An annual cycle of dimethylsulfoniopropionate-sulfur
and leucine assimilating bacterioplankton in the
coastal NW Mediterranean
Maria Vila-Costa,
1
Jarone Pinhassi,
1,2
Cecilia Alonso,
3†
Jakob Pernthaler
3‡
and
Rafel Simó
1
*
1
Institut de Ciències del Mar, CSIC. Pg. Marítim de la
Barceloneta 37-49, 08003 Barcelona, Catalonia, Spain.
2
Marine Microbiology, Department of Biology and
Environmental Sciences, University of Kalmar,
SE-39182 Kalmar, Sweden.
3
Max Planck Institute for Marine Microbiology,
Celsiusstrasse 1, D-28359 Bremen, Germany.
Summary
The contribution of major phylogenetic groups to het-
erotrophic bacteria assimilating sulfur from dissolved
dimethylsulfoniopropionate (DMSP) and assimilating
leucine was analysed in surface seawaters from
Blanes Bay (NW Mediterranean) over an annual study
between March 2003 and April 2004. The percentage
of bacteria assimilating DMSP-S showed a strong
seasonal pattern, with a steady increase from winter
(8 5%) to summer (23 3%). The same seasonal
pattern was observed for the rate of DMSP-S
assimilation. The annual average percentage of
DMSP-S-assimilating bacteria (16 8%) was lower
than the corresponding percentage of leucine-
assimilating cells (35 16%), suggesting that not all
bacteria synthesizing protein incorporated DMSP-S.
Smaller differences between both percentages were
recorded in summer. Members of the Alphaproteo-
bacteria (Roseobacter and SAR11) and Gammapro-
teobacteria groups accounted for most of bacterial
DMSP-S-assimilating cells over the year. All major
bacterial groups showed an increase of the percent-
age of cells assimilating DMSP-S during summer, and
contributed to the increase of the DMSP-S assimila-
tion rate in this period. In these primarily P-limited
waters, enrichment with P + DMSP resulted in a
stimulation of bacterial heterotrophic production
comparable to, or higher than, that with P + glucose in
summer, while during the rest of the year P + glucose
induced a stronger response. This suggested that
DMSP was more important a S and C source for
bacteria in the warm stratified season. Overall, our
results suggest that DMSP-S assimilation is con-
trolled by the contribution of DMSP to S (and C)
sources rather than by the phylogenetic composition
of the bacterioplankton.
Introduction
Microorganisms control biogeochemical cycles in the sea.
One of the current challenges in marine microbial ecology
consists of identifying what phylogenetic groups mediate
particular key biogeochemical processes in the ocean, to
increase our understanding of how these processes are
regulated over various temporal and spatial scales. For
instance, if relatively few studies have addressed the sea-
sonal variability of bacterial diversity in marine waters
(Pinhassi and Hagström, 2000; Eilers et al., 2001;
Schauer et al., 2003; Brown et al., 2005; Ghiglione et al.,
2005; Morris et al., 2005; Mary et al., 2006; Alonso-Sáez
et al., 2007), to our knowledge only one has analysed the
seasonality in the processing of different components of
the dissolved organic matter (DOM) pool (Alonso-Sáez
and Gasol, 2007).
Novel methods to link bacterial diversity and bio-
geochemical activity include the search and affiliation of
specific genes in metagenome analyses (e.g. Béjà et al.,
2002) and the single cell biogeochemistry analysis
techniques. Among the latter, the techniques that have
been applied with greatest success involve the use of
radioisotope substrates: MARFISH, a combination of
microautoradiography (MAR) and fluorescence in situ
hybridization of RNA (FISH) (Ouverney and Furhman,
1999; Lee et al., 1999; Cottrell and Kirchman, 2000), and
flow cytometry cell sorting (e.g. Servais et al., 2003). A
critical issue of these techniques is the choice of model
molecules from the complex mixture of the DOM pool,
which are representative of major matter fluxes in the sea.
Dimethylsulfoniopropionate (DMSP) is an ubiquitous
compound in the upper ocean, where it represents a
Received 27 January, 2007; accepted 13 May, 2007. *For
correspondence. E-mail rsimo@icm.csic.es; Tel. (+34) 932309590;
Fax (+34) 932309555. Present addresses:
†
Instituto de Investiga-
ciones Biológicas Clemente Estable, Av. Italia 3318, CP11600,
Montevideo, Uruguay;
‡
Limnological Station, Institute of Plant
Biology, Seestr. 187, CH-8802 Kilchberg, Switzerland.
Environmental Microbiology (2007) 9(10), 2451–2463 doi:10.1111/j.1462-2920.2007.01363.x
© 2007 The Authors
Journal compilation © 2007 Society for Applied Microbiology and Blackwell Publishing Ltd