Journal of Experimental Marine Biology and Ecology 256 2001 185–198
www.elsevier.nl locate jembe
DMSP-consuming bacteria associated with the calanoid copepod Acartia tonsa Dana
Kam W. Tang , Pieter T. Visscher, Hans G. Dam
Department of Marine Sciences , University of Connecticut, 1084 Shennecossett Road, Groton, CT 06340,
USA Received 20 April 2000; received in revised form 4 October 2000; accepted 20 October 2000
Abstract
DMSP-consuming bacteria DCB were recovered from the body and fecal pellets of the copepod Acartia tonsa Dana. The most probable number of DCB associated with starved A
.
2 21
tonsa was 9.2 3 10 cells copepod . The abundance of DCB recovered from the copepod body
4
increased to 1.6–2.8 3 10 after the copepod fed on DMSP-containing alga. DCB abundance
4 21
associated with fecal pellets averaged 1.2 3 10 cells pellet . In enrichment cultures, the DCB
21
grew with a doubling time of 1.1–2.9 days, and consumed DMSP at a rate of 4.5–7.5 fmol cell
21
day . The apparent DMSP-to-DMS conversion efficiency was 25–41 for DCB from copepod
body, and 99 for DCB from fecal pellets. Our study demonstrated that copepods and their fecal pellets may harbour dense populations of DCB, and that the copepod–bacteria coupling represents
a novel mechanism for DMSP consumption in the water column.
2001 Elsevier Science B.V. All rights reserved.
Keywords : Acartia tonsa; DMS; DMSP; Fecal pellets; Most probable number
1. Introduction
The climatologically active sulfur compound, dimethylsulfide DMS, can be formed by biological and chemical cleavage of dimethylsulfoniopropionate DMSP, a widely
distributed organic sulfur compound in the ocean Kettle et al., 1999. Although free-living, DMSP-cleaving bacteria are ubiquitous in the marine environment Diaz et
al., 1992; Visscher et al., 1992, 1994; Ledyard and Dacey, 1994, field measurements
˚
Corresponding author. Present address: Danish Institute for Fisheries Research, Kavelergarden 6, Charlotten- lund DK-2920, Denmark. Tel.: 145-3-396-3421; fax: 145-3-396-3434.
E-mail address : ktadfu.min.dk K.W. Tang.
0022-0981 01 – see front matter
2001 Elsevier Science B.V. All rights reserved. P I I : S 0 0 2 2 - 0 9 8 1 0 0 0 0 3 1 4 - 2
186 K
.W. Tang et al. J. Exp. Mar. Biol. Ecol. 256 2001 185 –198
usually reveal a weak correlation between DMS and particulate and dissolved DMSP concentrations Kettle et al., 1999, implicating the existence of other biogeochemical
sinks for DMSP and DMS. DMSP may undergo various microbial degradation pathways without the production
of DMS, such as demethylation and demethiolation Taylor and Gilchrist, 1991; Visscher and Taylor, 1994. Growing evidence shows that non-DMS producing
pathways are perhaps more common than DMSP cleavage in the marine environment Kiene and Service, 1991; Kiene, 1992; Visscher et al., 1992; Ledyard and Dacey,
35
1996. Using radioactive S-DMSP, Kiene et al. 1999 showed that marine bacteria
could incorporate a major portion of the DMSP-sulfur into amino acids and proteins. Bacteria that grow solely on DMSP as organic carbon source have also been isolated
from various oceanic settings Diaz et al., 1992; Visscher et al., 1992; Ledyard et al., 1993; Ledyard and Dacey, 1994; Visscher and Taylor, 1994. All these observations
point to the importance of bacteria in DMSP dynamics, and the existence of many different microbial–biochemical pathways for DMSP.
DMSP in phytoplankton may also be channeled to micro- and meso-grazers Wolfe et al., 1994; Kwint et al., 1996; Tang et al., 1999; Tang, 2000a, leading to an uncoupling
between the production of DMSP and DMS. Copepods are the dominant mesograzers in the ocean, and they play various roles in determining the fate of oceanic DMSP.
Copepods may release dissolved DMSP through grazing Dacey and Wakeham, 1986 and osmoregulation Tang et al., 2000a, retain DMSP in biomass Kwint et al., 1996;
Tang et al., 1999, 2000a, or repackage ingested DMSP into fecal material, which may be recycled or exported to deeper waters Kwint et al., 1996.
Copepod fecal pellets are often colonized by numerous bacteria that play a major role in remineralization of the fecal material Gowing and Silver, 1983; Jacobsen and Azam,
1984; Hansen et al., 1996. A field study has shown that microbial degradation of copepod fecal pellets may account for 100 of annual DOC production in the central
Greenland Sea Urban-Rich, 1999. Bacteria associated with copepod fecal pellets can use a wide variety of substrates Delille and Razouls, 1994; Hansen and Bech, 1996,
and their consumption of DMSP has been speculated Dacey and Wakeham, 1986. Tang 2000b showed that the copepod Acartia tonsa incorporated DMSP in fecal
pellets when fed the DMSP-containing alga Tetraselmis impellucida, and that DMSP concentration within the pellets was in the range of mM, which is orders of magnitude
higher than typical dissolved and particulate DMSP concentrations in the ocean Kettle et al., 1999. Therefore, these fecal pellets may act as ‘hot spots’ for microbial DMSP
consumption in the water column. In addition to fecal pellets, the body surface and intestines of copepods are also colonized by bacteria Nagasawa et al., 1985; Delille and
Razouls, 1994; Hansen and Bech, 1996. While these bacteria do not necessarily rely on the copepods for survival, by hitch-hiking on the copepods, they can exploit the
concentrated dissolved organic matter usually associated with the food patch located near the copepods, or the dissolved organic matter which results from food ingestion and
digestion by the copepods Carman, 1994. Tang et al. 2000b showed that field- collected copepods contain DMSP in their bodies, and the amount of DMSP per unit
biovolume ranged from mM to mM, which is several orders of magnitude higher than the ambient seston and dissolved DMSP concentrations. Therefore, copepod bodies
K .W. Tang et al. J. Exp. Mar. Biol. Ecol. 256 2001 185 –198
187
represent highly concentrated pockets of DMSP in the water column, and may also act as ‘hot spots’ for microbial DMSP consumption.
In the present study, we quantified DMSP-consuming bacteria DCB associated with the body and fecal pellets of the copepod A
. tonsa, using the most probable number MPN method. We also studied the growth of the DCB on DMSP in enrichment
cultures. Our results show that the copepod body and fecal pellets contained dense populations of DCB, whose activity may have important implications for the fate of
DMSP in the water column.
2. Material and methods
