmosphere predominantly in the form ofaerosol particles These aerosols may be deposited in rain and snow, thereby contributing to theacidity of natural precipitation (Plane 1989), and may act as cloud condensation nuclei (CCN) overthe remote oceans (Charlson et al 1987) During the 1980s concern over acid rain increased interest

in the relative strengths of the various sources of sulphur to the atmosphere (Bates & Cline 1985).Due to this concern, many studies were conducted to calculate the sea–air fluxes of DMS and other

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The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide 31

sulphur gases, such as carbonyl sulphide, carbon disulphide, and dimethyl disulphide (e.g., Barnard

et al 1982, Andreae & Raemdonck 1983, Andreae et al 1983, 1994, Andreae & Barnard 1984,Bates et al 1987, Erickson et al 1990, Malin et al 1993)

Fluxes are generally calculated from field measurements of DMS in sea water and estimates

of the transfer velocity, the term that quantifies the rate of transfer Gases are transferred acrossthe air–sea interface by a combination of molecular and turbulent diffusion processes, which areinfluenced by wind speed, boundary layer stability, surfactants, and bubbles (Liss & Merlivat 1986,Wanninkhof 1992, Nightingale et al 2000) Current understanding of the processes controlling theair–sea exchange of trace gases is covered in the recent monograph by Donelan et al (2002), andspecific discussions on DMS emissions can be found in Malin (1996) and Turner et al (1996) Tosummarise, the sea-to-air flux of DMS is currently estimated to be of the order of 15–33 Tg ofsulphur yr–1 (Kettle et al 1999).This flux accounts for a large fraction of total biogenic sulphuremissions (15–50 Tg sulphur yr–1, Chin & Jacob 1996), such that DMS makes a major contribution

to the atmospheric sulphur pool, and hence the chemistry and radiative properties of the atmosphere(Simó 2001)

DMS and its biogenic origins in sea water

DMS is formed mainly from the enzymatic breakdown of DMSP, a compatible solute produced bymarine algae to maintain their osmotic balance in sea water (Vairavamurthy et al. 1985, Dacey &Wakeham 1986) However, it has also been suggested that marine phytoplankton may produceDMSP as a cryoprotectant (Kirst et al 1991, Lee & de Mora 1999), an antioxidant (Sunda et al.2002), a methyl donor for a variety of biochemical processes (Cantoni & Anderson 1956, Ishida

1968, Kiene 1996), or a grazing deterrent (Wolfe et al 1997, 2002) Furthermore, it has beenhypothesised that DMSP may be produced as an overflow mechanism enabling cells to keep cysteineand methionine concentrations at a level that is low enough to prevent feedback mechanisms andallow continued sulphate assimilation even under nitrogen-limited conditions (Stefels 2000) In theearly 1980s Barnard et al. (1982) and Bates & Cline (1985) noted that the distribution of DMSand DMSP only correlated in a rather general way with phytoplankton biomass, leading them tosuggest that only certain groups of phytoplankton may produce significant amounts of DMSP.Subsequently, it was shown that some taxonomic groups, such as dinoflagellates and prymnesio-phytes, can contain high DMSP concentrations per unit cell volume, while diatoms have variablebut generally low concentrations (Keller et al. 1989)

DMS production and removal processes

The production of DMS from intracellular DMSP by healthy, growing cells was generally thought

to be relatively insignificant (Turner et al 1988, Keller et al 1989) Experimental evidence suggeststhat DMSP must first be released into the surrounding sea water by zooplankton grazing (Dacey

& Wakeham 1986, Leck et al. 1990, Malin et al. 1994, Wolfe et al. 1994), viral lysis (Hill et al.

1998, Malin et al. 1998), and natural senescence (Turner et al. 1988, Leck et al. 1990), where itwould then be available to marine bacteria that could break down the DMSP producing DMS.Although this may be the case for many species of phytoplankton, it is now thought that someDMSP may also be cleaved within the algal cell, resulting in the direct excretion of DMS (Wolfe

et al 2002) In both cases this initial breakdown of DMSP yields DMS, acrylate, and a proton in

a 1:1:1 ratio This process is catalysed by DMSP lyase enzymes, which can be found in certainphytoplankton and bacteria (Ledyard & Dacey 1994, Stefels et al 1996, Wolfe & Steinke 1996).Once in sea water DMS can be removed via a number of different pathways, includingventilation to the atmosphere (Bates et al 1987, Erickson et al 1990), consumption by the biota(Kiene & Bates 1990, Kiene 1992, Wolfe & Kiene 1993, Ledyard & Dacey 1996), or photochemical

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removal (Brimblecombe & Shooter 1986, Kieber et al 1996, Brugger et al 1998) Current evidencesuggests that the quantity of DMS emitted to the atmosphere is only a small proportion of thepotential marine pool (Malin et al 1992) Indeed, a recent estimate of the total DMS flux to theatmosphere, during a coccolithophore bloom, showed it to be equivalent to just 1.3% of the grossDMSP production and 10% of the DMS production in the surface layer (Archer et al 2002).Bacterial consumption of dissolved DMSP (DMSPd) and DMS is a major factor influencing thequantity of DMS available for transfer to the atmosphere The pathways involved in DMSP degradation

by aerobic microorganisms and their relative importance have been discussed in a number of reviewsand so will only be briefly covered here (Taylor 1993, Taylor & Visscher 1996, Kiene et al 2000).Recent studies reveal that DMSP-utilising bacteria are highly active in the field (Kiene et al.2000) It has been shown that DMSPd can undergo bacterially mediated degradation, not only viathe lyase pathway to form DMS, but also via demethylation pathways yielding either 3-methiol-propionate (MMPA), which is then demethiolated producing methanethiol (MeSH), or 3-mercap-topropionate (MPA), which leads to the formation of H2S (Taylor 1993, Kiene et al 2000).Several studies show that DMS is a relatively minor product of DMSPd metabolism under mostcircumstances in the water column (Ledyard & Dacey 1996, Van Duyl et al 1998), and currentfindings favour the demethylation/demethiolation pathway as being the major fate for DMSP insea water (Kiene et al 2000), accounting for 75% of the DMSP bacterial transformations (Kiene

& Linn 2000) Although the demethylation/demethiolation pathway is thought to be the majorremoval pathway for DMSP, a recent laboratory study investigated DMSP metabolism in 15culturable bacteria of a lineage common in sea water and found that they all expressed the lyasepathway, whereas only five also expressed the demethylation pathway (Gonzàlez et al 1999).Following DMSPd demethylation, MeSH is incorporated into the proteins of bacterioplankton

or other nonvolatile products Studies using 35S tracers showed that DMSP may be rapidly taken

up into bacteria, where it remains over many hours, with a significant fraction of the tracer beingshown to be assimilated into protein sulphur, primarily in the form of methionine (Kiene et al.2000) Furthermore, it is also thought that marine bacteria may opportunistically take up DMSP

to use as a compatible solute (Kiene et al 2000) It has also been shown that marine bacteria canutilise up to 100% of the available DMS, which, in addition to being incorporated into cell biomass,has the potential for transformation to other sulphur compounds such as DMSO (Kiene & Linn

2000, Zubkov et al 2002)

The CLAW hypothesis

In 1987 Charlson et al put forward the CLAW hypothesis (after the initials of the authors), thecontroversial hypothesis that the emissions of DMS may be linked with climate regulation Theidea was that increased seawater temperature leads to increased DMS emissions, followed byatmospheric oxidation, production of CCN, and increased cloud albedo, which would serve tocounteract the initial temperature increase Thus the rate of DMS release may influence cloudformation over the oceans, which in turn affects the global heat balance, thereby giving the biota

a modicum of “control” over the climate (Charlson et al 1987) Central to this hypothesis was theassumption that DMS emissions from sea water are directly controlled by temperature However,Malin et al (1994) stated that because DMS emissions result from a network of production,transformation, and consumption processes, temperature could be effective at several levels There

is now little doubt that DMS is a precursor for aerosol sulphate, or that sulphate-containing aerosolsare effective CCN (Schwartz 1988), and there is also persuasive theoretical evidence that theseCCN may affect cloud albedo (Charlson et al 1987, Idso 1992) Coherence between CCN con-centration and cloudiness has been documented using satellite data, strongly suggesting that DMSemissions can influence cloud radiative transfer properties (Boers et al 1994) However, the negativefeedback loop of the phytoplankton, DMS, and climate regulation hypothesis (Charlson et al 1987)remains somewhat controversial

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Dimethylsulphoxide in sea water

Analysis of DMSO in sea water

It was always assumed that DMSO would be present in sea water and would play a role in theDMS cycle However, this stable and soluble compound originally proved difficult to analyse atthe nanomolar concentration range anticipated in marine aquatic environments DMSO analysis

is problematic because DMSO is readily soluble in water, nonionic, and cannot be purged orsteam distilled (Harvey & Lang 1986) The various methods originally reported for DMSOanalysis in aqueous samples were based around direct measurement, which was insufficientlysensitive for nanomolar concentration ranges (Paulin et al 1966, Wong et al 1971, Ogata &Fujii 1979) or chemical reduction of DMSO to DMS (Andreae 1980a), which was prone tocontamination problems (Simó et al 1998b)

Subsequently, Harvey & Lang (1986) developed a sensitive direct method for the determination

of DMSO and DMSO2 in rainwater and marine air masses This method involved preconcentrating thesulphur compounds on a silica or Tenax GC column, with subsequent extraction of the compoundsinto methanol followed by gas chromatography Berresheim et al (1993) also developed a sensitivedirect method for the detection of DMSO in ambient air that is based on atmospheric pressure chemicalionization/mass spectrometry (APCI/MS) However, neither of these techniques was suitable for usewith saline solutions, and therefore could not be used for marine samples One direct method for DMSOanalysis has been demonstrated, which is suitable for use with seawater samples In this case thesamples were injected directly into a gas chromatograph, with increased detector sensitivity, due to theaddition of sulphur hexafluoride, giving a detection limit equivalent to 0.06 nmol dm–3 (Lee & de Mora1996) However, other research groups have not adopted this method

Chemical reduction of DMSO to DMS and the subsequent analysis of DMS have greater sensitivityand are suitable for saline solutions, but most existing methods are subject to some interferences Thesample preparation technique reported by Andreae (1980b) involved the addition of sodium borohydride(NaBH4) or chromium II chloride (Cr2Cl) to bring about this reduction However, the DMS yield by

Cr2Cl was only 42% of the expected level and the accuracy of the NaBH4 method was compromised

by the assumption that all DMS produced originated from DMSO, even though it had been shown thatNaBH4 can also initiate the conversion of DMSP to DMS and acrylic acid (Challenger & Simpson

1948, Simó et al 1998b) Ridgeway et al (1992) developed a novel isotope dilution method formeasuring DMS and DMSO in sea water, but this method also necessitates the breakdown of DMSOwith NaBH4 and the use of a mass spectrometer Chemical reduction using acidified stannous chloride

to reduce DMSO to DMS has also been used, but again, this requires prior removal of DMSP by alkalihydrolysis or correction for the measured DMSP concentrations (Anness 1981, Gibson et al 1990,Kiene & Gerard 1994)

During the past 10 yr, much work has been conducted to refine these chemical reductionmethods (Kiene & Gerard 1994, Simó et al. 1996, 1998a) These refined methods along with thedevelopment of a highly specific and sensitive enzyme-linked technique (Hatton et al. 1994b) haveallowed the measurement of DMSO in a variety of environments and an increased understanding

of the distribution of DMSO in both fresh- and marine waters In addition, recent suggestions thatphytoplankton may produce DMSO directly (Simó et al 1998a) have led to the development ofseveral methods to measure nanomolar concentrations of DMSO in particulate matter (DMSOp).These methods are based on the extraction of cellular DMSO into ethanol (Lee et al 1999a), orthe disruption of cells by applying osmotic pressure or via the use of cold alkali hydrolysis (Simó

et al 1998a,b) In all cases the resulting DMS was subsequently analysed using established gaschromatography methods

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Distribution of DMSO in sea water

A compilation of DMSO surface concentration data values from studies examining DMSO bution in marine waters is presented in Table 1 Figure 1 shows concentration values superimposedonto a world map and indicates that the current data set is rather sparse compared with similarcompilations of DMS data (Kettle et al 1999) In surface waters the concentration of DMSO isgenerally equal to or slightly higher than that of DMS (Hatton et al 1996, 1999) Figure 2 showsthe concentrations of DMS and DMSO found in surface waters, from four data sets collected by theauthors Seawater samples were collected from a wide range of geographical locations (Arabian Sea,Antarctic, North Sea, and northeast Atlantic), including both coastal and open-ocean sites Fromthese results it is clear that the distribution of DMSO in surface waters closely follows that of DMS.The data show a positive correlation between DMS and DMSO (r2 = 8005, p < 001) for the wholedata set (Figure 3), suggesting that a similar relationship exists between the two compounds atdifferent locations However, it should also be noted that some studies have found DMSO levelsthat are one to two orders of magnitude greater than those of DMS (Andreae 1980a, Lee & de Mora1996) In addition, studies during Phaeocystis pouchetii blooms in Antarctica (Gibson et al 1990)and in the Saguenay Fjord, Québec (Lee et al 1999a) found that DMSO levels were lower thanthose of related dimethylated sulphur compounds In both cases, it was concluded that poor lightpenetration limited the photochemical oxidation of DMS and prevented the accumulation of DMSO

distri-Table 1 DMSO concentration ranges in the marine environment

Location

DMSO concentration

a Not corrected for DMSP interference.

b Sample taken from sea ice.

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The Role of Dimeth

Figure 1 Location and levels of DMSO in surface waters collated from published data (see Table 1) Note: Where more than one concentration was detected at the

same geographical location, highest values are plotted

DMSO

(nmol dm- 3 )

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Figure 2 Near-surface concentrations for DMS ( ) and DMSO ( ) collected during two oceanographic cruises to (A) the North Sea (from 52˚ 46N, 01˚ 50E to 54˚ 03N, 02˚ 10E to 52˚ 51N, 03˚ 07E, April 1994) and (B) the Arabian Sea (from 19˚ 30N, 58˚ 09E to 16˚ 02N, 62˚ 00E, August 20, and September 1994), and from two shore-based sites in (C) the Antarctic (at 67˚ 34S, 68˚ 15W, between January and February 1999) and (D) Scottish coastal waters (at 56˚ 31N, 05˚ 33W, between September 1998 and August 1999) (Sections

A and B adapted from Hatton et al 1996 and published with permission of Plenum Press.)

A

0 2 4 6 8 10 12 14 16 18 20

0 5 10 15 20 25 30 35 40

Date

3 ) D

0 2 4 6 8 10 12

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The strong correlation between DMS and DMSO only appears to hold for surface waters andresults from depth profiles show a different story DMSO has been shown to be ubiquitous through-out the water column, having been detected in the deep oceans (Ridgeway et al.1992, Hatton et

al 1998, 1999), whereas DMS and DMSP are usually restricted to the euphotic zone DMSO hasbeen reported at concentrations greater than 1.5 nmol dm–3 at depths up to 1500 and 4000 m inthe equatorial Pacific Ocean and Arabian Sea, respectively (Hatton et al 1998, 1999) As aconsequence, when the whole water column is taken into account, depth-integrated DMSO levelsare significantly higher than those for DMSP Hence DMSO can be the dominant DMS-relatedsulphur species throughout the water column, especially in eutrophic regions (Hatton et al 1998).Seasonal variations in DMSO concentrations have also been found At a coastal site in NewZealand, DMSO levels were shown to be lowest during winter (Lee & de Mora 1996) In addition

to reduced phytoplankton biomass and lower bacterial activity at that time of year, it was statedthat reduced daylight hours would further decrease the photooxidation of DMS to DMSO Recently

an in-depth seasonal study of both dissolved and particulate DMSO was conducted in coastal watersand sea lochs on the west of Scotland Results showed a strong seasonal cycle in the production

of DMSO with concentrations of DMSOp up to 20 nmol dm–3 during spring and summer, andlevels below the analytical detection limit of 0.3 nmol dm–3 during winter (Hatton & Lyall, inpreparation) Increased levels of DMSOp coincided with increases in DMSOd, DMS, and chloro-phyll a, and it was concluded that DMSO production was linked with phytoplankton biomass.During spring the levels of DMSPd and DMSPp appeared to increase after the initial increase inDMSOp, indicating that the DMSOp may have been produced either by a different species or at adifferent point of the life cycle of the phytoplankton present

Using recently developed methods, DMSOp levels have now also been reported in a number

of other studies Simó et al (1998a) reported DMSOp levels ranging from 2.7–16 nmol dm–3 forsamples from the North Sea Lee et al (1999a) observed concentrations ranging from 0–110 nmol

dm–3 in the Saguenay Fjord, Québec, while Bouillon et al (2002) found concentrations between

0 and 16.9 nmol dm–3 in seawater samples from Baffin Bay in the Arctic In addition, it has beenshown that the majority of this DMSOp is found in the microplankton-size fraction of seawatersamples (Simó et al 1998a) In common with DMSOd, DMSOp has been detected at depths of

>100 m (Bouillon et al 2002), but depth profile data also show that, in parallel with DMSPp,DMSPd, and DMS, the highest concentrations of DMSOp tend to occur in the upper water column

Figure 3 Correlation between DMS and DMSO for data sets in the North Sea, Arabian Sea, Antarctic, and west coast of Scotland, as shown in Figure 2 The regression of DMSO concentration on DMS (y = 1.5184x + 0.96) is highly significant (r 2 = 0.8005, p < 0.001) Note: Data for the west coast of Scotland also include results from three alternate sample sites in addition to the one shown in Figure 2.

0 5

5

10 15 20 25 30 35 40

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(Bouillon et al 2002) DMSOp has also been measured in the sea ice algal communities of BaffinBay where levels ranged from 1.35–102 nmol dm–3 and were higher than those found in the watercolumn This difference in concentration was presumably because of the higher biomass of planktonfound in ice samples (Bouillon et al 2002)

DMSO and its influence on DMS biogeochemistry

In the past it has been proposed that DMSO may act as a sink or source for DMS It was generallythought that DMSO would be formed mainly from the photochemical (Brimblecombe & Shooter1986) or bacterial (Zeyer et al 1987) oxidation of DMS The formation of DMSO would thereforelead to the removal of DMS from sea water, effectively limiting the quantity of DMS available fortransfer to the atmosphere In addition, it was proposed that since DMSO concentrations aregenerally higher than those of DMS, and since some bacteria had been shown to be capable ofreducing DMSO to DMS (Zinder & Brock 1978), DMSO could also represent an important sourcefor DMS Although the interactions occurring between these two compounds may prove to be keyprocesses in DMS biogeochemistry (Lee et al 1999b), a great deal of research is still required ifthe relative significance of these pathways and the factors influencing them are to be fully under-stood The next two sections discuss the current understanding of the ways in which DMSO mayact as either a sink or a source for DMS in the marine environment

DMSO as a sink for DMS in the marine environment

The photochemical oxidation of DMS to form DMSO

DMS may be removed from the water column via chemical and photochemical oxidation to DMSO.One potential chemical oxidant in sea water is hydrogen peroxide (Zika et al 1985), becauseoxidation of DMS in the presence of hydrogen peroxide is much faster than oxidation by molecularoxygen (Shooter & Brimblecombe 1989) It has also been demonstrated that hydrogen peroxidecan be produced by marine phytoplankton (Palenik et al 1987), making it easily available for DMSoxidation However, the loss of DMS via photo-oxidation to DMSO in sea water is likely to be amore significant reaction The photochemical oxidation of DMS to DMSO was first implied byBrimblecombe & Shooter (1986), who estimated the global quantity of DMS photo-oxidised wouldamount to 6.4 Tg(S) yr–1 During laboratory experiments with aqueous solutions, they observedthat DMS could be rapidly destroyed by intense UV radiation, with no significant DMS photolysis

at visible wavelengths This finding was in line with previous work that had shown that DMS doesnot appreciably absorb light of wavelengths of >260 nm (McDiarmid 1974) However, Brimble-combe & Shooter (1986) went on to demonstrate that in the presence of photosensitisers, such asanthroquinone and humic acid, DMS is also susceptible to photolysis by visible light Theyconcluded that the photolysis of DMS in the presence of photosensitisers followed pseudo-first-order reaction kinetics, would lead to the formation of DMSO, and would proceed via the formation

of singlet oxygen In other words, the photosensitiser absorbs light and reacts with dissolvedmolecular oxygen to form singlet oxygen, which then reacts with the substrate However, it isimportant to point out that DMSO was never directly measured in their study, and the completeoxidation of DMS to DMSO was inferred from the observed loss of two molecules of DMS foreach molecule of oxygen

In 1996, Kieber et al also showed that DMS photolysis could be mediated by wavelengths inthe UVB range (280–315 nm) However, they concluded that in natural waters DMS photolysiswould be primarily mediated by PAR (photosynthetically active radiation or wavelengths from380–460 nm) In addition, their experiments demonstrated that DMSO was only a minor product

of DMS photolysis, accounting for 14% of all the DMS photolysed In a recent study, Hatton(2002a) also suggested that DMS photolysis may be mediated by both UVB (<315 nm) and

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UVA/visible wavelengths (>315 nm) in the northern North Sea It was concluded that under visiblewavelengths of light most of the photochemically removed DMS will be photo-oxidised to DMSO,with up to 99% of the DMS being oxidised to DMSO in the presence of 0.90 mg of C dm–3 ofdissolved organic carbon (DOC), whereas at wavelengths of <315 nm (UVB) a second DMSphotolysis pathway operates that does not yield DMSO The additional loss of DMS due to UVBradiation meant that the oxidation of DMS to DMSO accounted for only 37% of the total DMSlost under full natural light conditions (Hatton 2002a)

These results clearly indicate that UVB radiation may play a major role in the removal of DMSfrom surface waters Often the potential importance of UV radiation has been neglected due toearly reports that UV penetration was limited to the very top layers of the water column, even inthe open ocean However, with more sensitive instruments it has now been demonstrated that UVradiation can penetrate to depths of >20 m (Fleischmann 1989, Kaiser & Herndl 1997) Furthermore,

it has been determined that photolysis rates are highest close to the surface and sharply declinewith depth This decline with depth was confirmed by Brugger et al (1998), who found that 88%

of the DMS was photolysed in the top 10 m of the water column, which was within the 1% lightlevels for UVB in Adriatic coastal waters

These results have important consequences for the understanding of the photochemical cesses affecting the level of DMS in surface water It has been suggested that DMSO couldpotentially be reduced back to DMS (Suylen et al 1986, Weiner et al 1992) Therefore, any DMSremoved via its photooxidation to DMSO may be recycled and, as such, represents a future source

pro-of oceanic DMS, whereas the photolysis pro-of DMS by UVB radiation may result in its total removalfrom the water column

The formation of DMSO may also be affected by geographic location Higher DMS photolysisrate constants of 0.12 h–1 and 0.09–0.14 h–1 have been measured at coastal sites in the Adriatic Seaand North Sea, respectively (Brimblecombe & Shooter 1986, Brugger et al 1998), compared withincubations in the open-ocean Pacific, where much lower rate constants of 0.04 h–1 were found(Kieber et al 1996) It was suggested that these differences between coastal and open ocean could

be accounted for by the proportion of photosensitiser compounds present These compounds, such

as humic substances, have been shown to be a significant proportion of coastal seawater DOC (Lara

et al 1993) as opposed to open-ocean waters Furthermore, both bacteria and algae have beenshown to produce photosensitised compounds that can actively photooxidise DMS to DMSO (Fuse

et al 1997, 2000), and the occurrence of these processes may be more common in productiveregions

DOC may also affect the photolysis of DMS and the photoformation of DMSO throughout thewater column Using DOC concentrations, DMS photolysis rate constants determined at the surface,and a diffuse attenuation coefficient calculated for the wavelength range 380–460 nm, it was foundthat DMS photolysis continued to different depths in oligotrophic compared with coastal environ-ments (Brugger et al 1998) It was predicted that DMS photolysis was still a significant processdown to 60 m in the water column of the oligotrophic equatorial Pacific Ocean Conversely, inmore productive coastal areas, the photolysis of DMS was most significant in the top 10–20 m,before rates sharply declined with depth (Brugger et al 1998) This decline was not surprisingbecause high concentrations of DOC, such as those found in coastal areas, would prevent thepenetration of light at depth However, although there appear to be differences in the maximumdepth at which DMS photolysis occurred, these differences were not reflected in the final depth-integrated turnover rates calculated for more productive coastal waters and open-ocean waters,which ranged from 0.1–0.3 d–1 and 0.11–0.37 d–1, respectively Brugger et al (1998) suggested thatthis similarity in depth-integrated turnover rate may be due to a lower photolytic activity in theopen ocean, being compensated by a lower light attenuation In other words, it seems likely thathigh DOC concentration will affect photochemical processes in the marine environment by bothincreasing the initial photolysis rates in surface waters and reducing the quantity and quality of theirradiance penetration through the water column Furthermore, it should be noted that it has been

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shown that DMS photolysis (and thus DMSO production) may be affected not only by the quantitybut also by the quality of DOC present in sea water (Brugger et al 1998)

Several studies now indicate that losses of DMS due to photolysis are comparable with thosedue to bacterial consumption and atmospheric ventilation of DMS (Kieber et al 1996, Hatton2002b), demonstrating the potential importance of this pathway in the marine sulphur cycle.However, there is still some conflicting evidence concerning the mechanisms involved, the impor-tance of wavelength and the role of DOC in this pathway A fuller understanding of this pathway

is particularly important because the relative proportions of DMS photo-oxidised to DMSO andDMS photolysed without DMSO production may have significant implications for DMS bio-geochemistry

DMS photo-oxidation in the atmosphere

The photochemical oxidation of DMS to DMSO also occurs in the marine atmosphere (Barnes et

al 1987, Berresheim et al 1993, Koga & Tanaka 1993) Due to its low volatility and hygroscopicnature, DMSO would be scavenged from the air by rain (Lovelock et al 1972) and returned to theoceans in precipitation A few studies have reported DMSO in rainwater with concentrations rangingfrom 1–369 nmol dm–3 (Ridgeway et al 1992, Kiene & Gerard 1994, Hatton 1995, Sciare et al.1998) During a continuous study of rainwater DMSO at Amsterdam Island in the southern IndianOcean, a distinct seasonal cycle in the wet deposition of DMSO was found, with an average summermaximum and winter minimum of 90 and 25.6 nmol dm–3, respectively (Sciare et al 1998) Theseasonal cycle was found to be in line with variations observed for atmospheric DMS However,the authors hypothesised that the wet deposition of DMSO may not be important in the sulphurcycle because the annual average deposition rate of DMSO was 0.12 mmol m–2 d–1, which accountedfor only 3% of the annual average DMS flux from the same area

Bacterial oxidation of DMS leading to the formation of DMSO

In addition to the chemical and photochemical processes, it has been suggested that the formation

of DMSO from DMS may be enzymatically catalysed by bacteria (Taylor & Kiene 1989) organisms use sulphur compounds not only for assimilatory purposes, but also in biochemicalprocesses where they may act as electron donors or electron acceptors In the past a number ofculture studies were conducted that demonstrated that some phototrophic bacteria are capable ofoxidising DMS to DMSO, but most of the organisms studied at that time were obligate anaerobes(Zeyer et al 1987, Visscher & van Gemerden 1991, Hansen et al 1993) Zeyer et al (1987) showedthat enrichment cultures of phototrophic purple bacteria, including a pure strain of a marine

seven pure bacterial cultures that could utilise DMS as an electron donor for CO2 fixation, withDMSO as the only product Visscher & van Gemerden (1991) examined the purple sulphur bacte-rium Thiocapsa roseopersicina for photoautotrophic growth on DMS They demonstrated that thisbacterium was able to metabolise DMS in the light, and oxidised it stoichiometrically to DMSO.All these bacteria were shown to be able to utilise DMS as an electron donor for CO2 fixation,with DMSO as the only product In addition, Zhang et al (1991) isolated a strain of Pseudomonas

could not grow under chemoautotrophic conditions, presumably because it is unable to fix CO2.Furthermore, Hanlon et al (1994) isolated a strain of Rhodobacter sulfidophilus, which grewautotrophically with DMS serving as an electron donor in photosynthesis and respiration, but not

as a carbon source They identified a periplasmic DMS acceptor oxidoreductase enzyme that wasdistinct from the DMSO reductase found in this bacterium

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Following this research it has been shown that some chemotrophic aerobic marine bacteria are

also able to oxidise DMS to DMSO Aerobic oxidation of DMS has been observed in the marine

nitrifier, Nitrosococcus oceanus, using the enzyme ammonia mono-oxygenase (Juliette et al 1993)

Similarly, strains of Methylomicrobium, a marine methanotroph, have also been shown to aerobically

oxidise DMS to DMSO, where the oxidation was thought to proceed via the enzyme methane

mono-oxygenase (Fuse et al 1998) Recent work has now shown that the most notable marine

bacteria involved in the cycling of organosulphur compounds are probably those members belonging

to the Roseobacter lineage of the a-subclass of Proteobacteria These bacteria are not only able to

degrade DMSP into methanethiol and DMS, but some strains are also able to aerobically oxidise

DMS to DMSO and vice versa (González et al 1999) These bacteria may be fundamental to the

cycling of DMS in sea water because they are abundant in marine environments, especially during

DMSP-producing phytoplankton blooms (González et al 2000, Zubkov et al 2002) Moreover,

their growth has been shown to respond to increased concentrations of DMS and DMSP in

uncultured seawater samples (González et al 1999)

Formation of DMSO within sedimenting particles

The role sedimentation plays in the biogeochemical cycle of DMS is poorly understood It has

been suggested that sinking phytoplankton and faecal pellets from zooplankton may carry DMSP,

and therefore potentially DMS, out of the surface layer However, a number of reports do not

support this hypothesis (Bates et al. 1994, Corn et al. 1994, Daly & DiTullio 1996) Bates et al.

(1994) concluded that DMSP loss from the upper water column via sinking particles was minimal,

amounting to only 0.0023 mmol m–2 d–1 Corn et al (1994) found higher daily DMSPp sedimentation

fluxes of between 1.4 and 5.7 mmol m–2 d–1 However, as this accounted for only about 0.1% of

the DMSPp standing stock, they suggested that the downward flux of DMSPp would be likely to

have only a minor influence on the upper ocean budget of DMSPp Daly & DiTullio (1996) also

concluded that the downward flux of DMSP was low They showed that despite the fact that particle

fluxes were dominated by zooplankton faecal pellets, DMSPp fluxes were <1% of the integrated

DMSPp stock

In contrast, other studies suggest that loss of DMSP from surface waters through its breakdown

in sedimenting faecal pellets is a process that cannot be neglected (Wolfe et al 1994, Daly &

DiTullio 1996, Kwint et al 1996, Hatton 2002b) During experiments conducted to assess if DMSP

could be removed from surface waters through zooplankton grazing, Kwint et al. (1996) showed

that relatively large amounts of the ingested DMSP are packaged into the zooplankton faecal pellets

The amount of DMSP in the faecal pellets appeared to decrease about 30% during the first day;

after 5 days about 70% had disappeared, and after 2 wk only 10% was left Surprisingly, however,

no increase in the DMS or DMSPd concentrations could be detected This finding led them to

conclude that DMSP must be metabolised to other sulphur compounds by bacteria present in the

microaerobic or anaerobic faecal pellets In a laboratory study Wolfe et al. (1994) also found that

during grazing the ciliate Oxyrrhis marina metabolised up to 70% of the DMSP ingested without

DMS production It is also worth noting that recent work has suggested that zooplankton, such as

copepods, may incorporate some of the ingested DMSP into their body tissue (Tang et al 1999,

2000) Therefore, the results from a number of studies lead to the conclusion that DMSP loss

through zooplankton grazing and sedimentation could have been underestimated previously In fact,

Kwint et al (1996) concluded that up to 10% of the DMSP daily production could disappear from

the surface waters via this route

It is now thought that some of the DMSP repackaged into faecal pellets during zooplankton

grazing could be subsequently cleaved to DMS and oxidised to DMSO by anaerobic and

microaero-philic bacteria contained within the pellets (Hatton 2002b) Recent experiments have also shown

that the production of DMSO in sedimenting material can be inhibited by the addition of antibiotics,

demonstrating that this pathway is likely to be bacterially mediated (Hatton, in preparation) These

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experiments show that a bacterial production pathway for DMSO exists in natural samples collectedfrom the pelagic marine environment, although the importance of this process in the marine DMScycle is still conjecture

As previously discussed, DMSO can be detected at much greater depths than DMS and DMSP,

making DMSO the dominant sulphur compound in deep waters (Ridgeway et al 1992, Hatton et

al 1998, 1999) Although these authors suggested that the presence of DMSO in deeper waters

may have been due to either advection or diffusive mixing across the thermocline, coupled to a longresidence time for DMSO, the source of this deepwater DMSO has never been elucidated DMSO isknown to permeate membranes (Liu et al 1997) Therefore, DMSO produced within sedimentingmaterial may simply leach out of sedimenting particles into the surrounding sea water, representing

a source for the DMSO previously observed in deeper waters

Although DMSO may be generated as a result of the bacterial metabolism of DMSP withinsedimenting material, this pathway cannot account for all the DMSP lost from these sites, andtherefore other alternate loss pathways are likely to be involved in the removal of DMSP or DMSfrom the samples Zooplankton faecal pellets have been shown to be colonised by bacteria that canutilise DMSP (Tang et al 2001) It has also been suggested that because faecal pellets containmuch more concentrated DMSP than the surrounding sea water, they may act as hot spots for

microbial DMSP consumption (Tang et al 2001) Other alternative pathways and the dominant

sink for DMSP metabolism involving demethylation/demethiolation have been observed in anoxicsediments (Kiene & Taylor 1988) and in oceanic surface waters (Kiene 1996, Taylor & Gilchrist

1991, Visscher et al 1992, Kiene et al 2000) Therefore, DMS may also be removed from the

sample via non-DMSO-producing pathways Furthermore, it has previously been shown that anogenic bacteria may be present in zooplankton guts and enter the sinking particulate field throughthe formation of faecal pellets (DeAngelis & Lee 1994, Marty 1993, Karl & Tilbrook 1994, Holmes

meth-et al 2000) DMS is a known substrate for mmeth-ethanogenic bacteria (Zinder & Brock 1978, Finster

et al 1992), so it is feasible that any methanogenic bacteria present in faecal material could be

responsible for removal of DMS from these sites, resulting in the loss of total organic sulphur

DMSO as a source for DMS in the marine environment

Algal production of DMSO

The possibility that algae could directly produce DMSO had been considered for many years,following the detection of DMSO in various fruits and vegetables (Pearson et al 1981) and thelarge pool of DMSO observed in sea surface waters (Lee & de Mora 1996) Evidence to supportthe direct biosynthesis of DMSO by marine phytoplankton in sea water was first reported duringdiurnal studies in the coastal waters of North Island, New Zealand Rapid daytime production ofdissolved DMSO appeared to have little effect on the concentrations of DMS during diurnal studies(Lee & de Mora 1996) The authors speculated that the photo- and bacterial oxidation of DMS inthat environment could not have accounted for all of the light-dependent production of DMSO Itwas concluded that algal photosynthetic processes may play a role in the production and release

of DMSO

Subsequent to this study, the production of DMSOp by marine micro algae was observed in

laboratory culture studies of both the dinophyte, Amphidinium carterae, and the haptophyte, iania huxleyi (Simó et al 1998a) Intracellular production of DMSO coincided with logarithmic

Emil-growth, where the average logarithmic cellular content was approximately 0.3 and 0.1 pg of DMSOcell–1, translating to DMSPp:DMSOp ratios of 25 and 8, respectively Coinciding with intracellularproduction, the authors observed high DMSOd production

It has been argued that the ability of marine phytoplankton to synthesise DMSO may be present

in a wider range of species than the ability to synthesise DMSP Lee et al (1999a) found that theratio of these two compounds was not consistent between different stations in the Saguenay Fjord,

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