Chemical defense in the microplankton II: Inhibition of protist feeding by β‐dimethylsulfoniopropionate (DMSP)

Abstract

Examples of chemical defenses and their influence on predator-prey interactions abound in the terrestrial and marine benthic ecological literature. In contrast, considerably less is known about the role of chemical defenses in marine planktonic systems. In this study, we examined the potential for the phytoplankton-produced compound dimethylsulfoniopropionate (DMSP) and its cleavage products dimethyl sulfide (DMS) and acrylate to act as chemical defenses in seawater. Although added DMS and acrylate had no effect on protist grazers, added DMSP reduced grazing on the coccolithophorid Emiliania huxleyi by all four tested species (dinoflagellates Amphidinium longum, Gymnodinium sp., and Oxyrrhis marina and ciliate Coxliella sp.). A. longum and Gymnodinium were highly sensitive to 20-mol L Ϫ1 concentrations of DMSP, nearly ceasing to feed, whereas O. marina and Coxliella showed only minor reductions in grazing activity. Grazing suppression in A. longum was DMSP concentration-dependent over the range 0.05 to 1,000 mol L Ϫ1 and was also inhibited by added glycine betaine, a structural analog of DMSP. DMSP reduced A. longum grazing by similar amounts on five different algal species, some of which do not produce DMSP on their own. Thus, the efficacy of DMSP as a grazing deterrent appears to depend on grazer species, but not on algal strain or species. Because DMSP does not seem to be toxic, we hypothesize that DMSP and related compounds act as signals for the presence of potentially harmful algal cells. Should such sublethal chemical defense interactions be widespread in nature, they could be important in regulating the composition and biomass of phytoplankton communities.Chemical defenses against grazers, along with other grazing deterrence strategies, should be evolutionarily favored in marine phytoplankton. This is because most marine phytoplankton production is grazed by planktonic protists, both in coastal and in oceanic waters (Verity et al. 1993;Neuer and Cowles 1994;Landry et al. 1997). Thus, adaptations yielding even slight protection against protist grazing should confer a significant competitive advantage for a given phytoplankton strain or species (Strom in press).Some phytoplankton species are known to be toxic to planktonic protists: contact with or ingestion of these cells results in death (Hansen 1989;Uchida et al. 1995;Kamiyama and Arima 1997). Sublethal defenses, known to be widespread in other ecosystems, have been much less studied in planktonic communities. If present, sublethal grazing deterrents could play a role in shaping phytoplankton community structure. For example, it has been hypothesized that suppression of grazing is an important element in the formation and persistence of phytoplankton blooms, including blooms of ''harmful'' taxa (Turner and Tester 1997). Wolfe et al. (1997) have hypothesized that the cleavage of dimethylsulfoniopropionate (DMSP) into dimethyl sulfide (DMS) and acrylate constitutes a chemical defense against 1 Present address: Department of Biological Sciences, Ca...

Chemical defense in the microplankton I: Feeding and growth rates of heterotrophic protists on the DMS‐producing phytoplankter Emiliania huxleyi

“…Dissolved cues could be closely associated with the area around individual prey cells, and there has been considerable speculation that phytoplankton cells in general exist within a ''phycosphere'' of emitted, dissolved substances (e.g., Azam and Ammerman 1984). In additional research, we have shown that added DMSP causes feeding reductions in protists at low levels (mol L Ϫ1 , Strom et al 2003). Although bulk DMSP levels in seawater are typically less than this (e.g., Cantin et al 1996;Dacey et al 1998), higher local concentrations could easily be achieved by a pulse-like release from a prey cell (Wolfe 2000).…”

“…1) were isolated from local marine waters and maintained in sterile filtered seawater with dilute trace metal additions (henceforth ''ciliate medium,' ' Gifford 1985). These protists were fed a mixed diet of phytoplankton as optimized in growth trials (Strom and Morello 1998) and maintained at 12ЊC in dim light on a 14 : 10 LD cycle. Maintenance cultures were fed once or twice per week and transferred weekly.…”

“…By contrasting protist feeding and growth responses to high-lyase (HL) and low-lyase (LL) strains, we were able to gain insight into the potential for DMSP cleavage to act as a chemical defense. Related components of this work are presented separately, including algal initiation of DMSP cleavage (Wolfe et al 2002), the effects of DMSP and related compounds on grazers (Strom et al 2003), and a detailed study of feeding mechanisms and ultrastructure in one grazer, Amphidinium longum (Jacobson et al pers. comm.).…”

Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling

“…Such a mechanism could also be partly responsible for the significantly reduced feeding levels on high-lyase phytoplankton by other microzooplankton taxa (Strom et al 2003a;Wolfe 2000). However, it was recently suggested that DMSP rather than acrylate is the active deterrent of microzooplankton grazing (Strom et al 2003b) and readers are directed to the paper presented by Nejstgard et al (this issue) for a discussion on this subject. A few field experiments have combined the determination of microzooplankton grazing rates (the Landry-Hassett dilution technique) with DMS(P) analyses and have shown that DMSP-containing algal species may be proportionally less grazed than total algal biomass (Archer et al 2001b;Olson and Strom 2002;Wolfe et al 2000).…”

Copepods induce paralytic shellfish toxin production in marine dinoflagellates

“…Furthermore, injury induced cleavage of dimethylsulphonopropionate into dimethylsulphide (DMS) and acrylate that deters protozoan consumers has been suggested to occur in the bloom-forming coccolithophorid Emiliana huxleyi (Wolfe et al 1997), and the formation of terratogenic aldehydes from fatty acid precursors is induced by injury in several diatoms (Miralto et al 1999). However, the natural function of acrylate and DMS, as well as terratogenic aldehydes, has been questioned (Irigoien et al 2002;Strom et al 2003). Signal induced toxin production has previously been reported for the limnic cyanobacteria Microcystis aeruginosa, which was shown to produce more microcystins upon encounter with grazers or waterborne cues from grazers ( Jang et al 2003).…”