Deep Sea Research Part II: Topical Studies in Oceanography
Rapid turnover of dissolved DMS and DMSP by defined bacterioplankton communities in the stratified euphotic zone of the North Sea
Introduction
Dimethylsulphoniopropionate (DMSP) is a compound that algae synthesise and can use to maintain their osmotic balance with seawater (e.g. Keller et al., 1989; Kirst, 1996; Gage et al., 1997) and which can comprise a sizeable fraction of cellular algal carbon (0–19%) and sulphur (0–68%) (Matrai and Keller, 1994). Intracellular DMSP is released during algal senescence, viral lysis, and grazing (Belviso et al., 1990; Christaki et al., 1996; Hill et al., 1998; Malin et al., 1998), forming a dissolved pool of DMSP (DMSPd). Lyase enzymes found in some marine bacteria and algae catalyse the production of dimethylsulphide (DMS) from DMSP (de Souza and Yoch, 1995; Stefels and Dijkhuizen, 1996; Steinke et al., 1998; Yoch et al., 1997). However, DMS is a minor product of the overall DMSPd transformation in seawater (Kiene and Service, 1991; Kwint and Kramer, 1996), and probably the major proportion of DMSPd undergoes microbially mediated transformation via methanethiol (MeSH) (Kiene, 1996; Kiene and Linn, 2000a).
The biogeochemical flux of DMSP has attracted particular attention because DMSP is considered to be the major precursor of DMS in the ocean (Turner et al., 1988; Kiene, 1993). This transformation supports DMS emission to the atmosphere and contributes approximately half of the global sulphur input to the atmosphere (Andreae, 1990; Bates et al., 1992). DMS emission potentially can influence climate through aerosol formation and effects on albedo (Charlson et al., 1987; Schwartz and Andreae, 1996; Shaw, 1983). The rate of DMS emission depends strongly on the concentration of DMS in surface waters, which is controlled by production and removal processes of microbial and physical origin: biological consumption, air–sea exchange, vertical mixing, and photodegradation (Kieber et al., 1996; Simó and Pedrós-Alió, 1999). In addition to bacterial production of DMS, considerable consumption of DMS has been observed (Kiene, 1993; Kiene and Linn, 2000b; Kwint and Kramer, 1996; Wolfe et al., 1999). Recent studies also suggest that marine bacteria may control DMS formation by mediating the competitive process which converts DMSPd into MeSH (Kiene, 1996; Ledyard and Decay, 1996; van Duyl et al., 1998), some of which is ultimately assimilated into bacterial proteins (Kiene et al., 1999).
There is increasing evidence that one particular group of bacteria could play a role in mediating the biogeochemical flux of DMSPd. Cloning of the small subunit of bacterial ribosomal RNA (16S rRNA) genes and isolation of natural bacteria in culture have shown that members of the diverse Roseobacter clade of the α-group of Proteobacteria are abundant in marine environments, particularly during phytoplankton blooms (Giovannoni and Rappé, 2000; González and Moran, 1997; González et al., 2000; Kerkhof et al., 1999; Prokic et al., 1998; Riemann et al., 2000). Laboratory studies on Roseobacter cultures have demonstrated a general ability to metabolise DMSP and other organic sulphur compounds (González et al., 1999; Kiene et al., 1999; Ledyard et al., 1993). They are able to transform DMSP into DMS and MeSH, and switching between these two pathways may depend on bacterial sulphur demand (Kiene et al., 1999). Since other abundant bacterioplankton groups have not been isolated in culture, there is limited knowledge about their ability to metabolise organic sulphur compounds. According to molecular analysis of 16S rRNA genes, members of the γ-proteobacteria (Kerkhof et al., 1999) and the Cytophaga–Flavobacterium (CF) cluster (Riemann et al., 2000; González et al., 2000) dominate bacterioplankton alongside Roseobacter during phytoplankton blooms.
The aim of the present study was to quantify microbial fluxes of DMSPd and DMS and to relate these biogeochemical fluxes to the composition of the bacterioplankton community in two different layers of a coherent water mass that was followed Lagrangian-style after tagging it with the inert tracer sulphur hexafluoride (SF6). A previous communication (Zubkov et al., 2001) examined the relationship between bacterial community composition and biogeochemical fluxes of DMSPd and DMS throughout the euphotic zone. Here we examine the relationships in greater detail, making use of the Lagrangian temporal progression to explore differences between the two distinct layers within the euphotic zone of the water column, which showed remarkably similar community composition but different biogeochemical patterns.
Section snippets
Sampling site
The experiment (Dimethylsulphide biogeochemistry within a coccolithophore bloom, DISCO) was carried out in the northern part of the North Sea (60°N 3°E) in June 1999. Using satellite colour imagery and high reflectance from the coccoliths of Emiliania huxleyi, we located a bloom that covered an area of approximately 2000 km2. A patch of approximately 5×6 km located on the edge of the “bloom” was labelled with the inert water mass tracer, SF6 (Law et al., 1998), which allowed us to track the water
Stratification within the euphotic zone
The water column had a mixed surface layer to depths of 13–30 m. The surface and subsurface layers were segregated by a pronounced thermocline indicated by the 10°C isotherm. The 8°C isotherm indicated the depth of a second thermocline that formed the lower boundary of the subsurface layer (Fig. 2b). A third deep-water layer extending from the 8°C isotherm down to the bottom at 90–110 m was not sampled in detail. During the Lagrangian time series, the abundance and production of bacterioplankton
Stratification of the studied water mass
The vertical stratification of the euphotic zone in the studied area resulted in two distinctly different layers. Both layers were within the euphotic zone, although the lower depths of the subsurface layer could have been severely light-limited, particularly on cloudy days. The layers harboured somewhat different phytoplankton communities. The phytoplankton in the surface layer was characterised by high abundances (600–2400 cells ml−1) of the DMSP-producing coccolithophore Emiliania huxleyi, and
Conclusions
The surface and subsurface layers within the euphotic zone of the North Sea were populated by different phytoplankton communities but by a similar bacterioplankton community, comprised of a Roseobacter-related species, the SAR86 cluster and bacteria of the Cytophage–Flavobacterium cluster. The wind-driven deepening of the surface layer and corresponding temperature decrease in both layers had no apparent effect on rates of microbially driven processes, and the bacterial communities remained in
Acknowledgements
We would like to thank all scientists, officers and crew aboard the RRS Discovery for assistance. We are particularly grateful to P. Nightingale, M. Liddicoat and R. Ling for providing the Lagrangian framework. M.V.Z. would like to thank L. Linn for her help with preparatory experimental work. This work forms part of the Dimethylsulphide biogeochemistry within a coccolithophore bloom (DISCO) project and was supported by the Natural Environment Research Council, UK, MOD Defence Evaluation
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