Generally, most of the biomass produced in Phaeocystis blooms is remineralized in the water column (Wassmann 1994, Rousseau et al. 2000) by heterotrophic bacteria. Occasionally, however, accumulation of DOM and foam have been reported (e.g. Eberlein et al. 1985; Lancelot et al. 1987; Seuront et al., 2007). This seems to indicate that bacterial degradation of organic matter produced by in Phaeocystis blooms varies between blooms, and sometimes is hampered. There may be various reasons for slow degradation and they may be different in different stages of a bloom.
During the growth phase of a bloom of P. antarctica all DOM produced was found to be rapidly degraded by bacteria (Smith et al. 1998). With time, however, the composition and contribution of organic matter that can be utilized by bacteria will change from readily degradable freshly excreted DOM during the growth phase, to the DOM dominated by mucopolysaccharides and glucan during the senescent stage. In laboratory experiments it was shown that carbohydrates derived from P. globosa and P. pouchetii colonies were readily degraded by bacterial communities under both oxic and anoxic conditions (Osinga et al. 1997; Janse et al. 1999). The degradation rate of glucan was higher than that of mucopoly-saccharides (Osinga et al. 1997), but during degradation of the mucopolysaccharides the sugar composition of the mucopolysaccharides remained unchanged. Therefore, there is no indication of refractory parts within the mucopolysaccharide fraction (Janse et al. 1999).
Identification of bacteria involved in muco-polysaccharide degradation in cultures and a mesocosm revealed the presence of bacteria from different phylogenetic groups, such as a- and y-Proteobacteria, Cytophaga-Flavobacter (CF) cluster of the Bacteroidetes and the Planktomy-cetes and Verrucomicrobiales clade (Janse et al. 2000; Brussaard et al. 2005b; Alderkamp et al 2006b). During a P. globosa bloom in a mesocosm the bacterial community showed distinct changes with time (Brussaard et al. 2005b). The nature of the phytoplankton growth controlling substrate (i.e., N or P) did not influence the microbial community. In addition, since the species composition of the bacterial community remained unchanged during mucopolysaccharide degradation, degradation of mucopolysaccharides in itself does not require a succession of species (Janse et al. 2000). Therefore, the changes in the micro-bial community were likely induced by the growth stage of the P. globosa bloom and enhanced cell lysis and concomitant release of DOM during the senescent stage (Brussaard et al. 2005b). Degradation of polymers requires specialized extracellular enzyme systems to hydrolyze polymers prior to uptake by bacteria. These enzymes can be attached to the bacterial cell (ectoenzymes), or free extracellular enzymes (Chrost 1991). Arrieta and Herndl (2002) revealed a succession of different types of bacterial b-glucosidases during a P. globosa bloom, which was related to a change in the bacterial community. Therefore, the copious amounts of glucan and mucopolysaccharides produced during a Phaeocystis bloom may shape the composition of bacterial communities specialized in degradation of complex carbohydrates. Bacteria appearing during the senescent stage of the P. globosa bloom in the mesocosm mainly belonged to the a-Proteobacteria and CF cluster of the Bacteroidetes (Brussaard et al. 2005b). In the coastal North Sea, bacteria from CF clusters of the Bacteroidetes were dominant during and following a bloom of P. globosa (A. C. Alder-kamp et al. 2006b). Members of the CF cluster are chemo-organotrophic, and known for their capacity to degrade complex carbohydrates such as pectin, cellulose and chitin (Reichenbach and Dworkin 1991; Cottrell and Kirchman 2000; Kirchman 2002). Therefore, it may be that certain taxa of this cluster have adapted specifically to degradation of complex mucopolysaccharides produced by Phaeocystis.
Mineral nutrient limitation of microbial degradation has been put forward as an explanation for accumulation of carbon-rich DOM after a Phae-ocystis bloom (Thingstad and Billen 1994). The increase in carbohydrate/POC due to overflow metabolism will give rise to a substrate with a C/P and C/N ratio that is unfavorable to bacteria. Since the C/P ratio of bacteria may be considerably lower than that of phytoplankton (Vadstein et al. 1988), especially phosphate limitation may hamper microbial degradation (Thingstad et al.
1997). In addition, since P. antarctica was found to remove more CO2 per mole of phosphate than do diatoms (Arrigo et al. 1999), phosphate limitation during bacterial degradation of Phaeocystis material may be more severe than during degradation of diatom material. Indeed, while bacterial growth was carbon limited during the growth phase of a bloom of P. globosa, bacterial growth was colimited by carbon and phosphate during the massive release of the glucan and mucopoly-saccharides at the end of the bloom (Kuipers and Van Noort, in preperation). This may impede degradation of carbohydrates that are otherwise easily degradable, and prolong the degradation times.
Marine gels likely have an effect on microbial degradation of organic matter, yet few studies have examined this effect directly. Based on the current knowledge, gel formation may either enhance or slow down degradation of organic matter. In general HMW-DOC and gels have a higher rate of biodegradation and turnover than LMW-DOC (Amon and Benner 1996). Gels may serve as nutrient and/or attachment surfaces and offer hot-spots of high substrate concentrations for bacteria. They form enclosed microenvironments of substrate for bacteria to colonize, release their extracellular enzymes and efficiently take up the degradation products at high local concentrations (Azam 1998; Azam and Long 2001). Indeed, following a P. globosa bloom bacteria attached to particles were more active than the free-living community (Becquevort et al.
1998). On the other hand, assembly of free polymers into gels may complicate degradation.
Enzymatic degradation of carbohydrates that form insoluble gels was approximately 50 times slower than degradation of polymers composed of the same monomer linkages, but not forming gels (Alderkamp et al. 2007). If this difference is exemplary of the difference in degradation potential of 'free' polymers and polymers embedded in a gel, turnover times may slow down from days to years.
Microbial degradation dissolves the hydrogels when hydrolysis rates exceed the carbon demand of the bacteria, thereby releasing LMW products from the hydrogels (Smith et al. 1992; Fig. 3). Moreover, the kinetic properties of bacterial enzyme systems may result in the release of oligomers at a higher rate than the release of monomers that can be directly incorporated by the bacteria, resulting in release of LMW and medium molecular-weight (MMW) products (Alderkamp et al. 2007). In addition, polymer photocleavage by ultraviolet radiation can shorten polymer chains making tangled networks unstable (Edwards 1986) and can readily disperse marine polymer gel matrices (Orellana and Verdugo 2003). These three processes produce a random fragmentation, yielding LMW products that may be readily incorporated and metabolized by bacteria (Mopper et al. 1991; Moran and Zepp 1997; Mopper and Kieber 2001), adding to a rapid degradation of the organic matter in hydrogels. On the other hand, polymers may be released that are too large to be transported by bacterial permeases, yet too small to assemble into stable networks that bacteria can colonize and efficiently degrade with their extracellular enzymes. These polymers, indicated as DOM (MMW-DOM) in Fig. 3, may contribute to the formation of refractory DOM.
Bacterial activity may also increase aggregation of gels (Fig. 3). Studies on bacterial exopoly-mer production suggest that a significant portion of assimilated carbon is incorporated into exo-polymer capsular envelopes (Stoderegger and Herndl 1998). These capsular exopolymers increase aggregation probabilities of phytoplankton and other particles and act as stabilizers of already existing aggregates (Allison and Sutherland 1987; Decho 1990; Heissenberger and Her-ndl 1994). In addition, bacterial exopolymers are
Fig. 3 Conceptual representation of biotic and abiotic processes altering the size and recalcitrance of organic matter. (Abbreviations as in Fig. 1, MMW-DOM: medium-molecular-weight DOM)
resistant against bacterial enzymatic degradation, since a considerable fraction of bacterial extracellular enzymes are embedded in the exopoly-mer capsule. Therefore, release of bacterial derived exopolymers decreases the degradation potential of hydrogels. Finally, selective degradation of readily degradable compounds may alter the composition of the gels, and decrease the degradation potential of the remaining gel (San-nigrahi et al. 2005). At present it is not known to what extent the mechanisms discussed above influence microbial degradation of hydrogels. Therefore, microbial degradation of Phaeocystis derived DOM may either be enhanced or hampered by formation of hydrogels.
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