Mechanisms of DOM release during a Phaeocystis bloom

In general 10-25% of phytoplankton primary production is released as DOC (Sharp 1977; Larsson and Hagstrom 1979; Lignell 1990; Teira et al. 2003; Maranon et al. 2004). The three main mechanisms of DOM production are: (1) release after cell lysis, e.g., as a result of viral infection, zooplankton sloppy feeding and egestion, (2) bacterial cleavage of exopolysaccharides (Smith et al. 1995), or (3) direct release as a physiological process of intact cells (reviewed by Nagata 2000). Two physiological mechanisms of DOM production have been advocated: a passive diffusion of small metabolites through the cell membrane (Bj0rnsen 1988) and an overflow mechanism whereby excess photosynthetic products are actively released when the C fixation rate exceeds the rate of macromolecular production (Fogg 1983).

During the exponential growth phase of a Phaeocystis bloom DOM release as a result of non-physiological processes will be low. In a P. globosa bloom rates of cell lysis were low in the growth phase (Van Boekel et al. 1992; Brussaard et al. 1995, 1996, 2005a), therefore DOM release as a result of cell lysis will be insignificant. Since Phaeocystis colonies largely escape grazing control (Breteler and Koski 2003; Nejstgaard et al. 2007), sloppy feeding will not be a cause of significant DOM release either. In a diatom bloom it was shown that bacteria colonized healthy, actively growing Chaetoceros and Tha-lassiosira cells with high ectoenzyme activity. When the hydrolysis rate of phytoplankton surface material by bacteria exceeds the uptake rate, DOM will be released into the environment (Smith et al. 1995). Although the growth phase of P. globosa blooms are typically accompanied by an increase in bacterial numbers, bacterial production, and enzyme activity (Billen and Fontigny 1987; Van Boekel et al. 1992; Putt et al. 1994; Becquevort et al. 1998; Arrieta and Herndl 2002; Brussaard et al. 1996, 2005b), young healthy colonies are generally free of bacteria (Thingstad and Billen 1994; Lancelot and Rousseau 1994). Therefore, it is unlikely that hydrolysis of the mucous matrix by bacteria will lead to significant DOM production during the growth phase of the bloom. The only significant mechanisms for DOM production is probably direct release of DOM from healthy cells. During all growth stages DOM excretion from healthy cells was observed in cultures of Phaeocystis sp. (Biddanda and Benner 1997). Since DOM excretion rates are low (see above) on the whole DOM release during the growth phase of the bloom will be low.

During the stationary phase of a bloom, however, DOM release increases. During the stationary phase colonies become disrupted, and flagellate cells develop within the colonies (Pe-perzak et al. 2000). Due to the overflow production of mucopolysaccharides and glucan, the ratio of carbohydrates-C to POC increases. During this phase of a bloom DOM production through non-physiological processes will be high. Cell lysis rates of up to 33% day-1 were observed at the peak of P. globosa blooms (Van Boekel et al. 1992; Brussaard et al. 1995, 1996, 2005a). In this way the carbohydrate rich cell content is released as DOM. When the flagellate cells that develop inside colonies detach from the colony matrix, they are readily grazed upon by microzooplankton (Weisse and Scheffel-Moser 1990; Tang et al. 2001). This leads to DOM release by egestion of the microzooplankton. During the stationary phase of a bloom, bacterial communities attach to Phaeocystis colonies and to ghost colonies. Bacteria with high glucosidase activity are present in both free-living and particle-attached communities (Billen and Fontigny 1987; Becquevort et al. 1998). If hydrolysis rates of mucopolysac-charides from the colony matrix exceeds uptake of the sugars, the sugars and oligomers derived from mucopolysaccharides may be released as DOM.

The excess release of DOM under nutrient limitation has not been observed in Phaeocystis. In Phaeocystis sp. cultures DOC production was coupled to POC production at different growth stages (Biddanda and Benner 1997). Also in enclosures of P. antarctica, ratios of recently produced DOC increased only slightly after nutrient depletion (Smith et al. 1998; Carlson et al. 1998). This indicates that nutrient limitation does not lead to increased excretion of DOM resulting from an overflow mechanism.

Formation of hydrogels by Phaeocystis carbohydrates

Polysaccharides in aqueous environments may spontaneously assemble into hydrogels. These polymer gels can then penetrate neighboring gels, and anneal them together, increasing the size spectrum. Recent discoveries have highlighted the importance of polymer gels for biogeochem-ical cycling of organic carbon (see the review by Verdugo et al. 2004). As was discussed above, mucopolysaccharides spontaneously form polyan-ionic gels in aqueous solution. In addition to gel formation by mucopolysaccharides, b-1,3-glucans are also known to form non-ionic gels in aqueous solutions (Renn 1997; Kim et al. 2000). In general, gelling properties of b-glucans are dependent on the concentration of the molecules, their size, primary and secondary structure and temperature (Bohm and Kulicke 1999; Lazaridou et al. 2003). Therefore, gel-forming properties of laminarin in the marine environment are hard to predict. Preliminary results from our laboratory show that dissolving laminarin in seawater leads to an increase in viscosity, but to our knowledge no further investigations have been conducted to this end. Seuront et al. (2007) showed that Phae-ocystis derived polymeric matter could increase seawater viscosity up to two orders of magnitude. Because of the high aggregation potential of both glucan and mucopolysaccharides, the carbohydrates released during senescence of the Phaeo-cystis bloom will likely contribute to the increase in seawater viscosity (Fig. 2), thereby changing the physical nature and microscale structure of the organic matter encountered by bacteria.

Gels provide an abiotic vehicle to move organic molecules up the size spectrum to sizes capable of sedimentation, and may also constitute an intermediate in the formation of the foam often observed after Phaeocystis blooms (Fig. 2). Large gel particles, also known as transparent exopolymeric particles (TEP) can contribute significantly to sedimentation processes. This may be by direct sedimentation (Wassmann et al. 1990; Riebesell et al. 1995; Hong et al. 1997), or by acting as glue, adhering together organic matter present during a bloom and thus enhancing their contribution to a vertical flux (Passow and Wassmann 1994). Mari et al. (2005) showed that the properties of TEP produced under N or P limitation are different, as a result of which the export versus retention balance of the organic matter may be affected. It is tempting to speculate that the different N/P ratios may determine whether overflow metabolism is directed towards either glucan or mucopolysaccharide production. This would resemble the situation described for the diatom Cylindrotheca fusiformis, where P depletion leads to an increase in the ratio of heteropolysaccharides to glucan, compared to N-limitation (Magaletti et al. 2004). In this way the glucan/mucopolysaccharides ratio may influence properties of the hydrogels and TEP that is

Fig. 2 Conceptual representation of the formation of marine gels from different pools of Phaeocystis organic matter (after Verdugo et al. 2004). (abbreviations: LMW-DOM: low-molecular-weight DOM, HMW-DOM: high-molecular-weight DOM, POM: particulate organic matter, TEP: transparent exopolymeric particles)

formed, and thereby the degradation potential of Phaeocystis organic matter.

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