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Geochrmrca n Cosmochrmrca Acla Vol. 51, pp. 1675-1684
0 Pergamon Journals Ltd. 1987. Rinted m U.S.A. rml6-7037/87~3.00 + .m
Biogeochemistry of dimethylsulfide in a seasonally stratified coastal salt pond
S. G. WAKEHAM*, B. L. HOWES and J. W. H. DACEY
Woods Hole Oceanographic Institution, Woods Hole, MA 02543 U.S.A.
and
R. P. SCHWARZENBACH and J. ZEYER
Swiss Federal Institute for Water Resources and Water Pollution Control (EAWAG), CH-8600 Diihendorf, Switzerland
(Received November 6, 1986; accepted in revisedform March 23, 1987)
Abstract-Dimethylsulfide (DMS) is the major volatile reduced organic sulfur compound in the water
column of coastal Salt Pond, Cape Cod, MA. DMS concentration and vertical distributions vary seasonally
in response to changing biogeochemical processes in the pond. When the pond is thermally stratified in
summer, maximum DMS concentrations of up to 60 nmol/l were found in the oxygen-deficient metalimnion.
DMS concentrations in the epilimnion (typically 5-10 nmol/l) were always an order of magnitude higher
than in the hypolimnion (~0.2 nmol/l). The most likely precursor for DMS is algal dimethylsulfoniopro
pionate (DMSP), which showed vertical profiles similar to those of DMS. Laboratory experiments show that
microorganisms in the pond, especially in the metalimnion, are capable of decomposing DMSP to DMS,
while photosynthetic sulfur bacteria in the hypolimnion can consume DMS. Estimates of DMS production
and consumption in Salt Pond have been made, considering production of DMS in the epilimnion and
metalimnion and removal of DMS via gas exchange to the atmosphere, tidal exchange, and microbial
consumption in the hypolimnion.
INTRODUCTION
DIMETHYLSULFIDE (DMS) is ubiquitous in the surface
waters of the ocean where it is always present in sig-
nificantly higher concentrations than expected from
equilibrium with the atmosphere (LOVELOCK et al.,
1972; ANDREAE and RAEMDONCK, 1983; NGUYEN et
al., 1983; CLINE~~~ BATES, 1983; FEREK~~ al., 1986).
This large concentration gradient between oceans and
the atmosphere drives a DMS flux equal to almost half
of the biogenic sulfur flux to the earth’s atmosphere
(ANDREAE, 1985a, 1986; BATES et al., 1987). DMS
constitutes about 90% of the tlux of biogenic sulfur
from the ocean to the atmosphere, and on a global
scale, the oceanic DMS flux approaches anthropogenic
SO1 emissions. Considerable attention has therefore
focussed on the distribution and dynamics of DMS in
seawater in an effort to understand the mechanisms
controlling its flux to the atmosphere.
The most likely biogenic precursor of DMS in sea-
water is the algal natural product, dimethylsulfonio-
propionate (DMSP or dimethylpropiothetin, DMPT;
CHALLENGER et al., 1957; ACKMAN et al., 1966;
WHITE, 1982; VA~RAVAMURTHY et al., 1985). Enzy-
matic cleavage of DMSP yields DMS and acrylic acid
(CANTONI and ANDERSON, 1956). DMSP is a tertiary
sulfonium compound which, like quaternary ammo-
nium compounds (e.g. glycinebetaine), may be in-
volved in regulating cellular osmotic pressure in algae
and higher plants (DICKSON et al., 1980; VAIRAVA-
MURTHY et al., 1985). Many marine algae release DMS
and dimethylsulfoxide (DMSO) (CHALLENGER et al.,
* Present address: Skidaway Institute ofOceanography, P.O.
Box 13687, Savannah, GA 31416, U.S.A.
1957; ANDREAE, 1980a; VAIRAVAMURTHY et al..
1985) although the reasons for such release are poorly
understood. Algal DMSP content and DMS/DMSO
release vary greatly depending on species (ACKMAN et
al., 1966; ANDREAE, 1980a; WHITE, 1982; BARNARD
et al., 1984). However, a correspondence between
phytoplankton abundance and seawater DMS and
DMSO concentrations has been observed (CLINE and
BATES, 1983; ANDREAE and BARNARD, 1984; BAR-
NARD et al., 1984; LEE and WAKEHAM, 1987). DMS
release by marine phytoplankton is greatly increased
when the phytoplankton are subjected to zooplankton
grazing (DACEY and WAKEHAM, 1986) possibly due
to DMSP cleavage during cell disruption, breakdown
within the gut of the animals, or microbial breakdown
in their feces. In some marine settings, DMS produc-
tion associated with such grazing may be. the dominant
mechanism of DMS release. Bacterial decomposition
of sulfur-containing organic matter presents yet another
source of DMS (WAGNER and STADTMAN, 1962; KA-
DOTA and ISHIDA, 1972; ZINDER et al., 1977; ZINDER
and BROCK, 1978a,b; WAKEHAM et al.. 1984; AN-
DREAE, 1985b). Microbial decomposition may also be
a sink for DMS (ZINDER and BROCK, 1978~; WAKE-
HAM et al., 1984; KIENE et al., 1986; ZEYER et al., 1987)
and interconversion between DMS and DMSO in sea-
water has also been postulated (ANDREAE, 1980a), but
has yet to be demonstrated.
We have been investigating the biogeochemistry of
DMS in a seasonally stratified coastal salt pond, with
emphasis on the biogeochemical processes responsible
for production and removal of DMS in coastal seawater
(WAKEHAM et al., 1984). The hypolimnion of the pond
is anoxic during summer stratification and DMS con-
centrations are greatest in the oxygen-depleted meta-
1675
1676 S. G. Wakeham et al.
limnion. To better understand the biogeochemical
processes associated with DMS distributions in the
marine environment, we have dekrmined the seasonal
distributions of DMS in the water column of the pond
over several years. These observations have been cou-
pled with simultaneous measurements of DM!30 and
dissolved and particulate DMSP, chlorophyll a and
bacterial chlorophylls, water column geochemistry, and
laboratory microbial culture experiments.
SAMPLING AND METHODS
Salt Pond is a shallow (5.5 m deep) eutrophic marine basin
on Cape Cd Massachusetts that exhibits density ,qratification.
While aerobic proa3ses dominate the epilimnion, the anaer-
obic hypolimnion generally has high concentrations of HzS
(up lo 5 mM in summer) generated from sulfate reduction in
the bottom waters and sediments. In summer the anoxic zone
rises to within 2-3 m of the pond surface, and steep bioge+
chemical gradients develop across the oxic/anoxic interface.
During winter, the deptb of the oxic/anoxic interface deepens
and H2S concentrations decrease as a result of wind-driven
mixing; occasionally the water column overturns.
Sampling. DMS coMxlltrations were measured in the water
column of salt Pond between June 1982 and July 1983, and
again between May and August of 1985. Water samples were
collected along a vertical profile in the central basin of the
pond using a battery-operated per<ic pump and a weighted
silicon rubber tube lowered by a graduated fiberglass tape se-
quentially to the appropriate sampling depths. Glass sample
bottles (2 I) wen rinsed, l&d and capped with ground-glass
stoppers without headspace and held in the dark at approxi-
mately ambient temperatures. Water samples were returned
to the laboratory within 1 h of collection and weIc gently
syringe-filtered without headspace to reduce loss of DMS by
volatilization through in-line glass fiber (I pm nominal) and
0.22 pm membrane filters to remove algal cells and baaeria.
Filtration is a necc~sary step, since agitation of algal cells during
subsequent sparging analysis can result in release of DMS
from damaged cells; on the other hand, care must be taken
during filtration to minimize DMS release. via cell lysis.
Temperature, salinity (temperature compensated ret&-
tometer), pH (glass electrode), Eh (polished platinum elec-
trode) and pS*- (electrode after BERNER, 1963) were measured
in pond water pumped through an in-line flow chamber as
samples for DMS were being collected. The vertical profile of
dissolved oxygen was determined by lowering a temperature
and pressurecompensated Clark-type O2 electrode through
the water column just into the anoxic zone. Oxygen mea-
surements were corrected for salinity.
St&r spdes analysis. DMS and other volatile components
were collected from waters&samples (25-100 ml) by sparging
at room temperature for 20 min. with helium. Water vapor
was removed from the gas stream by passing it through one
meter of Nafion (Dupont) tubing coiled in a plastic box con-
taining anhydrous &SO,. Volatile components were cry-
ogenically trapped in a 25-cm Teflon U-tube filled with sily-
lated glass beads and immersed in liquid N1. The trapped
components were then thermally desorbed ( 100°C) From the
glass beads to a gas chromatographic column for subsequent
separation. Samples were analyzed in 1982-83 using a 50 m
X 0.3 mm id. glass capillary coated with Pluronic 121 with
cryofocussing (LN& during transfer and in 1985 with a 2 m
teflon column packed with Chromosil3 10 (Supetco). Sulfur-
containing compounds were detected with a flame photomet&!
detector (Tracer FPD). During 1982-83, thiophene was added
to samples before spafging as an internal standard and con-
centrations were corrected for 85% + 10% recovm for s+rging
and GC analysis In 1985, DMS concentrations wen calculated
relative to calibration curves determined by complete analysis
(spargin& trapping GC analysis) of standard solutions. The
detection limit was 0.1 ng S (DMS) and precision was 10%.
High concentrations of H&j interfere with our DMS assay.
HIS was removed from water samples in 1982-83 by precig
itation with HgCl,. Although a comparison of treated and
untreated samples from the epilimnion showed no loss of
DMS, the possibility that some fraction of the DMS might
coprecipitate with HIS from samples from the anoxic hypo-
limnion could not be ruled out. Subsequent experiments
showed that up to 50% of the DMS added to sulfidic samples
might be removed upon addition of HgC&. However, this
does not significantly change the profiles reported previously
(WAKEHAM er al., 1984) or below. Even after correcting for
a maximum possible loss (50%), DMS concentrations in an-
oxic waters remain very low compared lo oxic waters. This
problem was avoided during 1985 runs by stripping the HIS
from the gas stream using a NaOH trap upstream of the glass
bead trap. DMS was not affected by this procedure.
DMSP was determined in Salt Pond during 1985. Analysis
was based on the alkaline (pH 13) cleavage of DMSP to equi-
molar amounts of DMS and acrylic acid (ACKMAN et al..
1966) and subsequent measurements of DMS. Particulate
DMSP was measured on material collected on the glass fiber
and membrane filters used in the DMS analyses. The filters
were treated with base in sealed silylated glass test tubes with
Teflon-faced stoppers, allowed to mact overnight at room
temperature, and DMS released was measured by GC-FPD
analysis of the headspace. DMS concentrations in solution
were calculated using Bunsen coefficients for the alkaline so-
lutions as well as standards prepared from authentic DMSP
(Research Plus). Water column concentrations of dissolved
(free) DMSP were estimated during only the 27 August, 1985,
sampling. Water samples which had been filtered, sparged,
and analyzed for DMS were subsequently treated with base
(pH 13) and reas~yed for DMS. DMS liberated by base-treat-
ment was assumed to be equivalent to dissolved DMSP, al-
though other sulfonium compounds (e.g. ANDERSON et al..
1976) may also yield DMS upon treatment with base. Mea-
surement of equimolar quantities of acrylic acid would verify
the source of DMS as DMSP, but acrylic acid assays were not
possible in such dilute solutions.
DMSO profiles were measured on several sampling dates
using the borohydride reduction procedure of ANDREAE
(1980b). After a sample of pond water had been sparged and
analyzed for DMS, 0.2 ml of cont. HCI per 25-ml sample and
2 ml of 4% aqueous NaBI& were injected into the closed
stripper. The DMS released by the reduction of DMSO was
sparged and measured by GC-FPD, and concentrations cal-
culated relative to DMSO standards.
Pigmenfs. Photosynthetic pigments were determined on
parallel 750 ml and 250 ml subsamples filtered by A/E glass
fiber (47 mm) and Millipore 0.22 lrn (47 mm) filters, respec-
tively. Filters were extracted in IO ml cold 90% acetone (24
hours) and scanned (360-850 nm) on a Bausch & Lomb
Spectronic 2000 spectrophotometer using a I cm path length.
Since samples in the aerobic epilimnion never indicated de-
tectable bacterial chlorophylls, Chla, b and c were calculated
using trichromatic equations of JEFFREY and HUMPHREY
(1975). Chlorophyll a was corrected for phaeopigments by
addition of acid (2 N HCI) (PARSONS ef al., 1984).
The dominant bacterial chlorophyll was identified as BChld
using both the absorption spectm together with HPLC analysis.
BChld was calculated using the extinction coefficient of TAK-
AHASHI and kHIMUrU (1970). Chla and BChld values were
comected for cross interference using data from field samples
where only one was present. The correction determined for
the contribution of BChld absorbance to “Chla absorbance”
agreed closely with that calculated from solutions of purified
BChld from green sulfur Lmc@ia (GLOE et al.. 1975).
Geochemical analyses. Sulfate and sulfide measurements
were made in the laboratory on samples filtered and preserved
in the field. Water samples for ti,- analysis were injected
into gas-tight tubes with an argon head space and containing
Dimethylsulfide in a coastal salt pond 167-l
a CdClr solution to a final concentration of 35 mM. Samples
were held in the dark and upon returning to the laboratory
held at 5°C until analysis. Sulfate was determined by a mod-
ification of the barium precipitation technique of TABATABAI
(1974). Water samples for S*- were collected directly in syringes
and reacted with S*- reagents in the field, held in the dark,
and analyzed using the method of CLINE (1969). Methane
was measured by flame ionization gas chromatography on
samples obtained by headspace equilibration of 5 ml aliquots
of pond water which had been injected into gas tight 25-ml
serum bottles in the field. Suspended particulate organic car-
bon (POC) concentrations were determined by CHN analysis
of particles obtained by filtration onto precombusted glass
fiber filters (Gelman A/E). Light transmission was estimated
in 1985 by Secchi disk and ranged from 2.7 m in winter to
I .4 m in summer.
Biological turnover of DMSP to DMS. Water samples (40
ml) collected on July 26, 1985 in Salt Pond on a depth profile
and from a coastal site at Woods Hole were placed in glass
flasks (57 ml) sealed with butyl rubber stoppers; loss of DMS
to the stoppers was determined to be minimal in this study.
Two additional samples each from 2.5 and 3 m depth in the
pond were filter-sterilized (0.22 pm filter) and two other sets
of samples from the same depths were autoclaved. DMSP (0.5
mmol/ I) was then added to all samples and they were incu-
bated for 4 days at 22” under a headspace of air or N2:C02
(90: 10) in both the light and in the dark. The headspace was
periodically analyzed for the appearance of DMS by GC with
flame ionization detector (RD). Conversion of DMSP to DMS
was estimated by comparison with DMS standards prepared
by chemical conversion (pH 13) of synthetic DMSP to DMS.
Media and culture conditions for DMS metabolism by an-
aerobicphototrophic bacteria. Anaerobic marine basal medium
was prepared according to techniques described by WIDDEL
and PEENNIG (198 I) and WIDDEL et al. (1983). The compo-
sition of the medium was (g/l distilled HzO): KH,PO,: 0.20;
NHICI: 0.25; NaCI: 30.0; MgClz *6HrO: 0.20; KCI: 0.50,
CaC12. 2HzO: 0.15: NaHCOr: 2.52; trace element solution
SLIO: 0.5 ml/l; vitamin solution: 1.0 ml/l. The pH of the
medium was adjusted to 7.2-7.3 and the medium was sup
plemented, as discussed below, with sulfide from a 0.5 M
Na2S - 9H2G stock solution previously neutralized with HCI,
acetate from a I .O M sodium acetate stock solution, and DMS
from a 0.1 M stock solution. Cultures were incubated without
agitation at 20°C under strict anaerobic conditions in 57-ml
glass flasks with butyl rubber stoppers. Each flask contained
50 ml of culture and 7 ml of a N2:C02 (90~10) headspace.
The cultures were illuminated with a light intensity of 7-12
FE/m’ set, unless indicated otherwise below. DMS in the
headspace was monitored by GC/PID analysis.
RESULTS AND DISCUSSION
Sulfur species distributions. DMS is the most abun-
dant volatile reduced organic sulfur compound in the
water column of Salt Pond, as it is in open ocean sea-
water. Carbonyl sulfide, methyl mercaptan, carbon di-
sulfide, and dimethyl disulfide accounted for less than
10% of the volatile sulfur compounds and except for
CS2 in the anoxic hypolimnion were not rigorously
quantified. The range of DMS concentrations (0.2-60
nmol/l; Fig. 1) was considerably wider than concen-
trations typically observed in open ocean waters (0.5-
10 nmol/l; BARNARD et al., 1982, ANDREAE and
RAEMDONCK, 1983; CLINE and BATES, 1983; BAR-
NARD et al., 1984; ANDREAE and BARNARD, 1984;
BATES and CLINE, 1985; ANDREAE, 1985b), probably
due to the diverse chemical environment of the pond.
Oceanic DMS profiles often show near-surface con-
centration maxima, usually attributed to release of
DMS by phytoplankton, comparable to the 2- 10 nmol/
1 present year-round in the epilimnion of Salt Pond.
The highest levels in the pond (40-60 nmol/l in the
metalimnion) are similar to surface water concentra-
tions observed in highly productive coastal areas off
Brazil (ANDREAEand BARNARD, 1984) and in the Peru
upwelling (ANDREAE, 1985b).
Concentration and depth distributions of DMS in
Salt Pond varied seasonally (Figs. 1 and 2). During
periods when the water column was well mixed (winter
and early spring), maximum concentrations were gen-
erally found in the O-2 m depth interval. As bottom
waters became anoxic in summer, however, the max-
imum DMS concentrations were found just above the
oxic/anoxic boundary. During seasonal excursions of
the interface depth, the depth of maximum DMS con-
centration shifted accordingly (Fig. I and WAREHAM
et al., 1984). During one sampling (26 April, 1983)
two DMS peaks may have been present, one at 1 m
within the well mixed epilimnion and a second at about
5 m, just above a mildly anoxic zone. If the profile is
real, then this sampling might represent a transition
between winter mixing and summer stratification.
DMS concentrations in the anoxic bottom waters were
never greater than a few tenths of nmol/l.
During stratification, DMS concentration maxima
actually lie within the metalimnion (Fig. 2), where dis-
solved oxygen concentrations were ~0.2 mg Oz/l but
where HzS was not yet detectable (< 1 pmol/l). During
late summer, it was common for the metalimnion to
FIG. 1. DMS profiles (nmol/l) in Salt Pond. Note that the concentration scale is variable. The dotted line
indicates the depth below which H2S was detected. H2S was not detected in the pond on 14 May, 1985.
1678 S. G. Wakeham et al.
POC lmg/IJ
AWUST 27.1985
PIG. 2. Salt Pond water column profiles on 14 May 1985 (mixed water column) and 27 August 1985
(stratified water column). Bacterial chlorophyll on 27 August is primarily Bchld. Ekhld was not detected in
May.
thicken (as indicated by oxygen concentrations < 0.2
mg/l and H2S concentrations < 1 rmolll; Fig. 2) to
nearly 50 cm (August, 1985, Fig. 2; see also Fig. 2 of
WAKEHAM et al., 1984). When this occurred, the depth
of the maximum DMS concentration corresponded to
the depth interval of the steepest 02 gradient and was
significantly shallower than the depth at which sulfide
was detected. We also observed that the DMS peak
lies above the maximum concentrations of POC, chlo-
rophyll a and green sulfur bacterial pigment (BChld).
Both POC and BChld profiles reflect the increased
abundance of anaerobic phototrophic bacteria (pho-
tosynthetic bacterial plate) at the top of the hypolim-
nion (see below). The presence of a metalimnion with
undetectable O2 and HrS and coincident with a BChld
maximum is similar to observations of PARKIN and
BROCK (1981) and SMITH and OREMLAND (1987) in
meromictic lakes.
Particulate DMSP was measured before and after
stratification in 1985. Maximum concentrations, up
to 80 nmol/l, were always found within the 2-3 m
depth interval (Fig. 2). There was little correspondence
between particulate DMSP and POC and chlorophyll
distributions, but particulate DMSP was most abun-
dant at densities of 0, = 2 l-22. We consistently ob-
served that when concentration peaks for both DMSP
and DMS were present, there was a slight depth-offset,
with the DMS peak being slightly shallower (e.g. Fig.
2). We speculate that the fine structure for the partic-
ulate DMSP profile in August, 1985, might be due to
separate DMSP-bearing phytoplankton species which
reside at specific densities within the metalimnion. It
may be, however, that the major DMSP-producing
species are relatively minor contributors to the total
phytoplankton biomass in the pond. A distinctly bi-
modal DMSP profile was also observed on 16 July,
1985, with concentrations of about 90 and 120 nmoi/
1 at 3.13 and 3.38 m, respectively.
A vertical profile of dissolved DMSP was obtained
in August, 1985 (Fig. 2). The highest dissolved DMSP
concentration ( 18 nmol/l) was found at the pond sur-
face, and concentrations decreased steadily with in-
creasing depth in the water column. Dissolved DMSP
appeared to be uncoupled from particulate DMSP,
since no significant increase in dissolved DMSP was
found corresponding to the pronounced increase in
particulate DMSP observed in the metahmnion. A
similar difference in dissolved and particulate DMSP
profiles was found in the Cariaco Trench (LEE and
WAKEHAM, 1987). In the Cariaco Trench, the dissolved
Dimethylsulfide in a coastal salt pond 1679
DMSP concentration was highest (5 nmol/l) at the sea
surface, while particulate DMSP showed a strong con-
centration peak (4 nmol/l) at 40 m depth, roughly cor-
responding to the chlorophyll a maximum at 45 m.
This was in contrast to the DMS profile which exhibited
a broad maximum from IO-40 m with a maximum
concentration of 3 nmol/l. There was no apparent pro-
duction of DMS associated with the oxic/anoxic in-
terface at 275 m. Thus, in contrast to Salt Pond, DMS
and particulate DMSP profiles in the Cariaco Trench
(and probably other open ocean regions as well) do
correspond to algal biomass as indicated by Chl a. In
both environments the differences in the depth distri-
butions of DMS and particulate DMSP compared to
dissolved DMSP are taken as evidence that cell rupture
and production of free DMSP and DMS during anal-
ysis was minimal.
Depth profiles of DMSO generally tracked DMS;
Fig. 3 shows the DMSO profile in August, 1985. That
profile was strongly bimodal, with concentration max-
ima at 1 m in the epilimnion and at 3 m in the me-
talimnion. Furthermore, the concentration range was
similar to that of the DMS (5-20 nmolfl), and similar
profiles and concentration ranges were observed in all
samplings (n = 4) for which we have comparable DMS
and DMSO data. Thus, we did not find the order of
magnitude greater DMSO concentrations relative to
DMS as has been suggested previously for seawater
(ANDREAE, 1980a,c) and has been observed for some
algal cultures (ANDREAE et al., 1983; DACEY and
WAKEHAM, unpublished results). Our DMSO values
must be considered upper limits. The borohydride re-
duction procedure used will reduce both DMSO and
DMSP (ANDREAE, 1980b). Nevertheless, qualitative
and quantitive differences in DMSO and DMSP pro-
FIG. 3. DMS, DMSO, and CSz profiles in Salt Pond on 27
August 1985. The dotted lines indicate the interval between
which dissolved O2 concentrations were t2 mgJ1 and H2S
concentrations began to increase (see Fig. 2).
files suggest that at least the general nature of the
DMSO profiles are real and not analytical artifacts (i.e.
a contribution from DMSP to the l-m DMSO peak is
possible, but for the 3-m DMSO peak an artifact due
to DMSP conversion is unlikely).
DMS, DMSP and DMSO sources in Salt Pond. Ver-
tical profiles in Salt Pond suggest two sources for DMS
and DMSO. DMS and DMSO in the epilimnion might
result from direct release of phytoplankton. The im-
portance of marine phytoplankton as a source of DMS
and DMSO has been pointed out by Andreae and co-
workers who showed oceanic DMS and DMSO con-
centrations to be related to levels of marine primary
production (ANDREAE, 1980a.c; ANDREAE and
RAEMDONCK, 1983; ANDREAE and BARNARD, 1984).
Release of DMS and DMSO by phytoplankton and
macroalgae has been demonstrated in the laboratory
and varies greatly depending on species; dinoflagellates
and coccolithophorids generally release more DMS and
DMSO than, for example, diatoms (ACKMAN et al.,
1966; ANDREAE, 1980a). Algal DMSP content is also
extremely variable, with order-of-magnitude higher
concentrations (as determined by DMS release upon
alkaline hydrolysis) in Chlorophytes than in either
Phaeophytes or Rhodophytes (WHITE, 1982). In Salt
Pond, there is not a particularly strong correspondence
between DMS, DMSO, DMSP and chlorophyll a pro-
files. Major phytoplankton blooms in Salt Pond do
not seem to result in obvious concurrent peaks in DMS
or DMSO in the epilimnion.
DMS and DMSO maxima in the metalimnion might
also result from direct release by viable phytoplankton
near the Oz-HzS interface. Alternatively, DMS or
DMSO could be released during decomposition of
phytoplankton under conditions of oxygen depletion.
Whether the precursor is exclusively algal DMSP or a
combination of that and other organo-sulfur com-
pounds (e.g. methionine decomposition gives small
amounts of DMS; KADOTA and ISHIDA, 1972) cannot
be resolved at present. However, given the high con-
centrations of DMSP relative to methionine in plank-
ton and that the sub-oxic DMS peaks in the stratified
pond tend to coincide with the DMSP peak, we suggest
that decomposition of DMSP is the major source of
DMS. The results of incubations of microorganisms
from the pond with DMSP demonstrate that produc-
tion of DMS from DMSP can occur rapidly and may
become more important as depth increases into the
metalimnion (see below). Production of DMSO during
algal decomposition has not to our knowledge been
demonstrated. An axenic culture of the marine coc-
colithophorid Coccolithus huxleyi did, however, pro-
duce more DMSO than did a bacteria-containing cul-
ture (ANDREAE, 1980a), so that bacterial decomposi-
tion is not a necessary prerequisite for DMSO release.
Although the production of DMS is most likely the
enzymatically-catalysed cleavage of algal DMSP, the
processes controlling DMSP decomposition are poorly
understood. DMS and DMSO release may be asso-
ciated with normal phytoplankton metabolic processes.
1680 S. G. Wakeham et al.
BARNARD et al. (1984) have suggested that DMS may
be a by-product of acrylic acid production by certain
algae, since acrylate has been identified as having broad-
spectrum antibiotic properties (SIEBURTH, 1960,1968).
DACEY and WAKEHAM (1986) have shown that grazing
of phytoplankton by zooplankton results in release of
DMS to seawater. It is unclear whether DMS w& re-
leased during capture and handling of phytoplankton
cells by the zooplankton, excreted by the zooplankton,
or produced in and released from fecal pellets.
Our incubation experiments, in which pond water
was spiked with DMSP, did demonstrate the potential
for rapid biological formation of DMS from free DMSP
in Salt Pond. In all of the samples along a depth protie
(O-5 m), between 30 and 1009k of the DMSP was con-
verted to DMS in a four-day period. Autoclaved sam-
ples showed no activity. Since the conditions (head-
space of air or Nz:COz) at which the incubation were
conducted did not correspond exactly to ambient con-
ditions in the pond, a presentation of actual rate data
and a quantitative interpmtation of the conversion rates
is not warranted. However, in general, a lower activity
(factor of 2-3) was found in the epilimnion of the pond
compared to depths below about 2.5 m. Maximum
initial activity (turnover after 2 days) was detected in
samples from 3, 3.25, and 3.5 meters depth.
The results of these preliminary experiments suggest
at least one mechanism by which DMSP is converted
to DMS in Sah Pond. The fact that sterile-filtered sam-
ples retained their activity suggests that the conversion
might occur in the absence of living cells. This obser-
vation, along with the fact that autoclaved samples were
not active, indicates that the conversion is enzymatic.
Kinetic experiments designed to assess chemical (non-
enzymatic) cleavage of DMSP are planned, but pre-
liminary results suggest the chemical conversion to be
slow compared to an enzymatic reaction. And finally,
the finding of conversion of DMSP to DMS in other
oxic coastal waters means that the process is not unique
to Salt Pond, and not dependent on oxygen-depleted
conditions. A hydrolase which cleaves DMSP to DMS
and acrylic acid has been isolated and characterized
(CANTONI and ANDERSON, 1956).
DMS and DMSO formation in Salt Pond does not
seem to be associated with the sulfide produced by
sulfate reduction since the maximum concentrations
were never in the anaerobic hypolimnion and at times
the DMS maxima were in the oxic epilimnion. At all
times, DMS and DMSO concentrations were near or
below detection limits in the sulfidic hypolimnion,
consistent with anaerobic metabolism of DMS (ZINDER
and BROCK, 1978~; KIENE et al., 1986). Our
DMSP -) DMS incubation experiments suggest that
conversion of DMSP to DMS apparently can occur
under anoxic conditions, but consumption of DMS at
or immediately below the interface must be rapid in
order to support the strong concentration gradient ob-
served in the metalimnion.
A sedimentary source of DMS also seems unlikely
in Salt Pond, although production in the sediments
followed by diffusion into overlying waters and sub-
sequent consumption in the hypolimnion, while un-
likely, cannot be ruled out. Soil and sediment microbes
are known to produce DMS by decomposition of or-
ganosulfur substrates (KADOTA and ISHIDA, 1972;
BREMNER and STEELE, 1978; ZINDER et al., 1977),
and ANDREAE (1985b) has reported DMS concentra-
tions of up to 120 nmol/l in non-sulfidic pore waters
of sediments of the Peru sheIf (pore waters in Salt Pond
contain > 3 mM HzS). DMS concentrations in the
Peru sediments decreased sharply both toward the sed-
iment water interface, suggesting diffusion into the
overlying water, and toward H$-containing sediments
at depth, indicating active microbial consumption. This
is essentially the same trend we observed in the water
column of Salt Pond. On the other hand, CSz does
apparently have a sedimentary source in Salt Pond,
since its vertical profile (Fig 3) is analogous to methane
(Fig. 2; pore water CH, concentrations in Sah Pond
are >50 rmol/l at the sediment surface and -300
rmol/l at 20 cm depth) in that its concentration in-
creases in the hypolimnion toward the sediments.
Metabolism of DMS by anaerobic phototrophic bac-
teria in Salt Pond. The high concentration of bacterial
chlorophyll in the H&rich hypolimnion (Fig. 2) in-
dicates that a dense population of photosynthetic sulfur
bacteria is located in the hypolimnion. In order to
enumerate and culture them organisms in the labo-
ratory to test their DMSdegrading capacity, basic pa-
rameters such as temperature, pH, and salinity were
determined (Table 1) and appropriate media and
growth conditions were subsequently selected (see
Methods). The anaerobic phototrophic bacteria in the
stratified pond were enumerated using an agar shake
dilution technique reported by PFENNIG and TROPER
(198 1). Whereas very few anaerobic phototrophic bac-
teria were detectable in the epilimnion, some lo’- 1 O6
viable cells per ml were found in the hypolimnion (Ta-
ble 1). The highest bacterial numbers were present in
the depth interval of the maximum PGC and bacterial
chlorophyll concentrations. The colonies formed in the
solid medium used for enumeration were isolated and
examined microscopicahy. The cells were tentatively
identified by comparing their morphology with re-
ported characteristics (TROPER and PFENNIG, 1981).
Some 60% of all colonies consisted of Ameobobucter
sp. (purple sulfur bacteria) and 20% of Prostheuxhloris
sp. (green sulfur bacteria). It should be noted, however,
that culture conditions selected for purple over green
sulfur bacteria.
Given the HzS and DMS profiles, it appeared that
the anaerobic phototrophic bacteria which are abun-
dant in the hypolimnion might be capable of consum-
ing not only HIS but also DMS. To test this, anaerobic
marine basal medium was supplemented with HzS, ac-
etate and DMS and inoculated with samples of anaer-
obic phototrophic bacteria from Salt Pond and Great
Sippewissett Marsh (Table 2). During the first week,
no degradation of DMS took place and growth of the
cultures was slow, especially in the medium containing
Dimethylsulfide in a coastal salt pond 1681
Table 1: chemicrl-physical cberecteriatics and anaerobic phototropbic
becteris of Salt Pond, July 7, 1985.
Depth 82s Temperature pH selinity Aneeroblc Bacterial
(m) tmN1 ('C) 'I.., Phototropbic Chlorophyll d
Bacteria
(viable cella/ml)2 (urll)'
1.0 < 0.001 24.0 7.7 25 n.d.3 0
2.0 < 0.001 24.0 7.b 2a 4.0 x 101 0
3.0 < 0.001 21.5 7.3 30 n.d. 0
3.5 0.01 21.0 7.0 30 7.5 104 312
4.0 0.2 19.5 6.9 7.5 105 170
4.5 2.0 la.5 6.6 3.1 105 14b
lH2S and bacterial chlorophyll data are frm July lb, 1985.
'The viable cell number vlls deteroined by using the eger shake dilution
technique .a described by PFENNIG and TBUPER. (1981). The dilutiona were
mede in basal medium + 3.3 m!l acetate + 2.3 ml4 H2S + 1% agar (pH 7.2)
end the coloniee were counted after an incubation time of about 2 weeks
Ee: :‘,: i%Ld.
5 and 10 mmol/l DMS. However, during the second
week, significant DMS degradation was observed, and
dense cultures of phototrophic purple bacteria devel-
oped. Acetate stimulated growth and possibly DMS
metabolism as well (Table 2). Controls incubated under
sterile conditions or in the absence of light did not
degrade DMS, which suggests that DMS metabolism
was a light-dependent microbial process. In a more
recent set of experiments (ZEYER et al., 1987), purple
phototrophic bacteria capable of oxidizing DMS to
DMSO have been isolated from Salt Pond inocula.
However, the quantitative impact of this process on
DMS cycling in Salt Pond is unknown.
Anaerobic fermentation of DMS has been shown
by other investigators (ZINDER and BROCK, 1978~) to
Table 2: Degradation of DMS after two weeka in cultures
of anaerobic phototropbic bacterial
Anaerobic
Supplements Added to DMS Phototrophic
Basal Medium Consumed Bacteria
(IrIM) (X of initial) (viable cells
ml-l)4
Acetate H2S DE?
0 1 2 95
0 1 5 75 3.7 I lob
0 1 10 20
2 1 2 90
2 1 5 65 lo.8 I lob
2 1 10 30
IJ 2 2 a5
0 2 5 65 4.2 I. lob
0 2 10 15
2 2 2 99
2 2 5 a0 10.0 x lob
2 2 10 55
dark controls3 <5
sterile controls3 (5
lSemples containing anaerobic phototrophic bacteria
were collected in June end July 1985 in Sippewlasett
Marsh and Salt Pond (at a depth of 4n). A mixture of
these samples was used to Inoculate the aedia (5 ml
inoculum per 45 ml medium).
2The concentration of H2S wp8 also determined after 2
weeks and found to be 0.1 mM in aLl cultures.
3Hedium:
basal medium + 2 mM acetate + 2 I&! H2S +
5 mM DMS.
4Detemination: see legend to Table 1; counts only for
5 mM DMS supplements.
yield HzS, COz and CH, , and methylotrophic bacteria
can use DMS as their sole carbon source (SIVELA and
SUNDMAN, 1975; KIENE et al., 1986). However, like
H2S and dissolved CO2, the relatively high concentra-
tions (up to 40 rmole/l) of methane (Fig. 2) diffusing
out of the sediments in the pond precluded observation
of production of methane from nmol/l levels of DMS.
Biogeochemical cycle of DA4.Y in Salt Pond. An es-
timate of the average annual DMS inventory (inte-
grated over the 5.5 m depth of the central basin) yields
about 55 & 15 pmol DMS/m*. That the DMS inventory
in the pond is relatively invariant contrasts sharply with
H2S, the other major volatile reduced (inorganic) sulfur
species in the water column. Hydrogen sulfide was very
abundant in the anoxic bottom waters during summer
stratification, reaching concentrations up to 3 mmol/
1, several orders of magnitude more abundant than
DMS. Hydrogen sulfide was greatly depleted or even
not detectable (at the rmol/l level) in winter and early
spring during mixing and aeration of the water column.
In order to maintain a relatively constant DMS in-
ventory, there must be a balance between the rate of
DMS production by direct algal release and by micro-
bial breakdown of algal DMSP in the low-oxygen me-
talimnion and the rate of removal, either by exchange
to the atmosphere, by tidal exchange to coastal seawater
(Vineyard Sound), by oxidation of DMS in the epilim-
nion, or by metabolism of DMS at the top of the hy-
polimnion. We do not have sufficient data on produc-
tion and removal rates to construct a complete mass
balance (in particular we lack data on lateral transport
and eddy diffusion), but we can calculate the con-
straints on production and consumption rates.
Release of DMS by phytoplankton is well docu-
mented, but we know of only two published estimated
release rates: the coccolithophorid Hymenomonas car-
terue: 1.3 X 10s9 pmol/cell -d (VAIRAVAMURTHY et
al., 1985); the dinoflagellate Gynmodinium nelsoni: 23
x low9 pmol/cell-d (DACEY and WAKEHAM, 1986).
However, the apparent wide range of DMS release in
vitro could in fact be greater in the field, and in any
event, we have too little information on phytoplankton
species composition in Salt Pond to warrant extrapo-
1682 S. G. Wakeham et al.
lation from laboratory cultures to the pond. An aher-
nate estimate of the production of DMS in the epilim-
nion and metalimnion can be derived from the mea-
sured DMSP concentrations and PGC turnover rates.
For 27 August 1985, the DMSP inventory in the pond
is about 100 pmol/m’ over the 35meter depth above
the hypolimnion. POC turnover rates in summer are
about 0.2/d in the epilimnion as calculated from 14C
fixation rates and PGC pool size (LQHRENZ et al.,
1987). Assuming that all DMS from DMSP is asso-
ciated with phytoplankton production in the epilim-
nion and that particulate DMSP turnover is similar to
that of PGC and breakdown yields only DMS, then a
DMS production of 20 rmol/m2 - d would be necessary
to maintain the observed profile. This production rate
includes terms for grazing and decomposition of algal
cells settling into the hypolimnion; a small additional
contribution from direct exudation of DMS by living
phytoplankton would also be needed but is expected
to be minor.
A complementary approach is to consider losses of
DMS from the system. Since DMS is a volatile com-
pound (Henry’s law constant H = 2.0 I-atm/mol at
23°C; DACEY et al., 1984), gas exchange between the
pond surface water and the atmosphere will occur.
When applying the two&m theory (see e.g. Lrss and
SLATER, 1974; SMITH et al., 1980), the flux of DMS
across the water/air interface can be estimated from
DMS concentrations in water and air and the overall
mass transfer coefficient. Measurements of DMS in
the marine atmospheric boundary layer ( 10e4 nmol/l;
BARNARD et al., 1982) and in the epilimnion of Salt
Pond (10 nmol/l) indicate that the atmosphere is a
sink for DMS in the pond. For compounds with H
>, 1 I-atm/mol, gas exchange is controlled primarily
by the liquid film resistance and the overall mass
transfer coefficient is equal to the liquid film mass
transfer coefficient. The flux of DMS across the pond
surface may be calculated (Flux = -I&,) where k, is
the liquid film mass transfer coefficient (cm/h) and C,
the water concentration (nmol/l). In lakes and ponds,
IQ of a volatile compound may be estimated from ox-
ygen aeration rates, which depend on windspeed and
temperature (BANKS, 1975), and the ratio of molecular
diffusivities in water of oxygen and the volatile com-
pound in question. Assuming a mean windspeed of 3
m/s for Salt Pond in summer, a temperature of 298%
and pMS/Do2 = 0.6 (REID et al., 1977), we estimate
a mass transfer coefficient for DMS in Salt Pond of
approximately I .5 cm/h. With an average surface water
DMS concentration of 10 nmol/l, the flux of DMS
from Salt Pond to the atmosphere is projected to be
on the order of 4 pmol/m2 - d. For comparison, oceanic
fluxes of DMS have been estimated to be of the order
of 5 clmol/m2 - d for remote open ocean areas and 12
rmollm2 - d for coastal regions (ANDREAE, 1986).
Given the enclosed nature of Salt Pond, the lower
transfer rate is not unexpected.
Horizontal transport processes in a small pond like
SalI Pond could have an important effect on DMS dis-
tributions. For example, it is possible that lateral inputs
of either DMS or DMSP from sediments along the
boundary of the pond’s central basin might contribute
to the DMS and DMSP peaks in the metahmnion.
While we lack confirmation, and clearly more work is
needed in this area, we have no reason to believe that
there are significant sedimentary sources of either DMS
or DMSP. Tidal exchange with Vineyard Sound may
result in an additional physical mechanism for adding
and removing DMS in the pond. Vineyard Sound water
contains DMS, but the low concentrations there (~2
nmol/l) preclude it from being a significant source of
DMS to Salt Pond. We can estimate the rate of DMS
removal by tidal exchange using the following as-
sumptions. Water entering the pond from Vineyard
Sound in summer has a density of a, = -22
(GSCHWEND, 1979) and will flow to mid-depth, about
2 m, in the pond’s central basin. Outflow from the
pond will be primarily surface water. Tidal measure-
ments in the summer of 1982 showed a tidal range of
O-O. 1 m/ tide (C. TAYLOR, pet-s. commun.). Using this
tidal range, or O-O.2 m/d, and using a volume of 1
X lo5 m3 for the pond’s central basin, a mean epilim-
nion DMS concentration of 10 nmol/l yields a whole
pond dissolved export of O-2 pmol DMS/m2 * d. This
removal rate is surely a maximum value, since it is
unlikely that all of this DMS is actually removed on
each tidal cycle; some is probably returned on the sub-
sequent flood tide.
The sharp concentration gradient for DMS at the
metalimnion-hypolimnion boundary where H2S con-
centrations and numbers of anaerobic phototropic
sulfur bacteria begin to build up suggests a sink for
DMS at the top of the hypolimnion. DMS will be
transported into the hypolimnion by eddy diffusion.
A precise calculation of an eddy diffusion coefficient
for DMS is beyond the measurements we have avail-
able. However, assuming as eddy diffusion coefficient
on the order of 1 m2/d and a concentration gradient
across the metalimnion-hypolimnion boundary (AC/
AZ) of 30 pmol/m-* (August, 1985 in Fig. 2) would
yield a downward transport of some 30 pmol DMS/
m2 - d. In order that the DMS concentrations in the
hypolimnion remain low, an amount of DMS equiv-
alent to the downward flux must be consumed by mi-
crobes in the hypolimnion each day. This suggests that
microbial consumption (30 rmol/m2 - d) not atmo-
spheric loss (4 gmol/m2 - d) is the major sink for DMS
produced in the pond. This is supported by our cal-
culation of 20 rmol DMS/m2 * d production which is
also large relative to the atmospheric loss and suggests
another sink for DMS. While our DMS degradation
experiments do show that the microbial community
in the hypolimnion of Salt Pond are capable of utilizing
DMS, we used mixed microbial cultures which had
been enriched on DMS and therefore cannot use these
results to calculate in situ DMS metabolism. Secondly,
the laboratory incubations contained bacterial numbers
Dimethylsulfide in a coastal salt pond 1683
an order of magnitude higher than in the pond and
used DMS concentrations 5-6 orders of magnitude
higher than measured in Salt Pond.
SUMMARY
Distributions of dimethylsulfide in Salt Pond vary
in response to seasonal changes in source and removal
processes. The dominant source of DMS is most likely
algal production of dimethylsulfoniopropionate which
is present in the pond at concentrations and with ver-
tical profiles roughly similar to DMS. DMS production
is located in the epilimnion and in the oxygen-depleted
metalimnion. The processes producing DMS may in-
clude direct release of DMS by phytoplankton and
heterotrophic breakdown of algal-DMSP. We have
identified the major removal processes as gas exchange
to the atmosphere, tidal exchange, and degradation in
the hypolimnion. Order of magnitude estimates of re-
moval rates suggest that microbial consumption at the
top of the hypolimnion may be the dominant processes
by which DMS is lost from the pond.
Acknowledgements-We thank Elizabeth A. Manuel and Dale
D. Goehringer for assistance in this study. D. Imboden helped
with calculations of tidal exchange from the epilimnion and
eddy diffusional exchange into the hypolimnion. This research
was supported by National Science Foundation Grants OCE
84- 16203 and BSR 84- 18268 and NASA Grant NAGW-606;
additional support from the Coastal Research Center, Woods
Hole Oceanographic Institution to R.P.S. and the Andrew W.
Mellon Foundation to S.G.W. is acknowledged.
Editorial handling: C. S. Martens
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