Biogenic Sulfur in the Environment - American Chemical Society

Chapter 11

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Dimethyl Sulfide Production in Marine Phytoplankton Maureen D. Keller, Wendy K. Bellows, and Robert R. L. Guillard Bigelow Laboratory for Ocean Sciences, McKown Point, West Boothbay Harbor, M E 04575 Significant dimethyl sulfide (DMS) production is confined to a few classes of marine phytoplankton, mainly the Dinophyceae (dinoflagellates) and the Prymnesiophyceae (which includes the coccolithophores). One hundred and twenty-three individual clones of phytoplankton representing twelve algal classes were examined in exponential growth for intra- and extracellular DMS (and its precursor DMSP). There is a strong correlation between the taxonomic position of the phytoplankton and the production of DMS. Although the Dinophyceae and Prymnesiophyceae predominate, other chromophyte algae (those possessing chlorophylls a and c) also contain and release significant amounts of DMS, including some members of the Chrysophyceae and the Bacillariophyceae (the diatoms). The chlorophytes (those algae possessing chlorophylls a and b) are much less significant producers of DMS with the exception of a few very small species. Other classes, including the cryptomonads and the cyanobacteria, are minor producers. The oceans are a significant source of organic sulfur compounds that are implicated in acid precipitation and the production of atmospheric aerosols which affect global climate. These compounds are largely biogenic in origin, the most important being dimethyl sulfide (DMS) produced by marine phytoplankton (1-4). Although the distribution of DMS is broadly similar to that of primary productivity (5.6). attempts to directly correlate DMS roduction to primary production have been only moderately successful (e.g., ). This is mainly because only certain groups of algae are known to produce significant amounts of DMS. Thus, correlations of DMS with chlorophyll a measurements are often poor and need to be supplemented with information on species composition. Field observations nave implicated the colonial prymnesiopnyte, Phaeocystis sp., with high levels of D M S (4.8.9). Coccolithophores (members of the Prymnesiophyceae) and some dinoflagellates (Dinophyceae) have also been suspect (4.9). Until recently, no comprehensive survey of D M S production by phytoplankton has been made. Single clones of various marine species have been examined and of these, the coccolithophore, Hymenomonas (ex. Cricosphaera, Syracosphaera) carterae had the highest DMS levels (10.11).

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BIOGENIC SULFUR IN THE ENVIRONMENT

Representatives of the classes Bacillariophyceae (diatoms), Chlorophyceae, Chrysophyceae, Cryptophyceae and the Dinophyceae (dinoflagellates) had much lower concentrations. Freshwater representatives of these classes also showed little DMS production, although significant levels were found in freshwater cyanophytes (12). Marine macroalgae also release substantial uantities of DMS. The Chlorophyceae, especially Ulva, Enteromorpha, and •odium, and the red alga, Pofysiphonia, are capable of producing large amounts of DMS in contrast to the Phaeophyceae (brown algae) which produce little (13.14V In algae, DMS is produced by the cleavage of dimethylsulfoniopropionate (DMSP). The by-products of this enzymatic cleavage are DMS and acrylic acid (1:1). In macroalgae, there is a clear relationship between DMSP and osmotic adaptation (14). The intracellular concentrations of DMSP increase with increasing external salt concentrations. A similar response has been observed in a few species of phytoplankton, including the heterotrophic dinoflagellate,


2

Crypthecodinium (ex. Gyrodinium) cohnii (15.) and the coccolithophore,

Hymenomonas carterae (16), but only at extreme salinities or osmotic pressures (using sucrose). The role of DMSr and other osmotica, glycine betaine and homarine, have also been examined for a halotolerant strain of Platymonas (12). Phaeocystis, the prymnesiophyte most commonly associated with high DMS concentrations in situ, has not been examined for this property but it has been speculated that acrylic acid, the other product of DMSP decomposition, plays an important role in this alga's ecology. The acrylic acid produced by Phaeocystis may have antibiotic properties (IgJ and may inhibit bacterial growth or feeding by zooplankton on the colonies of Phaeocystis. Ageing cultures of Phaeocystis have excretion rates of acrylic acid up to 7/ig/l (12). In this situation, DMS would be the incidental byproduct of acrylic acid production. While it is generally accepted that phytoplankton, and most likely only certain groups of phytoplankton, are the most significant source of DMS in the oceans, there is little understanding of the physiology of its production or release. It is unclear whether algae actively excrete DMS or DMSP. Recent studies suggest that a considerable amount of DMSP is present in the water column (4.20). probably as a result of cell disruption. It is unlikely that DMSP passes through intact cell membranes, both because of the size and polarity of the molecule. It has been convincingly demonstrated that zooplankton stimulate the release of DMS (21). Thus, as algae age or are eaten, DMS is released, as well as DMSP. Once in the water column, there is little agreement as to its fate. DMS is soluble in seawater (22) and shows a steep gradient in concentration across the air-sea interface. An unknown proportion is oxidized to DMSO, both by bacteria (22) and photochemically (24). The fate of free DMSP is also unknown, although it is likely that bacteria mediate its breakdown to DMS at unknown rates (25). Processes occurring above the sea surface are also poorly understood. Most of the DMS is thought to be oxidized to S O 2 and subsequently to H2SO4, resulting in acid precipitation events, or becomes sulfate aerosols which serve as cloud condensation nuclei (CCN), critical to cloud formation and thus climate (2-4). Essential to a determination of the role of DMS in the global sulfur cycle is an understanding of the phytoplankton, determining which phytoplankters are capable of significant DMS production and the environmental variables affecting their physiology. Methods

All the phytoplankton clones are maintained at and available from the Provasoli-Guillard Center for Culture of Marine Phytoplankton (Bigelow Laboratory for Ocean Sciences, McKown Point, West Boothbay Harbor, Maine In Biogenic Sulfur in the Environment; Saltzman, E., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1989.

11. KELLER ET AL.

Dimethyl Sulfide Production in Marine

169

04575, U . S . A . ) . A l g a l cultures were grown i n 100 m l batch cultures i n appropriate media and, when possible, under identical light conditions ( 1 0 quanta«cm *sec" ; 14:10 light:dark cycle) and at 20°C. M e d i a selection and growth temperature were dependent upon the environment from which the phytoplankter was isolated. C e l l count samples were preserved with Lugol's fixative and counted on a 0.1 mm hemocytometer. Cell volumes were measured with live samples. Because we were interested i n the total potential production of D M S by each clone, we chose to measure both the intracellular D M S (in the form of D M S P ) and the extracellular D M S and D M S P . T o do this, we took advantage of the specific reaction which cleaves D M S P 1:1 into D M S and acrylic acid with the addition of a strong base (10.13). This method is simple and specific, and also eliminates some of the problems of sample preparation. Sampling, filtration and bottle effects undoubtably influence D M S release from D M S P . By measuring all the D M S (and D M S P ) in a culture, we obtain levels of total D M S , but are unable to discriminate between free D M S and that produced by the cleavage of D M S P . Thus, data are presented as D M S P equivalents (Figure 1). While still i n mid-exponential growth (as measured by fluorescence and cell counts), each phytoplankton culture was divided into two 50 ml portions. One was placed i n a silanized 100 ml serum bottle and sealed. The base (2 mis) was added, the sample incubated and headspace gas analysis was performed 24 h later. A l l samples were incubated for 24 h at room temperature in the dark, then incubated for 30 min at 40°C immediately before sampling to maximize release to the headspace. Constant headspace:sample ratios were maintained at all times. The number from this sample represents the total D M S produced by the culture without discriminating between intraand extracellular pools. The other 50 m l portion of the culture was gently (preferably by gravity) filtered through a G F / F filter (Whatman, nominal pore size 0.7 μπι). The filter was placed in a 10 ml silanized vial, sealed and base (1 ml) added. After incubation, headspace gas analysis was performed. The filtrate was collected, transferred to a silanized 100 ml serum bottle and treated in the same manner as the whole culture. D M S P standards were prepared by dissolving 1 mg D M S P (Research Plus, Bayonne, Ν J . , U.S.A.) in 100 mis of 0.2 um filtered seawater. The primary stock is volatile and it was remade weekly. Appropriate dilutions were made into 50 ml portions for liquid standards and for filter standards, small amounts of the primary stock were applied directly and absorbed by G F / F filters. One ml of the base was added to filter samples, 2 mis to liquid samples. The level of detection is 50 ng D M S for filter standards and 300 ng D M S for liquid standards. Appropriate amounts of headspace gas were removed and injected directly onto a Chromosil 330 Teflon column (6 ft.; 1/8 O.D.); injector 70°; column 70°; H e carrier gas 30 m l / m i n and detected with a F P D (detector temperature 150°). A V a n a n 3300 gas chromatograph was used. A l l measurements were performed in triplicate. Standards were run before and after and randomly during sample analysis. 16


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Results and Discussion One hundred and twenty-three individual phytoplankton clones representing twelve algal classes were examined for total U M S ( D M S P ) production. D M S was measured in whole cultures, cell and filtrate fractions (as outlined in Figure 1). D M S measurements for whole cultures (cells and filtrate) are given in Table I. Values for D M S levels in all fractions, whole culture, filtered cells and filtrate are not reported here but comparisons of the whole culture sample with the filtered cells and accompanying filtrate revealed that, for the most part, amounts of D M S i n the two fractions were equivalent to the amount i n the whole culture. Differences can largely be attributed to filtering problems. Even




1. 5N NaOH added to sample or standard

/ 2. DMSP standards

DMS released from standard amounts DMSP

\ 3. Algae in culture media

ι \ 4. Filtered

DMS released DMS released from internal from internal and extracellular DMSP DMSP

5. Algal filtrate

DMS released from extracellular DMSP

Figure 1. Sampling protocol for D M S measurements.


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Dimethyl Sulfide Production in Marine Phytoplankton

171

Table I. Phytoplankton Clones Examined for DMS Release, ng DMSP Corresponds to DMSP - Equivalents CalculatedfromStandard Curves as Explained in Text. N.D. = Not Detectable. See Text for Limits of Detection.


Class

Genus/Species

Clone

pgDMSP/céll

μηι DMSP/cmof cell volume 0.69

Bacillariophyceae Biddulphia sp. Centrales Chaetoceros (CENTRIC DIATOMS) affinis Chaetoceros decipiens Chaetoceros didymwn Chaetoceros simplex Coscinodiscus sp. Ditylum brightweUu Melosira manmuloides MinkUscus trioculatus Porosira glacialis Rhizosolenia setigera Skeletonema costatwn Skeletonema menzellii Thalassiosira guillardii Thalassiosira pseudonana Thalassiosira rotula Thalassiosira sp.

L1474 CCUR*

1.0 N.D.

WTCD

N.D.

L162*

0.04

BBSM

N.D.

COSCl* L154*

10.4 9.81

0.17 4.61

MEL3

34.5

264.18

GMe41*

0.10

32.91

18·

9.37

2.09

RHIZO

15.1

0.46

SKEL

0.50

21.87

MEN5

0.14

30.30

7-15*

N.D.

3H

0.08

16.64

MB411

0.25

1.05

PP86A*

5.48

1.82

Bacillariophyceae Amphora Pennales coffaeformis (PENNATE DIATOMS) Asterionella glacialis Cylmdrotheca closterium Navicula pelliculosa Nitzchia laevis Phaeodactylum tricornutum

47M

N.D.

A6

N.D.

NCLOST

1.49

04

N.D.

07

0.52

PHAEO

N.D.

18.21

41.42

7.34

Continued on next page


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Table I continued


Class Chloromonadophyceae (CHLOROMONADS)

Chlorophyceae (CHLOROPHYTES)

Chrysophyceae (CHRYSOPHYTES)

Ciyptophycceae (ŒYPTO]•MONADS) p

Genus/Species Chattonella harima Chattonella luteus

Clone WTOMO

N.D.

OLISTH

N.D.

EPT3 Chlamydomonas sp. Chlorella OPT10 capsulata Chlorella sp. 017 Chlorococcum sp. Chloro-1 Dunaliella DUN tertiolecta Nannochloris GSBNanno atomus Stichococcus sp. NB3-18 IVP16AX unidentified coccoid Chrysamoeba sp. Chrysosphaera sp. Ochromonas sp. Ochromonas sp. unidentified coccoid unidentified flagellate Chroomonas saUna Cryptomonas sp. Cryptomonas sp. Cyanophora paradoxa Rhodomonas lens unidentified ryptomonad cryptomonad unidentified cryptomonad

3

pg DMSP/cell μπι DMSP/cm of cell volume

IG5 UW397

vt

N.D. 0.61

25.22

N.D. 0.08 N.D.

0.14

N.D. N.D. N.D. 2.68 N.D. 038 0.58 024

596.27 200.75 529.10 42239

IVlbax N.D. MCI 3C

N.D.

CY2

2.86 N.D. N.D.

RLENS IVF 3

N.D. N.D.

IVP

8

N.D.

10c*

Cyanophyceae Synechococcus SYN (BLUE-GREEN ALGAE) bacillaris Synechococcus sp. DC, Synechococcus sp. um Synechococcus sp. L1604 Synecluxystis sp. CN0117 Trichodesmium sp. MACC0993

345.52

N.D. N.D. N.D. N.D. N.D. N.D. N.D.


11. KELLER ET AL.


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Table I continued


Class Dinophyceae (DINOFLAGELLATES)

Euglenophyceae (EUGIJENOPHYTES)

Pg DMSP/cell

3

μπι DMSP/cm of cell volume

Genus/Species

Clone

Amphidinium carterae Cachonina niei Ceratium longipes Crypthecodinium cohnii

AMPHI

19.3

2201.50

CACH 090201* CCOHNII

43.0 2.0 45.7

192.54 0.23 377.61

L823 Dissodinium lunula GT200A Gambierdiscus toxicus GP60e Gonyaulax pofyedra Wl* Gonyaulax spinifera GSBL Gymnodinium nelsoni WT8 Gymnodinium simplex Gymnodinium sp. 94GYR* KT3 Gyrodinium aureolum PLY497A Gyrodinium aureolum GYMNO Heterocapsa pygmaea GT23* Heterocapsa sp. NEPCC534 Oxyrrhis (w/DUN) marina EXUV Prorocentrum minimum IIBobi Prorocentrum sp. 8618T Prorocentrum sp. M12-11* Prorocentrum sp. GT429* Protogonyaulax tamarensis CCMP4 Pyrocystis noctiluca PERI Scrippsiella trochoidea HIPP Symbiodinium microadriaticwn L603 Thoracosphaera heimii DDT* dinoflagellate EEUI Eutreptia sp.

116.0

1.94

160.0

10.08

18.0

4.01

145.0

16.49

244.0

29.55

32.0

45.75

24.0 0.72

124.63 0.65

0.68

0.36

19.5

451.49

78.1 N.D.

190.30

21.4 16.4 N.D. 593.0 265.0

888.06 1082.10 190.30 139.55 0.01

6.06 384.0

350.00

24.2

344.78

26.6

194.03

91.6

83.58

N.D. Continued on next page


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Table I continued


Class

Genus/Species

Clone

pg DMSP/cell

3

Mm DMSP/cm of cell volume

Eustigmatophyceae Nannochloropsis (Ευ5ΉσΜΑΤΟΡΗΥΤΕ8)

GSB Sticho

0.02

22.76

Prasinophyceae (PRASINOPHYTES)

PLY189

0.13

29.18

DW8

0.03

161.94

IB

0.02

287.31

1.08

36.57

Mantoniella squamata Micromonas pusilla Micromonas pusilla Nephroselmis Piriformis Pedinomonas minutissima Pseudoscourfielda marina Pyraminonas sp. Tetraselmis levis Tetraselmis sp. unidentified coccoid unidentified coccoid unidentified coccoid unidentified flagellate

Prymnesiophyceae Chrysochromulina (PRYMNESIOPHYTES ericina including Chrysochromulina COCCOUTHOPHORES) herdlansis Coccolithus neohelis Emitiania huxleyi Imantonia rotunda Imantonia rotunda Isochrysis galbana Pavlova lutheri Pavlova pingus Pavlova sp. Pavlova sp. Pavlova sp.

4

PLY58 VA3 IVP

N.D. n

0.02

5.65

13-10PYR PLATY 1

0.02 1.62

0.53 32.76

OPT4 048-23

1.09 0.09

45.45 47.69

VH ax 2

1.92

126.87

VB

X

138

156.72

BE92*

0.03

484.33

NEPCC109A

3.81

251.49

NEPCC186

3.62

412.69

CONE

2.53

85.08

BT6

0.75

166.42

ΠΕ$

0.18

159.70

1197NTA

0.26

87.31

ISO

0.50

56.87

MONO

0.05

3.28

IG

0.71

46.87

0.22 0.65 0.45

53.36 156.72 51.19

7

ΠΒ3+ IIB^ax IIG +

3


11.

KELLER ET AL.


175

Table I continued


Class

Genus/Species Pavlova sp. Pavlova sp. Pavlova sp. Phaeocystis sp. Phaeocystis sp. Pleurochrysis carterae Prymnesium parvum Syracosphaera elongata Umbilicosphaera sibogae unidentified coccolithophore unidentified flagellate unidentified flagellate unidentified flagellate unidentified flagellate

Rhodophyceae

unidentified

Porphyridium omentum Rhodosorus marinus

Clone

pg DMSP/cell

IIG ax 3

Π0

+ 6

IIG ax 677-3 1209 6

COCCOII PRYM SE62 L1178 8613COCCO* 3D* 8610G6* 8610C3*

μπι DMSP/cm of cell volume

0.52 0.65 0.73 2.29 1.0 12.0

59.18 73.66 83.58 260.45 113.43 170.15

1.7

111.94

19.8

35.30

13.8

195.52

1.1

125.37

1.57

179.10

3.37

139.55

3.15

358.21

5.55

365.67

326-1* PORPH

N.D.

RHODO

0.31

35.67

2.81

94.78

LOBD* unidentified green flagellate

*Gulf of Maine isolates Bacteria isolatedfromthese clones showed no detectable DMS release +


3

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distribution and extraction of phytoplankters that grow in clumps or attached to the culture vessel walls is veiy difficult. Using the D M S values (calculated from the external D M S standards) and cell count data, we normalized the measurements to pg DMSP-equivalents/cell. A l s o , because there is a great diversity of size and form among the phytoplankton clones, ranging in the largest dimension from less than 1 μίτι to several hundred μτα% we calculated D M S levels on a per cell volume basis (v=0.5236(d) ). We used total cell volumes for these values, not attempting to estimate osmotic volume or to discriminate between vacuolate and nonvacuolate species. Thus, amounts of DMSP-equivalents (μΜ) per unit cell volume (CHF) may be underestimated by approximately a factor 0 1 2 (assuming an osmotic volume of 50% of total volume) for many species. Since the range of values is over five orders of magnitude, this discrepancy is probably not significant. When compared with published values of D M S P / c e l l volume (4.16.17.21^ the values are comparable though somewhat lower as expected. F o r example, a Platymonas (= Tetraselmis) had levels ranging from 50-250 μ Μ / c m (12) and a clone of Gymnodinium nelsoni had an estimated level of 280 (21). Our values for Tetraselmis clones were approximately 50 μ Μ / c m ; for Gymnodinium nelsoni, 30 μ Μ / c m . Other Gymnodinium's were considerably higher (up to 150 μ Μ / c m ) . T h e D M S (in the t o r m of D M S P ) is largely i n t r a c e l l u l a r for the phytoplankton, which were undergoing exponential growth. D M S does not appear to be released into the medium in any quantity and it is likely that the measured D M S is released, presumably in large part as D M S P , only upon cell death and lysis or with some mechanical disruption, such as grazing (21). Some members of the Prymnesiophyceae had substantial quantities of D M S (DMSP) in the medium. We believe that this is a real phenomenon and not just a filtering artifact. The significance of the extracellular D M S (DMSP) among the Prymnesiophytes is unclear. Certain members of this class, notably Phaeocystis, produce substantial quantities of extracellular mucilage and reports of sulfur odors during Chrysochromulina blooms suggest that this phenomenon occurs in situ as well (9). Most o i the phytoplankters examined were xenic (i.e. not bacteria-free). Because of concern that the presence of bacteria might affect D M S concentrations, we examined for D M S production several clones of algae with and without their accompanying natural bacteria. In the presence of bacteria, D M S concentrations were not significantly less (Table I). We also examined bacteria isolated from the algal cultures separately, both for D M S production and utilization of D M S P as a growth substrate, with negative results in both cases. A n analysis of D M S production by each phytoplankton class follows:


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3

3

3

3

Bacillariophvceae (centric and pennate diatoms). F o r the most part, the diatoms are not significant producers of D M S . A n exception is the estuarine species, Melosira nummuloiaes. In sufficient numbers (i.e. bloom situations) certain other species could be important. Therefore diatoms cannot be summarily dismissed as sources of D M S ; some consideration of species composition must be included. Chloromonadophvceae fChloromonadsl This class of phytoplankton has few known marine representatives but these species can form extensive blooms. They are not however a significant source o f D M S .


11.

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177

Chlorophyceae (Chlorophvtes-true green algae). These algae do not produce D M S i n any quantity. One minor exception is the Chlorella isolated from a small salt pond.


Chrvsophyceae (Chrysophvtes). There is a considerable range of D M S levels within this class. D M S was undetectable i n several clones but was very high, based on cell volume, in others. Crvptophyceae (Cryptomonads). The cryptomonads are insignificant producers of D M S . The small Cryptomonas clone, ID2, isolated from an oceanic area, gave the only detectable D M S concentration i n this group. It produces a substantial amount. Cvanophyceae (blue-green algae). The important prokaryote, Synechococcus, produces negligible amounts of D M S , as do other marine representatives of this class. By contrast, freshwater representatives apparently do produce D M S (12). D i n o p h y c e a e ( D i n o f l a g e l l a t e s ) . T h e dinoflagellates, along with the prymnesiophytes, are tbe major producers of D M S , although there is considerable variation when compared by cell volume. H i e dinoflagellates are a diverse group with a large size range and with auto- and heterotrophic representatives. Some of the very large oceanic dinoflagellates, such as Pyrocystis or Ceratium, are minor D M S producers. Others, such as the common coastal bloom-forming species, Amphidinium or Prorocentrum, are major potential sources. The heterotrophic dinoflagellate, Crypthecodiniwn cohnii, as reported (15), produces a substantial quantity of D M S , but there are many otner dinoflagellates which produce equivalent or greater amounts. The symbiotic dinoflagellate, Symbiodinium, associated with corals, contains a large amount of D M S . Reports of major D M S release from coral reefs have been reported (H) and may be related to this phytoplankter. Attempts to correlate D M S production with Orders within the Dinophyceae are only moderately conclusive. Certainly the Order Prorocentrales, which includes only the Prorocentrum, is significant. The Orders Gymnodiniales (which includes Amphidinium and Gymnodinium among others) and Peridiniales (which includes Heterocapsa and Protogonyaulax) are important but also include members which are insignificant D M S producers; Gyrodinium and Oxyrrhis and Ceratium, respectively. Euglenophvceae: Eustigmatophyceae: Rhodophyceae. These classes have few marine representatives and are insignificant producers of D M S . Prasinophyceae (Prasinophytes-green algae). For the most part, these algae do not produce much D M S but because of the very small size of representative clones, the intracellular quantities are quite large. This aspect will be discussed in further detail. Prymnesiophyceae (Prymnesiophytes-includes the coccolithophores). The prymnesiophytes are the second important class of phytoplankton i n terms of D M S p r o d u c t i o n . A l t h o u g h much less substantial per c e l l than the dinoflagellates, they do produce equivalent amounts when compared on a per cell volume basis, rhe coccolithophores are all significant producers but otner bloom-forming prymnesiophytes, such as Chrysochromulina, are also important. Phaeocystis, the phytoplankter most commonly linked to D M S emissions in situ, does not stand out among the prymnesiophytes in terms of D M S production. It


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is exceptional however in the magnitude and longevity of the blooms it produces


02JL2). It is difficult to extrapolate the values obtained for D M S from laboratory cultures to field situations but the clear taxonomic pattern of D M S production has important ecological implications. Based on this taxonomic relationship, it is evident that D M S will vary temporarily and spatially, dependent on the species composition of the flora. Although areas of high primary productivity may have significant D M S emissions, it is equally possible that they will not or the emissions may vary seasonally. A general understanding of phytoplankton distribution and succession coupled with this taxonomic survey of tne D M S production allows for speculation on D M S patterns in the oceans. Although the diatoms are not major D M S producers, their numerical abundance and diversity precludes their elimination from this discussion of those phytoplankters central to D M S production. Diatoms seasonally dominate the flora in most areas of the oceans, but are especially abundant in temperate and polar regions. Phytoplankton blooms are controlled i n large part by the physical state of the environment, which affects light, temperature and nutrients. Diatoms dominate i n turbulent waters, including coastal and upwelling areas, and during or immediately after mixing events, such as the spring and fall water column turnover. D i n o f l a g e l l a t e s , i n contrast, predominate i n stable environments, normally stratified, warm water communities ( 2 0 . The seasonal cycle of phytoplankton is a function of latitude and the timing and duration of the biological seasons are critical to the development of the phytoplankton community. Thus with increasing latitude, the peak of phytoplankton abundance will occur correspondingly later. If the oceans are divided into three macrozones, boreal (subarctic and subantarctic), temperate and tropical, certain generalities can be made. The boreal regions and temperate regions are not dissimilar except for the timing of the blooms. Both are essentially diatom-dominated communities with sporadic and often very large blooms of dinoflagellates and coccolithophores i n the summer. Nanoplankton often dominate in the transitional early summer months. Tne succession of phytoplankton within the G u l f of Maine serves as an example (see Table I for Gulf of Maine isolates). The spring diatom bloom, consisting of small, rapidly-growing diatoms, develops along the southwest coast of the Gulf and moves eastwards across the shelf. T h e diatoms are dominated by small centrics, mostly Thalassiosira, Chaetoceros and Skeletonema costatum. This community typically reestablishes itself in a second, smaller fall bloom. A s nutrients are depleted and stratification occurs, the spring diatom community diminishes and is replaced by a mixed p o p u l a t i o n o f flagellates and dinoflagellates. Its composition is not as predictable. T h e dominant dinoflagellate off-shore is Ceratium longipes; inshore populations consist of Protogonyaulax tamarensis, the common "red-tide" organism of temperate waters, Prorocentrum spp., Peridinium spp. and Dinophysis spp. (27-311 Other dinoflagellates, such as Gyrodinium sp., occasionally form massive localized patches (23). Phaeocystis pouchetii is always a component of the spring flora and occasionally, but not predictably, will disrupt the typical succession and completely dominate surface waters for prolonged periods. There are numerous records o f Phaeocystis blooms throughout the G u l f w i t h concentrations exceeding (19.27.301 There are also reports of blooms of the coccolithophore, Emiliania huxleyi offshore (38.311 We have observed major, extensive coccolithophore (presumably E. huxleyi) blooms i n midsummer since 1983. Thus, for the Gulf of Maine, we would expect to see a strong seasonality of D M S emissions. The winter and early spring months w o u l a b e periods of negligible release; mid-spring would be less predictable depending on the



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occurrence of Phaeocystis. In years of a Phaeocystis bloom, this period might see a major D M S emission. In early summer, near-shore waters would account for a substantial portion of the annual D M S release, with blooms of the common dinoflagellates, Prorocentrum and Protogonyaulax. Offshore, the picture would be less clear. Ceratium longipes is a minor D M S producer but the poorlycharacterized nanoplankton population may represent a significant source. In later summer, a major E. huxleyi bloom would be responsible for high D M S concentrations. The fall months would show a sharp decline i n D M S levels as the diatoms become dominant again. Rhuosolenia, common in late summer, is known to form macroscopic mats i n many environments (32.33). and may provide an exception. In such cases, cell densities reach 1 0 / m l and could represent a significant, if patchy, source of D M S . Also a few coastal forms such as Melosira and Cylindrotheca that occur in abundance on tidal flats and at the thermocline of stratified coastal water columns may be important. This scenario is somewhat typical of boreal and temperate regions in all the oceans and applies also to neretic areas i n tropical seas. The estuarine embayments i n the tropics are often seasonally dominated by Prorocentrum, Scrippsiella a n d Gymnodinium. In oligotrophic areas i n the tropics, dinoflagellates are often abundant and congregate at the pycnocline, forming a deep chlorophyll maximum at approximately the 1% light level (21). This "shade flora" is usually dominated by Ceratium or Pyrocystis, neither a major D M S producer. However, since the maximum number of dinoflagellates is usually subsurface (at the 10-1% light levels) in all environments, an interesting question is raised. Maximum D M S concentrations have been observed just above the deep chlorophyll maximum (2), presumably released by those phytoplankters comprising the maximum. Does this D M S contribute to the amount of D M S released to the atmosphere at the air-sea interface? Since many dinoflagellates are known to make diel vertical migrations, it is very possible in shallow water columns. For non-migrating species or deep euphotic zones, it is less clear. Coccolithophores are important i n oligotrophic waters. The majority of coccolithophore species are tropical but the few boreal species, notably E. huxleyi, can form blooms, with cell numbers of up to 3.5 χ 1 0 / ! recorded (25). E. huxleyi is also the species with the greatest biogeographical range and except i n tropical waters is the dominant coccolithophore. H i g h numbers of coccolithophores are also seen i n equatorial waters and in marginal seas in the tropics, but are dominated by Gephyrocapsa (26). Phaeocystis, another prymnesiophyte, forms extensive blooms i n late spring i n the A r c t i c and Antarctic. Recent advances i n satellite technology make coccolithophore blooms visible from space (22) and there is speculation that coccolithophore blooms are becoming more persistent and regular i n certain areas (26). it is also possible that other phytoplankters which are major producers of D M S are becoming more abundant. Phaeocystis blooms in particular are becoming more intense and frequent in the North Sea. It is suggested that these phenomena are linked to increasingeutrophication (2638). The distribution of Phaeocystis is well-known because of its colonial form; likewise E. huxleyi is well-characterized because o f its easily recognized coccoliths. B o t h of these species are members o f the nanoplankton (phytoplankton less than 20 um), which in general are poorly described. Many of the nanoplankton are flagellates or coccoid cells which belong to a smaller size fraction, the ultraplankton (those cells passing through a 3 μΐη filter (22)) and are members of several different algal classes, including the Chrysophyceae, Prasinophyceae and Prymnesiophyceae. They are mentioned here because many produce substantial amounts of D M S . Tnese small algae are present in 3

6


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6

7

all environments at densities of 10 - 10 /1 and often dominate deep chlorophyll maxima in oceanic areas (39-42). Thus, representatives of the Chrysophyceae, Prasinophyceae and Prymnesiophyceae may be important sources of DMS in areas they dominate. Comparisons of production per unit cell volume reveal that DMS levels are roughly equivalent to those of the dinoflagellates and coccolithophores. Since the abundance of these small phytoplankton is usually at least two orders of magnitude higher than their larger counterparts, size differences (which are also approximately two orders of mangitude) are overcome. DMS emissions from oligotrophic regions may be mainlyfromthis size class of phytoplankters. In coastal waters, phytoplankton of ultraplanktonic size are often major bloom-formers; e.g. the prymnesiophyte, Chrysochromulina (2), the prasinophyte, Micromonas pusilla (22.) and the newly-described chrysophyte, Aureococcus anophagefferens, responsible for the "brown tide" in Long Island Sound, U.S.A. waters, reaching densities of 10 /1 (42). All of these species and other similar forms may be responsible for occasional major DMS emissions. It is also noted that the ultraplankton are quite plastic and easily pass through filter pores much smaller than their smallest dimension (22). Therefore, it is recommended that filters used to either remove particulates from water samples before DMS measurement or collect cells for chlorophyll measurements be no larger than G F / F (nominal pore size 0.7 μπι). Correlations of DMS concentrations with chlorophyll a may improve with this method. DMS levels in marine phytoplankton are highly variable, rangingfromnondetectable up to 600 pg/cell or intracellular concentrations as high as 2000 μτη DMSP (equivalents)/cm cell volume. There is a clear taxonomic pattern, with major production confined to the Dinophyceae and the Prymnesiophyceae. However, representatives of other classes, especially other chromophyte (containing chlorophylls a and c) plankters, may be as significant. The eukaryotic ultraplankton may be especially important. Based on this taxonomic survey of DMS levels within phytoplankton and known distributions of individual phytoplankters in situ, it can be expected that DMS production will be seasonal and regional in nature and highly dependent on the numerical abundance of key species. A consideration of phytoplankton species composition and succession must be included in any area under study for DMS emissions from the oceans. 9

3

Acknowledgments Although the research described in this article has been funded wholly or in part by the United States Environmental Protection Agency through R812662 to R.K.L. Guillard, it has not been subjected to Agency review and therefore does not necessarily reflect the views of the Agency and no official endorsement should be inferred. We thank Patrick M. Holligan and Rhonda C. Selvin for their comments and suggestions. This manuscript is Bigelow contribution no. 88002. Literature Cited 1. Andreae, M. O.; Raemdonck, H. Science 1983, 221, 744-7. 2. Bates, T. S.; Charlson, R. J.; Gammon, R. H. Nature 1987,329,319-21. 3. Charlson, R. J.; Lovelock, J. E.; Andreae, M. O.; Warren, S. G . Nature 1987, 326, 655-61.


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33. Martinez, L.; Silver, M . W.; King, J. M.; Alldredge. Science 1983, 221, 152-4. 34. Taylor, F. J. R. In The Biology of Dinoflagellates; Taylor, F. D. R., Ed.; Blackwell Scientific, 1987; pp. 399-502. 35. McIntyre, A.; Be, A. W. H. Deep Sea Res. 1967, 14, 561-97. 36. Okada, H.; Honjo, S. Deep Sea Res. 1967, 20, 355-74. 37. Holligan, P. M.; Viollier, M.; Harbour, D. S.; Camus, P.; ChampagnePhilippe. Nature 1983, 304, 339-42. 38. Lancelot, C.; Billen, G.; Sournia,A.;Weisse, T.; Colijn, F.; Veldhuis, M. J. W.; Davies, A.; Wassman, P. Ambio. 1987, 16, 38-46. 39. Murphy, L. S.; Haugen, Ε. M. Limnol. Oceanogr. 1985,30,47-58. 40. Estep, K . W.; Davis, P. G . ; Hargraves, P. E.; Sieburth, J . M c N . Protistologica 1984, 20, 613-34. 41. Hooks, C. E.; Bidigare, R. R.; Keller, M . D.; Guillard, R. R. L. J. Phycol. 1988, in press. 42. Glover, H. E.; Keller, M. D.; Guillard, R. R. L. Nature 1986,319,142-3. 43. Smayda, T. In Proceedings of the Emergency Conference on "Brown Tide" and other unusual algal blooms. Oct. 23-4, New York, 1986. RECEIVED September 6, 1988


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