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

2727_C02.fm Page 29 Wednesday, June 30, 2004 3:37 PM

THE ROLE OF DIMETHYLSULPHOXIDE IN THE MARINE
BIOGEOCHEMICAL CYCLE OF DIMETHYLSULPHIDE
ANGELA D. HATTON,1* LOUISE DARROCH2 & GILL MALIN2
1Scottish Association for Marine Science, Dunstaffnage Marine Laboratory,
Oban, Argyll, PA37 1QA, U.K.
2School of Environmental Sciences, University of East Anglia,
Norwich, NR4 7TJ, U.K.
*E-mail:

Abstract Dimethylsulphoxide ((CH3)2SO; DMSO) occurs naturally in marine and freshwater
environments, rainwater, and the atmosphere. It is thought to be an environmentally significant
compound due to the potential role it plays in the biogeochemical cycle of the climatically active
trace gas, dimethylsulphide (DMS). Generally it has been assumed that the photochemical and
bacterial oxidations of DMS to DMSO represent major sources of this compound and significant sinks
for DMS in the marine environment. Conversely, it has also been suggested that DMSO may be a
potential 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 the
marine sulphur cycle has still to be elucidated. The methods available for determining DMSO in
aqueous 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 possible
role this compound may play in the cycling of DMS and global climate.

Introduction
Dimethylsulphoxide (DMSO), the simplest of the homologous series of organic sulphoxides, is
well known for its unique solvent properties (David 1972) and is produced either as a waste product
of the papermaking industry or commercially by oxidation of dimethylsulphide (DMS) with dinitrogen tetroxide (Robbins 1961). It is a colourless, strongly hygroscopic, nonvolatile liquid that
has a boiling point at 189˚C and a melting point at 18.45˚C. Among its many applications, DMSO
is widely used in cell biology and is well known as a cryoprotectant for the preservation of living
cells and tissues (Yu & Quinn 1994). DMSO has also been widely used for diverse medical

applications. 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 been
suggested that DMSO has an antibacterial action, may act as a sedative (David 1972) and can both
reduce the infectivity of HIV in vitro and bring about the systematic improvement in advanced
AIDS 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, it
has been detected in freshwater lakes and streams (Andreae 1980a, Richards et al. 1994), Antarctic
0-8493-2727-X/04/$0.00+$1.50
Oceanography and Marine Biology: An Annual Review 2004 42, 29–56
© R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors

© 2005 by CRC Press LLC

29


2727_C02.fm Page 30 Wednesday, June 30, 2004 3:37 PM

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 that
DMSO 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 has
been suggested that DMS could be both chemically and biologically oxidised within the marine
environment, leading to the formation of DMSO, and as such, DMSO is expected to play an important
role 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). The
development of a new sensitive technique (Hatton et al. 1994b) and the refinement of previously
established 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 global
importance of DMS, its marine biogenic origin and the potential role DMSO may play in the
biogeochemical 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 to
provide 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 sulphide as the gaseous link, was for a long time considered to explain most of the biologically driven
flow 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 DMS
was the natural sulphur compound filling the role originally assigned to H2S. At that time it was
already known that many living systems, including marine algae, produced DMS, and biochemical
data were available that suggested that dimethylsulphoniopropionate (DMSP) might be the precursor 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 volatile
sulphur species in the oceans and this fact, along with the suggestion that DMS may play an
important 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 Southern

Oceans (see Kettle et al. 1999 and references therein). These studies have shown that DMS is
normally restricted to the upper 200 m of the water column, with higher concentrations found on
continental 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, the
rapid oxidation of DMS leads to the production of sulphur dioxide (SO2), sulphate, and methane
sulfonate (MSA), with sulphate and MSA present in the atmosphere predominantly in the form of
aerosol particles. These aerosols may be deposited in rain and snow, thereby contributing to the
acidity of natural precipitation (Plane 1989), and may act as cloud condensation nuclei (CCN) over
the 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
© 2005 by CRC Press LLC


2727_C02.fm Page 31 Wednesday, June 30, 2004 3:37 PM

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 across
the air–sea interface by a combination of molecular and turbulent diffusion processes, which are
influenced by wind speed, boundary layer stability, surfactants, and bubbles (Liss & Merlivat 1986,
Wanninkhof 1992, Nightingale et al. 2000). Current understanding of the processes controlling the

air–sea exchange of trace gases is covered in the recent monograph by Donelan et al. (2002), and
specific discussions on DMS emissions can be found in Malin (1996) and Turner et al. (1996). To
summarise, the sea-to-air flux of DMS is currently estimated to be of the order of 15–33 Tg of
sulphur yr–1 (Kettle et al. 1999). This flux accounts for a large fraction of total biogenic sulphur
emissions (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 by
marine 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 produce
DMSP 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 been
hypothesised that DMSP may be produced as an overflow mechanism enabling cells to keep cysteine
and methionine concentrations at a level that is low enough to prevent feedback mechanisms and
allow continued sulphate assimilation even under nitrogen-limited conditions (Stefels 2000). In the
early 1980s Barnard et al. (1982) and Bates & Cline (1985) noted that the distribution of DMS
and DMSP only correlated in a rather general way with phytoplankton biomass, leading them to
suggest that only certain groups of phytoplankton may produce significant amounts of DMSP.
Subsequently, it was shown that some taxonomic groups, such as dinoflagellates and prymnesiophytes, can contain high DMSP concentrations per unit cell volume, while diatoms have variable
but 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 suggests
that 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 it

would 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 some
DMSP 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 certain
phytoplankton 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, including
ventilation 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

© 2005 by CRC Press LLC


2727_C02.fm Page 32 Wednesday, June 30, 2004 3:37 PM

32

A. Hatton, L. Darroch & G. Malin

removal (Brimblecombe & Shooter 1986, Kieber et al. 1996, Brugger et al. 1998). Current evidence
suggests that the quantity of DMS emitted to the atmosphere is only a small proportion of the
potential marine pool (Malin et al. 1992). Indeed, a recent estimate of the total DMS flux to the
atmosphere, during a coccolithophore bloom, showed it to be equivalent to just 1.3% of the gross
DMSP 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 the
quantity 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 reviews
and 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 via

the lyase pathway to form DMS, but also via demethylation pathways yielding either 3-methiolpropionate (MMPA), which is then demethiolated producing methanethiol (MeSH), or 3-mercaptopropionate (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 most
circumstances in the water column (Ledyard & Dacey 1996, Van Duyl et al. 1998), and current
findings favour the demethylation/demethiolation pathway as being the major fate for DMSP in
sea 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 major
removal pathway for DMSP, a recent laboratory study investigated DMSP metabolism in 15
culturable bacteria of a lineage common in sea water and found that they all expressed the lyase
pathway, 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 being
shown 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 can
utilise 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), the
controversial hypothesis that the emissions of DMS may be linked with climate regulation. The
idea was that increased seawater temperature leads to increased DMS emissions, followed by
atmospheric oxidation, production of CCN, and increased cloud albedo, which would serve to
counteract the initial temperature increase. Thus the rate of DMS release may influence cloud
formation 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 the
assumption 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 aerosols
are effective CCN (Schwartz 1988), and there is also persuasive theoretical evidence that these
CCN may affect cloud albedo (Charlson et al. 1987, Idso 1992). Coherence between CCN concentration and cloudiness has been documented using satellite data, strongly suggesting that DMS
emissions can influence cloud radiative transfer properties (Boers et al. 1994). However, the negative
feedback loop of the phytoplankton, DMS, and climate regulation hypothesis (Charlson et al. 1987)
remains somewhat controversial.
© 2005 by CRC Press LLC


2727_C02.fm Page 33 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

33

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 the
DMS cycle. However, this stable and soluble compound originally proved difficult to analyse at
the nanomolar concentration range anticipated in marine aquatic environments. DMSO analysis
is problematic because DMSO is readily soluble in water, nonionic, and cannot be purged or
steam distilled (Harvey & Lang 1986). The various methods originally reported for DMSO
analysis in aqueous samples were based around direct measurement, which was insufficiently
sensitive 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 to
contamination 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 the
sulphur compounds on a silica or Tenax GC column, with subsequent extraction of the compounds
into methanol followed by gas chromatography. Berresheim et al. (1993) also developed a sensitive

direct method for the detection of DMSO in ambient air that is based on atmospheric pressure chemical
ionization/mass spectrometry (APCI/MS). However, neither of these techniques was suitable for use
with saline solutions, and therefore could not be used for marine samples. One direct method for DMSO
analysis has been demonstrated, which is suitable for use with seawater samples. In this case the
samples were injected directly into a gas chromatograph, with increased detector sensitivity, due to the
addition of sulphur hexafluoride, giving a detection limit equivalent to 0.06 nmol dm–3 (Lee & de Mora
1996). However, other research groups have not adopted this method.
Chemical reduction of DMSO to DMS and the subsequent analysis of DMS have greater sensitivity
and are suitable for saline solutions, but most existing methods are subject to some interferences. The
sample 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 that
NaBH4 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 for
measuring DMS and DMSO in sea water, but this method also necessitates the breakdown of DMSO
with 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 alkali
hydrolysis 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 reduction
methods (Kiene & Gerard 1994, Simó et al. 1996, 1998a). These refined methods along with the
development of a highly specific and sensitive enzyme-linked technique (Hatton et al. 1994b) have
allowed 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 that
phytoplankton may produce DMSO directly (Simó et al. 1998a) have led to the development of
several 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), or
the 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 gas

chromatography methods.

© 2005 by CRC Press LLC


2727_C02.fm Page 34 Wednesday, June 30, 2004 3:37 PM

34

A. Hatton, L. Darroch & G. Malin

Table 1

DMSO concentration ranges in the marine environment
DMSO concentration
(nmol dm–3)

Location

Reference

Coastal and open Pacific

19–181a

Andreae 1980a

Coastal and open Pacific

2.7–138

Hatton et al. 1998

Open Pacific

4–20

Kieber et al. 1996

Open Pacific

4

Bates et al. 1994

Coastal Pacific

6.3–124

Lee & de Mora 1996

Coastal Atlantic

4–6

Ridgeway et al. 1992

Coastal Atlantic

1.4–13

Kiene & Gerard 1994

North Atlantic

3.8–26

Simó et al. 2000

North Sea

2.3–25

Simó et al. 1998b, 2000

North Sea

<0.5–17.5

Hatton et al. 1996

Arabian Sea

<0.5–18

Hatton et al. 1996, 1999

Arctic fjord

<0.016

Lee et al. 1999a

Coastal Arctic

13.1–106

Bouillon et al. 2002

Coastal Arctic ice

2.0–116b

Lee et al. 2001

Coastal Antarctic

0.9–6

Gibson et al. 1990

Mediterranean Sea

2.2–62

Simó et al. 1995, 1997

a

Not corrected for DMSP interference.

Sample taken from sea ice.

b

Distribution of DMSO in sea water
A compilation of DMSO surface concentration data values from studies examining DMSO distribution in marine waters is presented in Table 1. Figure 1 shows concentration values superimposed
onto a world map and indicates that the current data set is rather sparse compared with similar
compilations of DMS data (Kettle et al. 1999). In surface waters the concentration of DMSO is
generally equal to or slightly higher than that of DMS (Hatton et al. 1996, 1999). Figure 2 shows
the concentrations of DMS and DMSO found in surface waters, from four data sets collected by the
authors. 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. From
these 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 whole
data set (Figure 3), suggesting that a similar relationship exists between the two compounds at
different locations. However, it should also be noted that some studies have found DMSO levels
that are one to two orders of magnitude greater than those of DMS (Andreae 1980a, Lee & de Mora
1996). 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 than
those of related dimethylated sulphur compounds. In both cases, it was concluded that poor light
penetration limited the photochemical oxidation of DMS and prevented the accumulation of DMSO.

© 2005 by CRC Press LLC


80°W

40°W

0°E 20°E 40°E 60°E

80°E 100°E 120°E

120°E

120°E

50°N

50°N

DMSO
(nmol dm-3)
30°N

30°N

10°N

10°N

0.5−1.5
1.6−3.0
3.1−5.0
5.1−7.5
7.6−10.0

10°S

10°S

10.1−15.0
15.1−30.0
30.1−45.0

30°S

30°S

45.1−100.0
100.1−125.0

50°S

50°S

120°E
120°E

140°E 160°E 180°W 160°W

120°W

80°W

40°W

0°E 20°E 40°E 60°E

80°E

100°E 120°E

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

2727_C02.fm Page 35 Wednesday, June 30, 2004 3:37 PM

120°W

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

© 2005 by CRC Press LLC

120°E 140°E 160°E 180°W 160°W

35


2727_C02.fm Page 36 Wednesday, June 30, 2004 3:37 PM

36

A. Hatton, L. Darroch & G. Malin

Sulphur (nmol dm−3)

A 20
18
16

14
12
10
8
6
4
2
0
1

2

3

4

5

6

7

8

9 10 11 12 13 14 15 16

Station No.

Sulphur (nmol dm−3)

B 12
10
8
6
4
2
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Station No.

07-Feb

04-Feb

02-Feb

29-Jan

26-Jan

22-Jan

20-Jan

14-Jan

10-Jan

Sulphur (nmol dm−3)

C 40
35
30
25
20
15
10
5
0

Date

Sulphur (nmol dm−3)

D 12
10
8
6
4
2

Aug

July

June

May

April

March

Feb

Jan

Dec

Nov

Oct

Sept

0

Month

Figure 2 Near-surface concentrations for DMS (᭡) and DMSO (ⅷ) 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.)

© 2005 by CRC Press LLC


2727_C02.fm Page 37 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

37

40

DMSO (nmol dm−3)

35
30
25
20
15
10
5
0
0

5

10
DMS (nmol

15

20

25

dm−3)

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 (r2 = 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.

The strong correlation between DMS and DMSO only appears to hold for surface waters and
results from depth profiles show a different story. DMSO has been shown to be ubiquitous throughout 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 has
been reported at concentrations greater than 1.5 nmol dm–3 at depths up to 1500 and 4000 m in
the equatorial Pacific Ocean and Arabian Sea, respectively (Hatton et al. 1998, 1999). As a
consequence, when the whole water column is taken into account, depth-integrated DMSO levels
are significantly higher than those for DMSP. Hence DMSO can be the dominant DMS-related
sulphur 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 New
Zealand, 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 stated
that 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 waters
and 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, and
levels below the analytical detection limit of 0.3 nmol dm–3 during winter (Hatton & Lyall, in
preparation). Increased levels of DMSOp coincided with increases in DMSOd, DMS, and chlorophyll 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 in
DMSOp, indicating that the DMSOp may have been produced either by a different species or at a
different 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 for
samples 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 been
shown that the majority of this DMSOp is found in the microplankton-size fraction of seawater
samples (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
© 2005 by CRC Press LLC


2727_C02.fm Page 38 Wednesday, June 30, 2004 3:37 PM

38

A. Hatton, L. Darroch & G. Malin

(Bouillon et al. 2002). DMSOp has also been measured in the sea ice algal communities of Baffin
Bay where levels ranged from 1.35–102 nmol dm–3 and were higher than those found in the water
column. This difference in concentration was presumably because of the higher biomass of plankton
found 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 generally
thought that DMSO would be formed mainly from the photochemical (Brimblecombe & Shooter
1986) or bacterial (Zeyer et al. 1987) oxidation of DMS. The formation of DMSO would therefore
lead to the removal of DMS from sea water, effectively limiting the quantity of DMS available for
transfer to the atmosphere. In addition, it was proposed that since DMSO concentrations are
generally higher than those of DMS, and since some bacteria had been shown to be capable of
reducing DMSO to DMS (Zinder & Brock 1978), DMSO could also represent an important source
for DMS. Although the interactions occurring between these two compounds may prove to be key
processes in DMS biogeochemistry (Lee et al. 1999b), a great deal of research is still required if

the relative significance of these pathways and the factors influencing them are to be fully understood. The next two sections discuss the current understanding of the ways in which DMSO may
act 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), because
oxidation of DMS in the presence of hydrogen peroxide is much faster than oxidation by molecular
oxygen (Shooter & Brimblecombe 1989). It has also been demonstrated that hydrogen peroxide
can be produced by marine phytoplankton (Palenik et al. 1987), making it easily available for DMS
oxidation. However, the loss of DMS via photo-oxidation to DMSO in sea water is likely to be a
more significant reaction. The photochemical oxidation of DMS to DMSO was first implied by
Brimblecombe & Shooter (1986), who estimated the global quantity of DMS photo-oxidised would
amount to 6.4 Tg(S) yr–1. During laboratory experiments with aqueous solutions, they observed
that 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 does
not appreciably absorb light of wavelengths of >260 nm (McDiarmid 1974). However, Brimblecombe & Shooter (1986) went on to demonstrate that in the presence of photosensitisers, such as
anthroquinone and humic acid, DMS is also susceptible to photolysis by visible light. They
concluded that the photolysis of DMS in the presence of photosensitisers followed pseudo-firstorder 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 dissolved
molecular oxygen to form singlet oxygen, which then reacts with the substrate. However, it is
important to point out that DMSO was never directly measured in their study, and the complete
oxidation of DMS to DMSO was inferred from the observed loss of two molecules of DMS for
each molecule of oxygen.
In 1996, Kieber et al. also showed that DMS photolysis could be mediated by wavelengths in
the UVB range (280–315 nm). However, they concluded that in natural waters DMS photolysis
would be primarily mediated by PAR (photosynthetically active radiation or wavelengths from
380–460 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

© 2005 by CRC Press LLC


2727_C02.fm Page 39 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

39

UVA/visible wavelengths (>315 nm) in the northern North Sea. It was concluded that under visible
wavelengths 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 of
dissolved organic carbon (DOC), whereas at wavelengths of <315 nm (UVB) a second DMS
photolysis pathway operates that does not yield DMSO. The additional loss of DMS due to UVB
radiation meant that the oxidation of DMS to DMSO accounted for only 37% of the total DMS
lost under full natural light conditions (Hatton 2002a).
These results clearly indicate that UVB radiation may play a major role in the removal of DMS
from surface waters. Often the potential importance of UV radiation has been neglected due to
early reports that UV penetration was limited to the very top layers of the water column, even in
the open ocean. However, with more sensitive instruments it has now been demonstrated that UV
radiation 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 decline
with 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% light
levels for UVB in Adriatic coastal waters.
These results have important consequences for the understanding of the photochemical processes affecting the level of DMS in surface water. It has been suggested that DMSO could
potentially be reduced back to DMS (Suylen et al. 1986, Weiner et al. 1992). Therefore, any DMS
removed via its photooxidation to DMSO may be recycled and, as such, represents a future source
of oceanic DMS, whereas the photolysis of DMS by UVB radiation may result in its total removal
from the water column.

The formation of DMSO may also be affected by geographic location. Higher DMS photolysis
rate constants of 0.12 h–1 and 0.09–0.14 h–1 have been measured at coastal sites in the Adriatic Sea
and North Sea, respectively (Brimblecombe & Shooter 1986, Brugger et al. 1998), compared with
incubations 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 been
shown 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 productive
regions.
DOC may also affect the photolysis of DMS and the photoformation of DMSO throughout the
water 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 found
that DMS photolysis continued to different depths in oligotrophic compared with coastal environments (Brugger et al. 1998). It was predicted that DMS photolysis was still a significant process
down to 60 m in the water column of the oligotrophic equatorial Pacific Ocean. Conversely, in
more 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 surprising
because high concentrations of DOC, such as those found in coastal areas, would prevent the
penetration of light at depth. However, although there appear to be differences in the maximum
depth at which DMS photolysis occurred, these differences were not reflected in the final depthintegrated 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 that
this similarity in depth-integrated turnover rate may be due to a lower photolytic activity in the
open ocean, being compensated by a lower light attenuation. In other words, it seems likely that
high DOC concentration will affect photochemical processes in the marine environment by both
increasing the initial photolysis rates in surface waters and reducing the quantity and quality of the
irradiance penetration through the water column. Furthermore, it should be noted that it has been
© 2005 by CRC Press LLC

2727_C02.fm Page 40 Wednesday, June 30, 2004 3:37 PM

40

A. Hatton, L. Darroch & G. Malin

shown that DMS photolysis (and thus DMSO production) may be affected not only by the quantity
but 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 those
due to bacterial consumption and atmospheric ventilation of DMS (Kieber et al. 1996, Hatton
2002b), demonstrating the potential importance of this pathway in the marine sulphur cycle.
However, there is still some conflicting evidence concerning the mechanisms involved, the importance 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 and
DMS photolysed without DMSO production may have significant implications for DMS biogeochemistry.

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 hygroscopic
nature, DMSO would be scavenged from the air by rain (Lovelock et al. 1972) and returned to the
oceans in precipitation. A few studies have reported DMSO in rainwater with concentrations ranging
from 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 Indian
Ocean, a distinct seasonal cycle in the wet deposition of DMSO was found, with an average summer
maximum and winter minimum of 90 and 25.6 nmol dm–3, respectively (Sciare et al. 1998). The
seasonal 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 sulphur
cycle because the annual average deposition rate of DMSO was 0.12 mmol m–2 d–1, which accounted
for 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). Microorganisms use sulphur compounds not only for assimilatory purposes, but also in biochemical
processes where they may act as electron donors or electron acceptors. In the past a number of
culture studies were conducted that demonstrated that some phototrophic bacteria are capable of
oxidising 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) showed
that enrichment cultures of phototrophic purple bacteria, including a pure strain of a marine
Thiocystis species, rapidly oxidised up to 10 mM DMS to DMSO. Hansen et al. (1993) isolated
seven pure bacterial cultures that could utilise DMS as an electron donor for CO2 fixation, with
DMSO as the only product. Visscher & van Gemerden (1991) examined the purple sulphur bacterium Thiocapsa roseopersicina for photoautotrophic growth on DMS. They demonstrated that this
bacterium 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
acidovorans, which oxidised DMS to DMSO under aerobic conditions. However, this bacterium
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 grew
autotrophically 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 was
distinct from the DMSO reductase found in this bacterium.

© 2005 by CRC Press LLC


2727_C02.fm Page 41 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

41

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 microaerophilic 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
© 2005 by CRC Press LLC


2727_C02.fm Page 42 Wednesday, June 30, 2004 3:37 PM

42

A. Hatton, L. Darroch & G. Malin

experiments show that a bacterial production pathway for DMSO exists in natural samples collected
from the pelagic marine environment, although the importance of this process in the marine DMS
cycle 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 long
residence time for DMSO, the source of this deepwater DMSO has never been elucidated. DMSO is
known to permeate membranes (Liu et al. 1997). Therefore, DMSO produced within sedimenting
material 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 within
sedimenting material, this pathway cannot account for all the DMSP lost from these sites, and
therefore other alternate loss pathways are likely to be involved in the removal of DMSP or DMS
from the samples. Zooplankton faecal pellets have been shown to be colonised by bacteria that can
utilise DMSP (Tang et al. 2001). It has also been suggested that because faecal pellets contain
much 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 anoxic
sediments (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 methanogenic bacteria may be present in zooplankton guts and enter the sinking particulate field through
the formation of faecal pellets (DeAngelis & Lee 1994, Marty 1993, Karl & Tilbrook 1994, Holmes
et al. 2000). DMS is a known substrate for methanogenic 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 the
large pool of DMSO observed in sea surface waters (Lee & de Mora 1996). Evidence to support
the direct biosynthesis of DMSO by marine phytoplankton in sea water was first reported during

diurnal studies in the coastal waters of North Island, New Zealand. Rapid daytime production of
dissolved 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 in
that environment could not have accounted for all of the light-dependent production of DMSO. It
was 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, Emiliania huxleyi (Simó et al. 1998a). Intracellular production of DMSO coincided with logarithmic
growth, where the average logarithmic cellular content was approximately 0.3 and 0.1 pg of DMSO
cell–1, translating to DMSPp:DMSOp ratios of 25 and 8, respectively. Coinciding with intracellular
production, 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 the
ratio of these two compounds was not consistent between different stations in the Saguenay Fjord,

© 2005 by CRC Press LLC


2727_C02.fm Page 43 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

43

Québec. For example, ratios of DMSOp to DMSPp at two stations in the fjord were calculated at
26:1 and 112:1. Although DMSOp concentrations were similar at both sites, the variation in the
ratios was driven by the dominance of DMSP-producing phytoplankton measured at the former
site. Similar evidence was found in the waters of Baffin Bay in the Arctic (Bouillon et al. 2002).
Toward the end of this study (the final month of a 3-month period) it was found that DMSPp did
not correlate significantly with chlorophyll a, whereas DMSOp had a strong positive correlation

with chlorophyll a throughout the study period, and this finding was thought to be consistent with
the notion of ubiquitous DMSOp production. One suggestion for the strong positive correlation
between DMSOp and chlorophyll a was that DMS may be oxidised to DMSO within cells by
chlorophyll a and other photosynthetic pigments. Fuse et al. (1997) found that DMS could be
oxidised to DMSO in the light by lyophilised algae as long as plant pigments were present, which
might lead to positive correlations with chlorophyll a in the natural environment. However, positive
correlations between chlorophyll a and DMSOp are not consistent. For example, no correlations
were found between chlorophyll a and the DMSOp in ice algal communities, leading to speculation
that DMSOp production may vary with species in these environments (Lee et al. 2001). In addition,
negative correlations were found in the Saguenay Fjord (Lee et al. 1999a).
More recently, laboratory experiments conducted to investigate the production of DMSO by a
wide range of phytoplankton species have now shown that the production of DMSO by marine
phytoplankton may be group specific (Hatton et al., in preparation). These results indicate that, in
common with DMSPp, prymnesiophytes and dinoflagellates appeared to be the main producers of
DMSO, with diatoms being relatively poor producers. In addition, the results indicate that the level
of DMSO produced increased significantly during stationary phase and senescence, compared with
the log phase. In the sea, therefore, the stage of a phytoplankton bloom may have an important
impact on the levels of DMSO observed, especially because release of DMSOp may occur through
passive diffusion across cell membranes.
It is clear that currently there is insufficient evidence to make firm conclusions as to the
cellular role of DMSO. Given that DMSO is well established as an effective radical scavenger
(Datta et al. 2002, Hooiveld et al. 2003), it has been suggested that it may offer protection against
reactive oxygen radicals generated during photosynthesis. The role of DMSO as an antioxidant
in marine algae has been discussed in several other articles (Simó et al. 1998a, Lee & de Mora
1999, Sunda et al. 2002). Sunda et al. (2002) speculated that intracellular DMSO may be part
of an antioxidant system within cells. They proposed that DMSPp, its cleavage products DMS
and acrylate, and the oxidation products of DMS could all react with reactive oxygen radicals
to defend against oxidative stress. Their laboratory experiments demonstrated that DMSO could
be produced through the oxidation of DMSP by OH radicals or through the oxidation of DMS
by OH radicals and singlet oxygen. DMSO would then be further oxidised to methane sulphinic

acid (MSNA) and, subsequently, MSA. Similarly, Steinke et al. (2002) suggested that DMSO
could result from the reaction of DMS with oxygen radicals, caused by high irradiance levels.
The authors noted that the ratio of DMSP lyase activity and DMSOd to chlorophyll a increased
toward the surface of the northern North Sea, where cells are exposed to higher solar UV
irradiation.
Other potential functions suggested for intracellular DMSO are as an intracellular electrolyte
modifier or as a cryoprotectant (Lee & de Mora 1999). However, Lee et al. (2001) dismiss the
possibility of a cryoprotective role because the cellular concentration of DMSOp in Arctic ice algae,
estimated to be between a few tens to hundreds of mmol dm–3, was thought to be too low to have
a significant influence on the freezing point depression of intracellular fluids.
Although the role of DMSO in cells is still subject to considerable debate, the fact that marine
phytoplankton may directly produce DMSO could be considered to be one of the most interesting
and exciting discoveries within DMS biogeochemistry in recent times. As it has been hypothesised
that DMSO may be reduced to DMS via bacterial transformations, the direct synthesis and release
of DMSO by phytoplankton may potentially represent a novel source of DMS in sea water.
© 2005 by CRC Press LLC


2727_C02.fm Page 44 Wednesday, June 30, 2004 3:37 PM

44

A. Hatton, L. Darroch & G. Malin

Reduction of DMSO to DMS
It has been suggested that DMSO can be reduced chemically to DMS by sulphide (Zinder & Brock
1978), or it can disproportionate, via a biomolecular redox reaction, to DMS and DMSO2 (Harvey
& Lang 1986) as follows:
2CH3SOCH3 Ỉ CH3SCH3 + CH3SO2CH3
However, the biological reduction of DMSO in sea water is likely to be far more significant.

Although it has been suggested that a wide range of organisms, including prokaryotes and eukaryotes, are capable of reducing DMSO to DMS using a DMSO reductase enzyme (Zinder & Brock
1978, Bilous & Weiner 1985), many of the transformations involving DMSO reported to date
involve marine purple bacteria, which are also known as proteobacteria (Visscher & van Gemerden
1991, Jonkers et al. 1996, 1998, Vogt et al. 1997).
The DMSO reductase, which functions in anaerobic growth, has been the subject of several
studies. Anaerobic respiration of DMSO provides a sink for electrons generated during phototrophic
growth on highly reduced carbon sources (Richardson et al. 1988). A number of facultative
anaerobes have been shown to utilise DMSO in this way, with DMSO acting as a terminal electron
acceptor in anaerobic respiration (Zinder & Brock 1978). These included Proteus vulgaris, Rhodobacter capsulatus, Shewanella putrefaceins, and Escherichia coli (McEwan et al. 1985, Bilous &
Weiner 1985, Clarke & Ward 1988).
Two distinct types of respiratory DMSO reductase have been identified that terminate a protontranslocating respiratory chain (McEwan et al. 1991a). These are exemplified by those from
Escherichia coli (Weiner et al. 1988) and Rhodobacter capsulatus (McEwan et al. 1991b). In
Escherichia coli the DMSO reductase is membrane associated with its catalytic face toward the
cytoplasm and contains both molybdenum and iron sulphur clusters (Weiner et al. 1992). By
contrast, the second type of DMSO reductase is located in the periplasmic space of Rhodobacter
capsulatus (McEwan et al. 1985) and contains only molybdenum (McEwan et al. 1987). The
periplasmic DMSO reductase has been purified as a monomer of molecular weight (Mr) of 82,000
daltons (McEwan et al. 1991a), whereas the membrane-associated enzyme has an Mr of 155,000
daltons, consisting of three subunits of apparent Mr values of 82,600, 23,600, and 22,700 daltons
(Weiner et al. 1988).
Although most studies of the reduction of DMSO to DMS have been done using anaerobic
bacteria or anaerobic environments/conditions, including more up-to-date work on the green bacteria, Chlorobium vibrioforme (Vogt et al. 1997), and the mat-forming cyanobacterium, Phormidium
sp. (van Bergeijk & Stal 1996), recent studies have now shown that five species of the Roseobacter
group, isolated from oxygenated sea water, were able to reduce DMSO to DMS (Gonzàlez et al.
1999).

Removal of DMSO without DMS production
Although DMSO has been shown to be reduced by a variety of both aerobic and anaerobic bacteria,
leading to the formation of DMS, two strains of Hyphomicrobium have also been described that
utilise DMSO as a carbon source during aerobic growth (deBont et al. 1981, Suylen et al. 1986, Hatton

et al. 1994a). In this case DMSO reduction is the first step in its assimilation as a carbon source and
as such the DMS is also utilised. deBont et al. (1981) suggested a pathway for the metabolism of
DMSO and DMS in Hyphomicrobium S via the serine pathway (deBont et al. 1981, Suylen et al.
1986, Suylen 1988). This type of growth by Hyphomicrobium on methylated sulphur compounds has
been described as chemolithoheterotrophic. These bacteria are heterotrophs and therefore need an
organic compound as a carbon and energy source but can gain additional energy from the oxidation
of reduced inorganic sulphur compounds (Suylen 1988).

© 2005 by CRC Press LLC


2727_C02.fm Page 45 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

45

In addition to its consumption, the oxidation of DMSO to dimethylsulphone (DMSO2), with
H2O2 by chloroperoxidase enzymes in some marine bacteria, has also been hypothesised (Lee et
al. 1999b). It has been suggested that this pathway may occur in sea water because chemiluminescent
bacteria present in oxygenated oceanic environments are known to have chloroperoxidases (Taylor &
Kiene 1989). In the marine environment, possible bacterial consumption of DMSO has only been
observed during dark incubations with natural sea water (Simó et al. 2000). Simó et al. (2000)
calculated a net DMSO consumption rate of 4 nmol dm–3 d–1, that is, a turnover time of 2 days in
the North Sea. Although consumption appeared to have no effect on DMS levels, it could not be
concluded that DMSO was not being reduced to DMS, as the production and consumption of DMS
were tightly coupled at that site.
No data have been published demonstrating the presence of DMSO2 in marine waters (Lee et
al. 1999b). In studies where measurements were taken for DMSO2 (de Mora et al. 1996) this
compound was never shown to be above the analytical detection limit (0.16 nm dm–3). It has been

suggested that this may be due to two possibilities. First, if the bacterial oxidation of DMSO to
DMSO2 does occur, then it is likely to be an intracellular process with DMSO2 being retained for
further use. Alternatively, subsequent loss processes involving DMSO2 could be more rapid than
the formation processes (Lee et al. 1999b).

Summary and conclusions
In the marine environment, interest in the distribution of DMSO focuses around the concept that
DMSO may play a role in DMS biogeochemistry, influencing the concentrations of DMS in sea
water available to be transferred to the atmosphere. The flux of DMS to the air and the factors
controlling its concentration in surface water are extremely important for a number of reasons.
First, it is now widely accepted that DMS plays a major role in the global sulphur cycle by
transferring sulphur from the oceans to land (Lovelock et al. 1972). Second, atmospheric oxidation
products of DMS not only contribute to the acidity of precipitation (Andreae 1990, Bates et al.
1992) but may also influence climate through the formation of cloud condensation nuclei (Charlson
et al. 1987). Third, DMS and its precusors represent important sources of carbon, reduced sulphur,
and energy for bacterioplankton (Kiene 1993, Kiene et al. 2000).
Although DMSO may theoretically play a role in controlling the levels of DMS in marine
waters, it is in its own right an important component of the marine sulphur cycle (Lee et al. 1999b).
DMSO occurs in the marine environment as a result of a network of chemical and biological
processes, including photochemical and enzymatic oxidation of DMS, direct production of DMSO
by marine phytoplankton, and anaerobic formation of DMSO in sedimenting faecal pellets (Figure
4). On occasion DMSO levels can exceed those of DMS and DMSP in euphotic waters, and when
the whole water column is taken into account, depth-integrated DMSO levels are significantly
higher than those of other dimethylated sulphonium compounds, making it the dominant DMSrelated sulphur species throughout the water column (Hatton et al. 1998).
In surface waters, the concentrations of DMSO closely parallel those of DMS, and this finding
has led to the suggestion that photochemistry may be one of the main factors controlling the
interaction between these two compounds in surface waters. It is now known that losses of DMS
due to photolysis are comparable with those due to bacterial consumption and atmospheric ventilation, and a number of studies have estimated that between 14 and 37% of the DMS lost is oxidised
to DMSO (Kieber et al. 1996, Hatton 2002a).
In addition to photochemical oxidation it was traditionally thought that DMS would also be

enzymatically catalysed to DMSO. Although most early studies to investigate bacterial oxidation
of DMS to DMSO were conducted using cultures of obligate anaerobes (Zeyer et al. 1987, Visscher
& van Gemerden 1991, Hansen et al. 1993), the enzymatic oxidation of DMS in oceanic waters now
seems highly likely because it has been observed in proteobacteria isolated from oxygenated coastal
waters (González et al. 1999). Furthermore, the anaerobic oxidation of DMS has been demonstrated
© 2005 by CRC Press LLC


Photochemical
oxidation
Atmosphere
Ocean
Photochemical
oxidation

Photolysis

Microbial
oxidation

DMS
Direct
emissions
Microbial
lysis

Microbial
reduction

DMSO

Microbial
oxidation

DMSO2

Bacterial
consumption

Permeative
loss

Particulate
DMSO

Grazing and
lysis

Sedimentation

Particulate
DMSP

Figure 4 The biogeochemical cycle for DMSO in the marine environment, based on discussion within this paper. Dotted line denotes recently hypothesised pathways.
(Adapted from Lee et al. 1999b by permission of the Canadian Meteorological and Oceanographic Society.)

A. Hatton, L. Darroch & G. Malin

Dissolved
DMSP

2727_C02.fm Page 46 Wednesday, June 30, 2004 3:37 PM

46

© 2005 by CRC Press LLC

Atmospheric
transfer


2727_C02.fm Page 47 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

47

within sedimenting faecal pellets, leading to the formation of DMSO within these sites (Hatton
2002b). As DMSO readily permeates membranes it seems likely that it would leach out of the
faecal pellets into surrounding waters, representing a source for dissolved DMSO in both euphotic
and deeper waters.
In recent years it has been shown that DMSO can be produced directly within the cells of
marine phytoplankton (Simó et al. 1998a). The exact role DMSO plays in cells is still subject to
debate, but it has been suggested that it may be a by-product of sulphur metabolism, an antioxidant,
or act as a cryoprotectant. Whatever the reason, permeative loss of DMSO from cells may contribute
to dissolved DMSO concentrations, and as such, this new pathway must be considered an important
component of DMSO biogeochemistry.
Loss processes for DMSO in marine waters include its oxidation and utilisation by microorganisms and its reduction to DMS. It has generally been thought that the bacterially mediated
reduction of DMSO would be an important pathway in the DMS cycle. However, much of the
work conducted on this pathway was carried out using cultures of anaerobic bacteria (Zinder &

Brock 1978, Bilous & Weiner 1985). Although recent work has shown that five species of the
Roseobacter group isolated from surface waters were able to reduce DMSO to DMS, suggesting
this process may occur in oxic waters, the actual occurrence of biological DMSO-to-DMS conversion in oxygenated waters has still not been demonstrated.
Significant progress has now been made in elucidating the processes involved in the production
and transformation of DMSO, but further work is required if we are to fully understand the relative
significance of the pathways involved. Furthermore, if we are to reveal the full extent to which DMS
affects global climate through the formation of CCN (CLAW hypothesis, see p. 32), we must first
discover whether DMSO represents a net sink or source for oceanic DMS and how the interactions
between these two compounds alter with changing climatic conditions.

Acknowledgements
This work was supported by a Ph.D. studentship (GT04/99/MS/69) and three fellowships
(GT5/97/6/MAS, NER/I/S/1999/00160, and GT5/98/8/MS) from the U.K. Natural Environment
Research Council. We thank the Scottish Association for Marine Science and the University of
East Anglia for supporting our DMSO research. Thanks are also given to Steve Gontarek for help
with ArcMap and Stephen Teape for help with references. This work is contribution number 441/3
of the European Union ELOISE Programme in the framework of the ESCAPE project carried out
under contract MAS3-CT96-0050.

References
Andreae, M.O. 1980a. Dimethylsulfoxide in marine and freshwaters. Limnology and Oceanography 25,
1054–1063.
Andreae, M.O. 1980b. Determination of trace quantities of dimethylsulfoxide in aqueous solution. Analytical
Chemistry 52, 150–153.
Andreae, M.O. 1986. The ocean as a source of atmospheric sulfur compounds. In The Role of Air–Sea Exchange
in Geochemical Cycling, P. Buat-Menard (ed.). Dordrecht: Reidel, pp. 331–362.
Andreae, M.O. 1990. Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Marine
Chemistry 30, 1–29.
Andreae, M.O. & Barnard, W.R. 1984. The marine chemistry of dimethylsulphide. Marine Chemistry 14,
267–279.

Andreae, M.O., Barnard, W.R. & Ammons, J.M. 1983. The biological production of dimethylsulfide in the
ocean and its role in the global atmospheric sulfur budget. Environmental Biogeochemistry 35,
167–177.

© 2005 by CRC Press LLC


2727_C02.fm Page 48 Wednesday, June 30, 2004 3:37 PM

48

A. Hatton, L. Darroch & G. Malin

Andreae, M.O. & Raemdonck, H. 1983. Dimethylsulfide in the surface ocean and the marine atmosphere: a
global view. Science 221, 744–747.
Andreae, T.W., Andreae, M.O. & Schebeske, G. 1994. Biogenic sulfur emissions and aerosols over the tropical
south Atlantic. 1. Dimethylsulfide in sea water and in the atmospheric boundary layer. Journal of
Geophysical Research 99, 22819–22829.
Anigbogu, A.N.C., Williams, A.C., Barry, B.W. & Edwards, H.G.M. 1995. Fourier-transform raman-spectroscopy of interactions between the penetration enhancer dimethyl-sulfoxide and human stratum-corneum. International Journal of Pharmaceutics 125, 265–282.
Anness, B.J. 1981. The determination of dimethylsulphoxide in aqueous solution. Journal of Scientific Food
Agriculture 32, 353–358.
Aranda-Anzaldo, A., Ablashi, D.V. & Viza, D. 1992. In vitro reduction of HIV infectivity by dimethylsulphoxide. AIDS 6, 1402–1403.
Archer, S.D., Smith, G.C., Nightingale, P.D., Widdicombe, C.E., Tarran, G.A., Ress, A.P. & Burkill, P.H. 2002.
Dynamics of particulate dimethylsulphoniopropionate during a Lagrangian experiment in the northern
North Sea. Deep-Sea Research II 49, 2979–2999.
Barnard, W.R., Andreae, M.O., Watkins, W.E., Bingemer, H. & Georgii, H.W. 1982. The flux of dimethylsulfide
from the oceans to the atmosphere. Journal of Geophysical Research 87, 8787–8793.
Barnes, I., Becker, K.H., Carlier, P. & Mouvier, G. 1987. FTIR study of the DMS/NO2/I2/N2 photolysis system.
The reaction of IO radicals with DMS. International Journal of Chemical Kinetics 19, 489–501.
Bates, T.S. & Cline, J.D. 1985. The role of the ocean in a regional sulfur cycle. Journal of Geophysical

Research 90, 9168–9172.
Bates, T.S., Cline, J.D., Gammon, R.H. & Kelly-Hansen, S.R. 1987. Regional and seasonal variations in the
flux of oceanic dimethylsulfide to the atmosphere. Journal of Geophysical Research 92, 2930–2938.
Bates, T.S., Lamb, B.K., Guenther, A., Dignon, J. & Stoiber, R.E. 1992. Sulphur emissions to the atmosphere
from natural sources. Journal of Atmospheric Chemistry 14, 315–337.
Bates, T.S., Kiene, R.P., Wolfe, G.V., Matrai, P.A., Chavez, F.P., Buck, K.R., Blomquist, B.W. & Cuhel, R.L.
1994. The cycling of sulfur in surface sea water of the northeast Pacific. Journal of Geophysical
Research 99, 7835–7843.
Berresheim, H., Eisele, F.L., Tanner, D.J., McInnes, L.M., Ramsey-Bell, D.C. & Covert, D.S. 1993. Atmospheric
sulfur chemistry and cloud condensation nuclei concentrations over the northeastern Pacific Coast. Journal
of Geophysical Research 98, 12701–12711.
Bertelli, G., Dini, D., Forno, G., Gozza, A., Venturini, R., Ballella, G. & Rosso, R. 1993. Dimethylsulphoxide
and cooling after extravasation of antitumour agents. The Lancet 341, 1098–1099.
Bilous, P.T. & Weiner, J.H. 1985. Dimethylsulfoxide reductase activity by anaerobically grown E. coli HB101.
Journal of Bacteriology 162, 1151–1155.
Boers, R., Ayers, G.P. & Gras, J.L. 1994. Coherence between seasonal variation in satellite-derived cloud
optical depth and boundary layer CCN concentrations at a mid-latitude southern hemisphere station.
Tellus 46B, 123–131.
Bouillon, R.-C., Lee, P.A., de Mora, S.J., Levasseur, M. & Lovejoy, C. 2002. Vernal distribution of dimethylsulphide, dimethylphoniopropionate, and dimethylsulphoxide in the North Water in 1998. Deep-Sea
Research II 49, 5171–5189.
Brimblecombe, P. & Shooter, D. 1986. Photo-oxidation of dimethylsulphide in aqueous solution. Marine
Chemistry 19, 343–353.
Brugger, A., Slezak, D., Obernosterer, I. & Herndl, G.J. 1998. Photolysis of DMS in the northern Adriatic
Sea: dependence on substrate concentraion, irradiance and DOC concentration. Marine Chemistry 59,
321–331.
Cantoni, G.L. & Anderson, D.G. 1956. Enzymic cleavage of dimethylpropiothetin by Polysiphonia lanosa.
Journal of Biological Chemistry 222, 171–177.
Challenger, F. 1951. Biological methylation. Advanced Enzymology 12, 429–491.
Challenger, F. & Simpson, M.I. 1948. Studies on biological methylation XII: a precursor of the dimethylsulfide
evolved by Polysiphonia fastigate, dimethyl-2-carboxyethyl-sulphonium hydroxide and its salts. Journal of the Chemical Society 3, 1591–1597.

Charlson, R.J., Lovelock, J.E., Andreae, M.O. & Warren, S.G. 1987. Oceanic phytoplankton, atmospheric
sulfur, cloud albedo and climate. Nature 326, 655–661.

© 2005 by CRC Press LLC


2727_C02.fm Page 49 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

49

Chin, M. & Jacob, D.J. 1996. Anthropogenic and natural contributions to tropospheric sulphate: a global
model analysis. Journal of Geophysical Research 101, 18691–18699.
Clarke, G.J. & Ward, F.B. 1988. Purification and properties of trimethylamine-N-oxide reductase from
Shewanella species NCMB400. Journal of General Microbiology 133, 379–386.
Corn, M., Belviso, S., Nival, P., Vigot, A. & Buat-Menard, P. 1994. Downward flux of particulate dimethylsulphoniopropionate in the tropical open ocean. Oceanologica Acta 17, 233–236.
Dacey, J.W.H. & Wakeham, S.G. 1986. Oceanic dimethylsulfide: production during zooplankton grazing on
phytoplankton. Science 233, 1314–1316.
Daly, K.L. & DiTullio, G.R. 1996. Particulate dimethylsulphoniopropionate removal and dimethylsulfide
production by zooplankton in the Southern Ocean. In Biological and Environmental Chemistry of
DMSP and Related Sulphonium Compounds, R.P. Kiene et al. (eds). New York: Plenum Press, pp.
223–238.
Datta, K., Babbar, P., Srivastava, T., Sinha, S. & Chattopadhyay, P. 2002. p35 dependent apoptosis in glioma
cell lines in response to hydrogen peroxide induced oxidative stress. The International Journal of
Biochemistry and Cell Biology 34, 148–157.
David, N.A. 1972. The pharmacology of dimethylsulphoxide. Annual Review of Pharmacology 12, 343–374.
DeAngelis, M.A. & Lee, C. 1994. Methane production during zooplankton grazing on marine phytoplankton.
Limnology and Oceanography 39, 1298–1308.
deBont, J.A.M., van Dijken, J.P. & Harder, W. 1981. Dimethyl sulphoxide and dimethyl sulphide as a carbon,

sulfur and energy source for growth of Hyphomicrobium S. Journal of General Microbiology 127,
315–323.
de Mora, S.J., Lee, P., Shooter, D. & Eschenbruch, R. 1993. The analysis and importance of dimethylsulfoxide
in wine. American Journal of Enology and Viticulture 44, 327–332.
de Mora, S.J., Lee, P.A., Grout, A., Schall, C. & Heumann, K.G. 1996. Aspects of the biogeochemistry of
sulfur in glacial melt water ponds on the McMurdo Ice Shelf, Antarctica. Antarctic Science 8, 15–22.
Diamond, W.J.W., Cowden, L. & Goldberg, B. 1997. An Alternative Medicine Definitive Guide to Cancer.
Tiburon, CA: Future Medicine Publishing Co. Inc.
Donelan, M.A., Drennan, W.M., William, M., Saltzman, E.S. & Wanninkhof, R. (eds). 2002. Gas transfer at
water surfaces. Geophysical Monograph Series 127. Washington, DC: American Geophysical Union.
Erickson, D.J., Ghan, S.J. & Penner, J.E. 1990. Global ocean to atmosphere dimethylsulfide flux. Journal of
Geophysical Research 95, 7543–7552.
Evans, M.S., Reid, K.H. & Sharp, J.B. 1993. Dimethylsulfoxide blocks conduction in peripheral nerve fibres:
a possible mechanism of analgesia. Neuroscience Letters 150, 145–148.
Finster, K., Tanimoto, Y. & Bak, F. 1992. Fermentation of methanethiol and dimethylsulfide by a newly isolated
methanogenic bacteria. Archives of Microbiology 157, 425–430.
Fleischmann, E.M. 1989. The measurement and penetration of ultraviolet radiation into tropical marine waters.
Limnology and Oceanography 34, 1623–1629.
Fuse, H., Ohta, M., Takimura, O., Murakami, K., Inoue, H., Yamaoka, Y., Oclarit, J.M. & Omori, T. 1998.
Oxidation of trichloroethylene and dimethyl sulfide by a marine Methylomicrobium strain containing
soluble methane monooxygenase. Bioscience Biotechnology and Biochemistry 62, 1925–1931.
Fuse, H., Osamu, T., Kamimura, K., Murakami, K. & Yamaoka, Y. 1997. Oxidation of dimethyl sulfide by
plant pigments. Journal of Marine Biotechnology 5, 158–161.
Fuse, H., Takimura, O., Murakami, K., Yamaoka, Y. & Omori, T. 2000. Utilization of dimethyl sulfide as a
sulfur source with the aid of light by Marinobacterium sp. strain DMS-S1. Applied and Environmental
Microbiology 66, 5527–5532.
Gibson, J.A.E., Garrick, R.C., Burton, H.R. & McTaggart, A.R. 1990. Dimethylsulfide and the alga Phaeocystis
pouchetii in Antarctic coastal waters. Marine Biology 104, 339–346.
González, J.M., Kiene, R.P. & Moran, M.A. 1999. Transformation of sulfur compounds by an abundant lineage
of the marine bacteria in the a-subclass of the class Proteobacteria. Applied and Environmental

Microbiology 65, 3810–3819.
González, J.M., Simó, R., Massana, R., Covert, J.S., Casamayor, E.O., Pedrós-Alió, C. & Moran, M.A. 2000.
Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic
algal bloom. Applied and Environmental Microbiology 66, 4237–4246.

© 2005 by CRC Press LLC


2727_C02.fm Page 50 Wednesday, June 30, 2004 3:37 PM

50

A. Hatton, L. Darroch & G. Malin

Hanlon, S.P., Holt, R.A., Moore, G.R. & McEwan, A.G. 1994. Isolation and characterisation of a strain of
Rhodobacter sulphidophilus: a bacterium which grows autotrophically with dimethylsulphide as an
electron donor. Microbiology 140, 1953–1958.
Hansen, T.A., Quist, P., van der Maarel, M.J.E.C. & Dijkhuizen, L. 1993. Isolation of marine dimethylfulfideoxidizing bacteria. In Dimethylsulphide: Oceans, Atmosphere and Climate, G. Restelli & G. Angeleth
(eds). London: Kluwer Academic Publishers, pp. 37–41.
Harvey, G.R. & Lang, R.F. 1986. Dimethylsulphoxide and dimethylsulphone in the marine atmosphere.
Geophysical Research Letters 13, 49–51.
Hatton, A.D. 1995. Dimethylsulphoxide in Sea Water. Ph.D. thesis, University of East Anglia, U.K.
Hatton, A.D. 2002a. DMSP removal and DMSO production in sedimenting particulate matter in the northern
North Sea. Deep-Sea Research II 49, 3053–3065.
Hatton, A.D. 2002b. Influence of photochemistry on the cycling of dimethylsulphide in the northern North
Sea. Deep-Sea Research II 49, 3039–3052.
Hatton, A.D., Malin, G. & Liss, P.S. 1999. Distribution of biogenic sulfur compounds during and just after
the southwest monsoon in the Arabian Sea. Deep-Sea Research II 46, 617–632.
Hatton, A.D., Malin, G. & McEwan, A.G. 1994a. Identification of a periplasmic dimethylsulphoxide reductase
in Hyphomicrobium EG grown under chemolithoheterotrophic conditions with dimethylsulphoxide as

carbon source. Archives of Microbiology 162, 148–150.
Hatton, A.D., Malin, G., McEwan, A.G. & Liss, P.S. 1994b. Determination of dimethyl sulfoxide in aqueous
solution by an enzyme-linked method. Analytical Chemistry 66, 4093–4096.
Hatton, A.D., Malin, G., Turner, S.M. & Liss, P.S. 1996. DMSO: a significant compound in the biogeochemical
cycle of DMS. In Biological and Environmental Chemistry of DMSP and Related Sulphonium Compounds, R.P. Kiene et al. (eds). New York: Plenum Press, pp. 405–413.
Hatton, A.D., Turner, S.M., Malin, G. & Liss, P.S. 1998. Dimethylsulphoxide and other biogenic sulfur
compounds in the Galapagos Plume. Deep-Sea Research II 45, 1043–1053.
Hill, R.W., White, B.A., Cottrell, M.T. & Dacey, J.W.H. 1998. Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process. Aquatic Microbial Ecology
14, 1–6.
Holmes, M.E., Sansone, F.J., Rust, T.M. & Popp, B.N. 2000. Methane production, consumption, and air–sea
exchange in the open ocean: an evaluation based on carbon isotope ratios. Global Biogeochemical
Cycles 14, 1–10.
Hooiveld, M.J.J., Roosendaal, G., van den Berg, H.M., Bijlsma, J.W.J. & Lafeber, F.P.J.G. 2003. Haemoglobinderived iron-dependent hydroxyl radical formation in blood-induced joint damage: an in vitro study.
Rheumatology 42, 784–790.
Idso, S.B. 1992. The DMS-cloud albedo feedback effect: greatly underestimated. Climate Change 21, 429–433.
Ishida, Y. 1968. Physiological studies on evolution of dimethylsulphide from unicellular marine algae. Memoirs
of the College of Agriculture, Kyoto University 94, 47–82.
Jonkers, H.M., Koopmans, G.F. & van Gemerden, H. 1998. Dynamics of dimethyl sulfide in a marine microbial
mat. Microbial Ecology 36, 93–100.
Jonkers, H.M., van der Maarel, M.J.E.C., van Gemerden, H. & Hansen, T.A. 1996. Dimethylsulfoxide reduction
by marine sulfate-reducing bacteria. FEMS Microbiology Letters 136, 283–287.
Juliette, L.Y., Hyman, M.R. & Arp, D.J. 1993. Inhibition of ammonia oxidation in Nitrosomonas europaea
by sulfur compounds: thioethers are oxidized to sulfoxides by ammonia monooxygenase. Applied and
Environmental Microbiology 59, 3718–3727.
Kadota, H. & Ishida, Y. 1968. Effects of salts on enzymatical production of DMS from Gyrodinium cohni.
Bulletin of the Japanese Society of Science and Fisheries 34, 512–518.
Kaiser, E. & Herndl, G.J. 1997. Rapid recovery of marine bacterioplankton activity after inhibition by UV
radiation in coastal waters. Applied and Environmental Microbiology 63, 4026–4031.
Karl, D.M. & Tilbrook, B.D. 1994. Production and transport of methane in oceanic particulate organic matter.
Nature 368, 732–734.

Keller, M.D., Bellows, W.K. & Guillard, R.R.L. 1989. Dimethyl sulfide production in marine phytoplankton.
In Biogenic Sulfur in the Environment, E.S. Saltzman & W.J. Cooper (eds). Washington, DC: American
Chemical Society, pp. 167–181.
Kelly, D.P. & Baker, S.C. 1990. The organosulfur cycle: aerobic and anaerobic processes leading to turnover
of C1-sulfur compounds. FEMS Microbiology Reviews 87, 241–246.

© 2005 by CRC Press LLC


2727_C02.fm Page 51 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

51

Kettle, A.J., Andreae, M.O., Amouroux, D., Andreae, T.W., Bates, T.S., Berresheim, H., Bingemer, H.,
Boniforti, R., Curran, M.A.J., DiTullio, G.R., Helas, G., Jones, G.B., Keller, M.D., Kiene, R.P., Leck,
C., Levasseur, M., Malin, G., Maspero, M., Matrai, P., McTaggart, A.R., Mihalopoulos, N., Nguyen,
B.C., Novo, A., Putaud, J.P., Rapsomanikis, S., Roberts, G., Schebeske, G., Sharma, S., Simo, R.,
Staubes, R., Turner, S. & Uher G. 1999. A global database of sea surface dimethylsulfide (DMS)
measurements and a procedure to predict sea surface DMS as a function of latitude, longitude, and
month. Global Biogeochemical Cycles 13, 399–444.
Kieber, D.J., Jiao, J., Kiene, R.P. & Bates, T.S. 1996. Impact of dimethylsulfide photochemistry on methyl
sulfur cycling in the equatorial Pacific Ocean. Journal of Geophysical Research 101 (C2), 3715–3722.
Kiene, R.P. 1992. Dynamics of DMS and DMSP in oceanic water samples. Marine Chemistry 37, 29–52.
Kiene, R.P. 1993. Microbial sources and sinks for methylated sulfur compounds in the marine environment.
In Microbial Growth on C1 Compounds, J.C. Murrell & D.P. Kelly (eds). Andover, U.K.: Intercept
Ltd., pp. 15–33.
Kiene, R.P. 1996. Production of methane thiol from dimethylsulphoniopropionate in marine surface waters.
Marine Chemistry 54, 69–83.

Kiene, R.P. & Bates, T.S. 1990. Biological removal of dimethylsulphide from sea water. Nature 345, 702–705.
Kiene, R.P. & Gerard, G. 1994. Determination of trace levels of dimethylsulfoxide (DMSO) in sea water and
rainwater. Marine Chemistry 47, 1–12.
Kiene, R.P. & Linn, L.J. 2000. The fate of dissolved dimethylsulfoniopropionate (DMSP) in sea water: tracer
studies using 35S-DMSP. Geochimica et Cosmochimica Acta 64, 2797–2810.
Kiene, R.P., Linn, L.J. & Bruton, J.A. 2000. New and important roles for DMSP in marine microbial
communities. Journal of Sea Research 43, 209–224.
Kiene, R.P. & Taylor, B.F. 1988. Demethylation of dimethylsulfoniopropionate and production of thiols in
anoxic marine sediment. Applied and Environmental Microbiology 54, 2208–2212.
Kirst, G.O., Thiel, C., Wolff, H., Nothnagel, J., Wanzek, M. & Kimke, R. 1991. Dimethylsulfoniopropionate
(DMSP) in ice-algae and its possible biological role. Marine Chemistry 35, 381–388.
Koga, S. & Tanaka, H. 1993. Numerical study of the oxidation processes of DMS in the marine atmosphere.
Journal of Atmospheric Chemistry 17, 201–228.
Kwint, R.L.J., Irigoien, X. & Kramer, K.J.M. 1996. Copepods and DMSP. In Biological and Environmental
Chemistry of DMSP and Related Sulphonium Compounds, R.P. Kiene et al. (eds). New York: Plenum
Press, pp. 239–252.
Lara, R.J., Hubberten, U. & Kattner, G. 1993. Contribution of humic substances to the dissolved nitrogen
pool in the Greenland Sea. Marine Chemistry 41, 327–336.
Leck, C., Larsson, U., Bagander, L.E., Johansson, S. & Hadju, S. 1990. DMS in the Baltic Sea: annual
variability in relation to biological activity. Journal of Geophysical Research 95, 3353–3363.
Ledyard, K.M. & Dacey, J.W.H. 1994. Dimethylsulfide production from dimethylsulfoniopropionate by a
marine bacterium. Marine Ecology Progress Series 110, 95–103.
Ledyard, K.M. & Dacey, J.W.H. 1996. Microbial cycling of DMSP and DMS in coastal and oligotrophic sea
water. Limnology and Oceanography 41, 33–40.
Lee, P.A. & de Mora, S.J. 1996. DMSP, DMS and DMSO concentrations and temporal trends in marine
surface waters at Leigh, New Zealand. In Biological and Environmental Chemistry of DMSP and
Related Sulphonium Compounds, R.P. Kiene et al. (eds). New York: Plenum Press, pp. 391–413.
Lee, P.A. & de Mora, S.J. 1999. Intracellular dimethylsulfoxide (DMSO) in unicellular marine algae: speculations on its origin and possible biological role. Journal of Phycology 35, 8–18.
Lee, P.A., de Mora, S.J., Gosselin, M., Levasseur, M., Bouillon, R., Nozais, C. & Michel, C. 2001. Particulate
dimethylsulfoxide in Arctic sea-ice algal communities: the cryoprotection hypothesis revisited. Journal

of Phycology 37, 488–499.
Lee, P.A., de Mora, S.J. & Levasseur, M. 1999b. A review of dimethylsulfoxide in aquatic environments.
Atmosphere-Ocean 37, 439–456.
Lee, P.A., Haase, S.J., de Mora, S.J., Chanut, J.P. & Gosselin, M. 1999a. Dimethylsulfoxide (DMSO) and
related sulfur compounds in the Saguenay Fjord, Québec. Canadian Journal of Fisheries and Aquatic
Science 56, 1631–1638.
Liss, P.S., Malin, G. & Turner, S.M. 1993. Production of DMS by marine phytoplankton. In Dimethylsulphide:
Oceans, Atmosphere and Climate, G. Restelli & G. Angeletti (eds). London: Kluwer Academic
Publications, pp. 1–14.

© 2005 by CRC Press LLC


2727_C02.fm Page 52 Wednesday, June 30, 2004 3:37 PM

52

A. Hatton, L. Darroch & G. Malin

Liss, P.S. & Merlivat, L. 1986. Air–sea gas exchange rates: introduction and synthesis. In The Role of Air–Sea
Exchange in Geochemical Cycling, P. Buat Menard (ed.). Dordrecht: Reidel, pp. 113–127.
Liss, P.S. & Slater, P.G. 1974. Flux of gases across the air–sea interface. Nature 247, 181–184.
Liu, J., Zieger, M.A.T., Lakey, J.R.T., Woods, E. & Critser, J.K. 1997. Water and DMSO permeability at 22˚C,
5˚C and –3˚C for human pancreatic islet cells. Transplant Proceedings 29, 1987.
Lovelock, J.E., Maggs, R.J. & Rasmussen, R.A. 1972. Atmospheric dimethyl sulphide and the natural sulfur
cycle. Nature 237, 452–453.
Malin, G. 1996. The role of DMSP and DMS in the global sulfur cycle and climate regulation. In Biological
and Environmental Chemistry of DMSP and Related Sulphonium Compounds, R.P. Kiene et al. (eds).
New York: Plenum Press, pp. 177–190.
Malin, G., Liss, P.S. & Turner, S.M. 1994. Dimethylsulfide: production and atmospheric consequences. In

The Haptophyte Algae, J.C. Green & B.S.C. Leadbeater (eds). Oxford: Clarendon Press, pp. 303–320.
Malin, G., Turner, S.M. & Liss, P.S. 1992. Sulphur: the plankton/climate connection. Journal of Phycology
28, 590–597.
Malin, G., Turner, S.M., Liss, P.S., Holligan, P. & Harbour, D. 1993. Dimethylsulphide and dimethylsulphoniopropionate in the Northeast Atlantic during the summer coccolithophore bloom. Deep-Sea Research
40, 1487–1508.
Malin, G., Wilson, W.H., Bratbak, G., Liss, P.S. & Mann, N.H. 1998. Elevated production of dimethylsulfide
resulting from viral infection of cultures of Phaeocystis pouchetii. Limnology and Oceanography 43,
1389–1393.
Marty, D.G. 1993. Methanogenic bacteria in sea water. Limnology and Oceanography 38, 452–456.
McDiarmid, R. 1974. Assignment of Rydberg and valence transitions in the electronic spectrum of dimethylsulphide. Journal of Physical Chemistry 61, 274–281.
McEwan, A.G., Benson, N., Bonnett, T.C., Hanlon, S.P., Ferguson, S.J., Richardson, D.J. & Jackson, J.B.
1991a. Bacterial dimethylsulphoxide reductases and nitrate reductases. Respiratory Electron Transfer
Complexes 19, 605–608.
McEwan, A.G., Ferguson, S.J. & Jackson, J.B. 1991b. Purification and properties of dimethylsulphoxide
reductase from Rhodobacter capsulatus. Biochemistry Journal 274, 305–307.
McEwan, A.G., Wetzstein, H.G., Ferguson, S.J. & Jackson, J.B. 1985. Periplasmic location of the terminal
reductase in trimethylamine-N-oxide and dimethylsulphoxide respiration in the photosynthetic bacterium Rhodopseudomonas capsulata. Biochimica Biophysica Acta 806, 410–417.
McEwan, A.G., Wetzstein, H.G., Meyer, O., Jackson, J.B. & Ferguson, S.J. 1987. The periplasmic nitrate
reductase of Rhodobacter capsulatus; purification, characterisation and distinction from a single
reductase for trimethylamine-N-oxide, dimethylsulphoxide, and chlorate. Archives of Microbiology
147, 340–345.
Nightingale, P.D., Malin, G., Law, C.S., Watson, A.J., Liddicoat, M.I., Boutin, J. & Upstillgoddard, R.C. 2000.
In situ evaluation of air–sea gas exchange parameterizations using novel conservative and volatile
tracers. Global Biogeochemical Cycles 14, 373–387.
Ogata, M. & Fujii, T. 1979. Quantitative determination of urinary dimethylsulfoxide and dimethylsulfone by
a gas chromatograph equipped with a flame photometric detector. Industrial Health 17, 73–78.
Palenik, B., Zafiriou, O.C. & Morel, F.M.M. 1987. Hydrogen peroxide production by a marine phytoplankter.
Limnology and Oceanography 32, 1365–1369.
Paulin, H.J., Murphy, J.B. & Larson, R.E. 1966. Determination of dimethylsulfoxide in plasma and cerebrospinal fluid by gas liquid chromatography. Analytical Chemistry 38, 651–652.
Pearson, T.W., Dawson, H.J. & Lackey, H.B. 1981. Natural occurring levels of dimethyl sulphoxide in selected

fruits, vegetables, grains and beverages. Journal of Agriculture and Food Chemistry 29, 1089–1091.
Plane, J.M.C. 1989. Gas-phase atmospheric oxidation of biogenic sulfur compounds: a review. In Biogenic
Sulfur in the Environment, E.S. Saltzman & W.J. Cooper (eds). Washington, DC: American Chemical
Society, pp. 404–423.
Richards, S.R., Rudd, J.W.M. & Kelly, C.A. 1994. Organic volatile sulfur in lakes ranging in sulfate and
dissolved salt concentration over 5 orders of magnitude. Limnology and Oceanography 39, 562–572.
Richardson, D.J., King, G.F., Kelly, D.J., McEwan, A.G., Ferguson, S.J. & Jackson, J.B. 1988. The role of
auxiliary oxidants in maintaining redox balance during phototrophic growth of R. capsulatus on
propionate or butyrate. Archives of Microbiology 150, 131–137.

© 2005 by CRC Press LLC


2727_C02.fm Page 53 Wednesday, June 30, 2004 3:37 PM

The Role of Dimethylsulphoxide in the Marine Biogeochemical Cycle of Dimethylsulphide

53

Ridgeway, R.G., Thornton, D.C. & Bandy, A.R. 1992. Determination of trace aqueous dimethylsulfoxide
concentrations by isotope dilution gas chromatography/mass spectrometry: application to rain and sea
water. Journal of Atmospheric Chemistry 14, 53–60.
Robbins, M.D. 1961. Pulp plant wrings profit from lignin. Chemical Engineering 68, 100–102.
Schwartz, S.E. 1988. Are global cloud albedo and climate controlled by marine phytoplankton? Nature 336,
441–445.
Sciare, J., Baboukas, E., Hancy, R., Mihalopoulos, N. & Nguyen, B.C. 1998. Seasonal variation of dimethylsulphoxide in rainwater at Amsterdam island in the southern Indian Ocean: implications on the
biogenic sulfur cycle. Journal of Atmospheric Chemistry 30, 229–240.
Sciare, J. & Mihalopoulos, N. 2000. A new technique for sampling and analysis of atmospheric dimethylsulfoxide (DMSO). Atmospheric Environment 34, 151–156.
Shimoda, K., Nomura, M. & Kato, M. 1996. Effect of antioxidants, anti-inflammatory drugs, and histamine
antagonists on sparfloxacin-induced phototoxicity in mice. Fundamental and Applied Toxicology 31,

133–140.
Shooter, D. & Brimblecombe, P. 1989. Dimethylsulphide oxidation in the ocean. Deep-Sea Research 36,
577–585.
Simó, R. 2001. Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends in Ecology and Evolution 16, 287–294.
Simó, R., Grimalt, J.O. & Albaigés, J. 1996. Sequential method for the field determination of nanomolar
concentrations of dimethyl sulfoxide in natural waters. Analytical Chemistry 1996, 1493–1498.
Simó, R., Grimalt, J.O. & Albaigés, J. 1997. Dissolved dimethylsulphide, dimethylsulphoniopropionate and
dimethylsulphoxide in western Mediterranean waters. Deep-Sea Research II 44, 929–950.
Simó, R., Grimalt, J.O., Pedrosalio, C. & Albaigés, J. 1995. Occurrence and transformation of dissolved
dimethyl sulfur species in stratified sea water (western Mediterranean Sea). Marine Ecology Progress
Series 127, 291–299.
Simó, R., Hatton, A.D., Malin, G. & Liss, P.S. 1998a. Particulate dimethyl sulphoxide in sea water: production
by microplankton. Marine Ecology Progress Series 167, 291–296.
Simó, R., Malin, G. & Liss, P.S. 1998b. Refinement of the borohydride reduction method for trace analysis
of dissolved and particulate dimethyl sulfoxide in marine water samples. Analytical Chemistry 70,
4864–4867.
Simó, R., Pedrós-Alió, C., Malin, G. & Grimalt, J.O. 2000. Biological turnover of DMS, DMSP and DMSO
in contrasting open-sea waters. Marine Ecology Progress Series 203, 1–11.
Stefels, J. 2000. Physiological aspects of the production and conversion of DMSP in marine algae and higher
plants. Journal of Sea Research 43, 183–197.
Stefels, J., Gieskes, W.W.C. & Dijkhuizen, L. 1996. Intriguing functionality of the production and conversion
of DMSP in Phaeocystis sp. In Biological and Environmental Chemistry of DMSP and Related
Sulphonium Compounds, R.P. Kiene et al. (eds). New York: Plenum Press, pp. 305–316.
Steinke, M., Malin, G., Gibb, S.W. & Burkill, P.H. 2002. Vertical and temporal variability of DMSP lyase
activity in a coccolithophorid bloom in the northern North Sea. Deep-Sea Research II 49, 3001–3016.
Sunda, W., Kieber, D.J., Kiene, R.P. & Huntsman, S. 2002. An antioxidant function for DMSP and DMS in
marine algae. Nature 418, 317–320.
Suylen, G.M.H. 1988. Microbial Metabolism of Dimethyl Sulphide and Related Compounds. Ph.D. thesis,
University of Delft, The Netherlands.
Suylen, G.M.H., Stefess, G.C. & Kuenen, J.G. 1986. Chemolithotrophic potential of a Hyphomicrobium

species, capable of growth on methylated sulfur compounds. Archives Microbiology 146, 192–198.
Tang, K.W., Dam, H.G., Visscher, P.T. & Fenn, T.D. 1999. Dimethylsulphoniopropionate (DMSP) in marine
copepods and its relation with diets and salinity. Marine Ecology Progress Series 179, 71–79.
Tang, K.W., Fenn, T.D., Visscher, P.T. & Dam, H.G. 2000. Regulation of body dimethylsulphoniopropionate
(DMSP) content by the copepod Temora longicornis: a test of four mechanisms. Marine Biology 136,
749–757.
Tang, K.W., Visscher, P.T. & Dam, H.G. 2001. DMSP-consuming bacteria associated with the calanoid copepod
Acartia tonsa (Dana). Journal of Experimental Marine Biology and Ecology 256, 185–198.
Taylor, B.F. 1993. Bacterial transformations of organic sulfur compounds in marine environments. In Biogeochemistry of Global Change: Radiatively Active Trace Gases, R. Oremland (ed.). New York:
Chapman & Hall, pp. 745–781.

© 2005 by CRC Press LLC