DIMETHYLSULFONIOPROPIONATE CLEAVAGE BY MARINE PHYTOPLANKTON IN RESPONSE TO MECHANICAL, CHEMICAL, OR DARK STRESS¹

Abstract

Several bloom‐forming marine algae produce concentrated intracellular dimethylsulfoniopropionate (DMSP) and display high DMSP cleavage activity in vitro and during lysis after grazing or viral attack. Here we show evidence for cleavage of DMSP in response to environmental cues among different strains of the haptophyte Emiliania huxleyi (Lohmann) Hay et Mohler and the dinoflagellate Alexandrium spp. (Halim). Sparging or shaking live cells of either taxon increased dimethyl sulfide (DMS), especially in dinoflagellates, known to be very sensitive to shear stresses. Additions of polyamines, known triggers of exocytosis in some protists, also stimulated DMSP cleavage in a dose‐responsive manner. We observed DMS production by some algae after shifts in light regime. When most exponential‐phase E. huxleyi were transferred to continuous darkness, cells decreased in volume and DMSP content within 24 h; DMSP content per unit cell volume remained relatively steady. DMS accumulated as long as cells remained in the dark, but on returning to a light:dark cycle DMS accumulation ceased within 24 h. However, E. huxleyi strain CCMP 373, containing highly active in vitro DMSP lyase, produced only transient accumulations of DMS in the dark. This was apparently due to production and concomitant oxidation or uptake of DMS, because cells of this strain rapidly removed DMS added to cultures. Three strains of the dinoflagellate Alexandrium tamarense containing high in vitro DMSP lyase activity showed no DMS production in the dark, and all appeared to remove additions of DMS. Alexandrium tamarense strain CCMP 1771 also removed dimethyl disulfide, an inhibitor of bacterial DMS consumption. These data suggest that physical or chemical cues can trigger algal DMSP cleavage, but DMS production may be masked by subsequent oxidation and/or uptake.

Annual cycle of dimethylsulfoniopropionate (DMSP) and dimethylsulfoxide (DMSO) related to phytoplankton succession in the Southern North Sea

“…Overall, maximum DMSP t and DMS values associated to the Phaeocystis bloom in this near-shore shallow and very productive coastal environment (1740 and 250 nmol L − 1 , respectively) were one to two orders of magnitude higher than those typically encountered in open oceanic waters, as well as those in the deeper stratified northern North Sea even during blooms of high DMSP producing coccolithophorids. Wolfe et al, 2002 …”

In vivo DMSP‐biosynthesis measurements using stable‐isotope incorporation and proton‐transfer‐reaction mass spectrometry (PTR‐MS)

“…Hence, we might have underestimated A, and as a consequence also B, when conversion or exudation of DMSP took place during the growth phase. We have reason to believe that this is a minor part of the particulate fraction (van Rijssel and Gieskes 2002;Wolfe et al 2002), but even when it is substantial, this would not have affected the results substantially: A doubling of A, and hence an almost doubling of B, would have resulted in a lower calculated 64 MP eq by only 1% and hence an increase of the equilibrium fractionation factors (α EQ ) by 2%.…”

The relative significance of viral lysis and microzooplankton grazing as pathways of dimethylsulfoniopropionate (DMSP) cleavage: An Emiliania huxleyi culture study

“…DMSP and its cleavage products generated via the action of DL have been suggested to have many functions within the cell relating to metabolic processes and maintaining homeostasis (for more details see Stefels 2000; Simo 2001), for example as an antioxidant cascade (Sunda et al 2002). DMSP and its downstream products have also been implicated in cellular defense against grazing (Wolfe et al 1997) and viral infection (Evans et al 2006b). …”

“…Autolysis (Nguyen et al 1988), grazing (Dacey and Wakeham 1986), viral lysis , and mechanical and chemical stress (Wolfe et al 2002) have all been shown to increase DMS production. During grazing by Oxyrrhis marina on Emiliania huxleyi it was established that the concentration of DMS generated was directly related to the activity of the DL of the prey organism (Wolfe and Steinke 1996). Previously DMS production during viral lysis of phytoplankton has only been shown in the presence of bacteria (Hill et al 1998).…”