Aerobic degradation of phytoplankton debris dominated by Phaeocystis sp. in different physiological stages of growth

Osinga, Ronald; deVries, KA; Lewis, WE; vanRaaphorst, W; Dijkhuizen, Lubbert; vanDuyl, FC

doi:10.3354/ame012011

Cited by 27 publications

(21 citation statements)

References 19 publications

(22 reference statements)

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“…The absence of acrylate is most likely due to rapid conversion, a finding that was also noted by Ansede et al (2), who, using nuclear magnetic resonance analysis, were unable to detect acrylate production by a Roseobacter species even though DMS was produced. The present results also agree with environmental studies that show rapid degradation of acrylate by bacterial communities associated with algal cells or debris (34).…”

Section: Discussionsupporting

confidence: 82%

Dimethylsulfoniopropionate Metabolism by Pfiesteria -Associated Roseobacter spp

Miller

Belas

2004

Appl Environ Microbiol

104

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The Roseobacter clade of marine bacteria is often found associated with dinoflagellates, one of the major producers of dimethylsulfoniopropionate (DMSP). In this study, we tested the hypothesis that Roseobacter species have developed a physiological relationship with DMSP-producing dinoflagellates mediated by the metabolism of DMSP. DMSP was measured in Pfiesteria and Pfiesteria-like (Cryptoperidiniopsis) dinoflagellates, and the identities and metabolic potentials of the associated Roseobacter species to degrade DMSP were determined. Both Pfiesteria piscicida and Pfiesteria shumwayae produce DMSP with an average intracellular concentration of 3.8 M. Cultures of P. piscicida or Cryptoperidiniopsis sp. that included both the dinoflagellates and their associated bacteria rapidly catabolized 200 M DMSP (within 30 h), and the rate of catabolism was much higher for P. piscicida cultures than for P. shumwayae cultures. The community of bacteria from P. piscicida and Cryptoperidiniopsis cultures degraded DMSP with the production of dimethylsulfide (DMS) and acrylate, followed by 3-methylmercaptopropionate (MMPA) and methanethiol (MeSH). Four DMSP-degrading bacteria were isolated from the P. piscicida cultures and found to be taxonomically related to Roseobacter species. All four isolates produced MMPA from DMSP. Two of the strains also produced MeSH and DMS, indicating that they are capable of utilizing both the lyase and demethylation pathways. The diverse metabolism of DMSP by the dinoflagellate-associated Roseobacter spp. offers evidence consistent with a hypothesis that these bacteria benefit from association with DMSP-producing dinoflagellates.

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Section: Discussionsupporting

confidence: 82%

Dimethylsulfoniopropionate Metabolism by Pfiesteria -Associated Roseobacter spp

Miller

Belas

2004

Appl Environ Microbiol

104

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“…Breakdown rates for mucopolysaccharides-The breakdown rate for mucopolysaccharides (50% in 11 d) was lower than that reported for the rapidly degradable fraction of Phaeocystis by Osinga et al (1997) (50% in 2-3 d). However, it is much higher than the rate they found for a slowly degradable fraction (80-99% in 1 yr).…”

Section: Effect Of Inhibitors On Mucopolysaccharide Degradation-mentioning

confidence: 62%

“…In addition, the relatively constant, complex composition of mucus carbohydrates throughout various spring blooms (Janse et al 1996a) could be interpreted as an indication for the absence of significant degradation. In the only direct study on the biodegradability of Phaeocystis, Osinga et al (1997) found that marine bacteria are able to degrade part of the Phaeocystis biomass. However, as degradation was only monitored by total organic carbon (TOC) measurements of nonpurified biomass, nothing could be concluded about the nature of the organic matter that was degraded or about the colony components it was derived from.…”

Section: Acknowledgmentsmentioning

confidence: 99%

Microbial breakdown of Phaeocystis mucopolysaccharides

Janse

Rijssel

Ottema

et al. 1999

Limnology & Oceanography

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Mucus from the microalga Phaeocystis was partially purified and used as the C source in various stable enrichment cultures wherein the mucus carbohydrates were degraded under oxic as well as anoxic conditions. The breakdown of mucopolysaccharides (initially at a rate of 50% in 11 d at 12ЊC) markedly slowed after about 15 d, leaving a fraction nondegraded. The carbohydrate composition of the residual fraction did not change during breakdown. It was shown that the incomplete degradation of mucopolysaccharides was not due to inherent resistance to breakdown in parts of the mucus carbohydrates but to the release of inhibitors produced during breakdown. The (potentially high) overall degradability of mucopolysaccharides has important consequences for the fate of C fixed by Phaeocystis. The balance between recycling of Phaeocystis biomass in surface waters and its accumulation, sedimentation, and burial in the sediment will greatly depend on factors such as nutrient availability, presence of inhibiting agents, and composition of the microbial community, rather than on structural impediments inhibiting mucopolysaccharide degradation.

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“…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 mucopolysaccharides (Osinga et al 1997), but during degradation of the mucopolysaccharides the sugar composition of the mucopolysaccharides remained unchanged.…”

Section: Microbial Degradation Of Phaeocystis Carbohydratesmentioning

confidence: 99%

“…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 mucopolysaccharides (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).…”

Section: Microbial Degradation Of Phaeocystis Carbohydratesmentioning

confidence: 99%

The carbohydrates of Phaeocystis and their degradation in the microbial food web

2007

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The ubiquity and high productivity associated with blooms of colonial Phaeocystis makes it an important contributor to the global carbon cycle. During blooms organic matter that is rich in carbohydrates is produced. We distinguish five different pools of carbohydrates produced by Phaeocystis. Like all plants and algal cells, both solitary and colonial cells produce (1) structural carbohydrates, (hetero) polysaccharides that are mainly part of the cell wall, (2) mono-and oligosaccharides, which are present as intermediates in the synthesis and catabolism of cell components, and (3) intracellular storage glucan. Colonial cells of Phaeocystis excrete (4) mucopolysaccharides, heteropolysaccharides that are the main constituent of the mucous colony matrix and (5) dissolved organic matter (DOM) rich in carbohydrates, which is mainly excreted by colonial cells. In this review the characteristics of these pools are discussed and quantitative data are summarized. During the exponential growth phase, the ratio of carbohydrate-carbon (C) to particulate organic carbon (POC) is approximately 0.1. When nutrients are limited, Phaeocystis blooms reach a stationary growth phase, during which excess energy is stored as carbohydrates. This so-called overflow metabolism increases the ratio of carbohydrate-C to POC to 0.4-0.6 during the stationary phase, leading to an increase in the C/N and C/P ratios of Phaeocystis organic matter. Overflow metabolism can be channeled towards both glucan and mucopolysaccharides. Summarizing the available data reveals that during the stationary phase of a bloom glucan contributes 0-51% to POC, whereas mucopolysaccharides contribute 5-60%. At the end of a bloom, lysis of Phaeocystis cells and deterioration of colonies leads to a massive release of DOM rich in glucan and mucopolysaccharides. Laboratory studies have revealed that this organic matter is potentially readily degradable by heterotrophic bacteria. However, observations in the field of accumulation of DOM and foam indicate that microbial degradation is hampered. The high C/N and C/P ratios of Phaeocystis organic matter may lead to nutrient limitation of microbial degradation, thereby prolonging degradation times. Over time polysaccharides tend to self-assemble into hydrogels. This may have a profound effect on carbon cycling, since hydrogels provide a vehicle to move DOM up the size spectrum to sizes subject to sedimentation. In

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Aerobic degradation of phytoplankton debris dominated by Phaeocystis sp. in different physiological stages of growth

Cited by 27 publications

References 19 publications

Dimethylsulfoniopropionate Metabolism by Pfiesteria -Associated Roseobacter spp

Dimethylsulfoniopropionate Metabolism by Pfiesteria -Associated Roseobacter spp

Microbial breakdown of Phaeocystis mucopolysaccharides

The carbohydrates of Phaeocystis and their degradation in the microbial food web

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