Dissolved Organic Nitrogen Hydrolysis Rates in Axenic Cultures of
            <i>Aureococcus anophagefferens</i>
            (Pelagophyceae): Comparison with Heterotrophic Bacteria

Berg, Gry Mine; Repeta, Daniel J.; LaRoche, Julie

doi:10.1128/aem.68.1.401-404.2002

Cited by 84 publications

(83 citation statements)

References 29 publications

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“…Given the low concentration of aminosugars (0.82% of the HMW DON pool in West Neck Bay pore water), they are probably not an important fraction of the DOM. In contrast to N-acetyl polysaccharides, the protein fraction of HMW DON appears to be directly bioavailable to A. anophagefferens on the basis of cell surface peptide hydrolysis measurements (Berg et al 2002;Mulholland et al 2002). The aminopeptide hydrolysis rate in A. anophagefferens cultures grown on HMW DON and NO is four times greater than Ϫ 3 in cultures grown on urea (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…We examined the potential for cell surface protein and chitin polymer breakdown using the fluorogenic substrates L-leucine-4-methylumbelliferylamide HCl (Leu-MUF; Fluka 61888) and 4-methylumbelliferyl-N-acetyl-␤-D-glucosaminide (MUF-GlcNAc; Sigma M2133) according to Berg et al (2002). A. anophagefferens demonstrated no extracellular chitinolytic activity (data not shown).…”

Section: Resultsmentioning

confidence: 99%

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The role of the picoeukaryote Aureococcus anophagefferens in cycling of marine high—molecular weight dissolved organic nitrogen

Berg

Repeta

LaRoche

2003

Limnology & Oceanography

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Environmental evidence suggests that Aureococcus anophagefferens (Pelagophyceae), a eukaryotic picoplankton that blooms in coastal seawaters, can outcompete other organisms because of its ability to use abundant dissolved organic nitrogen (DON). To test this hypothesis, we isolated A. anophagefferens in axenic culture and monitored its growth on high-molecular weight (HMW) DON collected from sediment pore waters, a putative source for DON in bays where blooms occur. HMW DON originating from pore water had a substantially higher protein content than surface seawater DON. We found that A. anophagefferens could deplete 25-36% of the available nitrogen in cultures with HMW DON as the sole source of nitrogen and that this corresponded well with the protein fraction in pore-water HMW DON. High rates of cell surface peptide hydrolysis and no detectable N-acetyl polysaccharide hydrolysis, together with the high percentage of hydrolyzable amino acids compared to hydrolyzable aminosugars present in the HMW DON, pointed to the protein fraction as the more likely source of nitrogen used for growth. Whether or not nitrogen scavenging from protein is a common mechanism in phytoplankton is at present unknown but needs to be investigated.Intense blooms of Aureococcus anophagefferens, or brown tides, were first observed in 1985 at three separate locations along the northeast coast of the United States (Cosper et al. 1987;Sieburth et al. 1988;Olsen 1989). The simultaneous occurrence of brown tides in geographically isolated regions along the U.S. East Coast suggested that regional-scale, climatological forcing might play a role in triggering the blooms. Yet, attempts to correlate bloom initiation with rainfall (Cosper et al. 1990) or wind stress (Vieira and Chant 1993) have failed to provide a consistent explanation for the bloom. In a review of historical data, LaRoche et al. (1997) hypothesized that brown tide blooms are controlled by interannual variability in the relative supply of dissolved inorganic and organic nitrogen, determined in part by groundwater flow. The supply of inorganic nitrogen through groundwater is greater than any other external source of nitrogen to Long Island bays, and a decrease in groundwater input coupled with a seasonal build-up of DON 1 To whom correspondence should be addressed. Present address: Alfred-Wegener Institute for Polar and Marine Research, Postfach 120161, Bremerhaven D-27515, Germany. AcknowledgmentsGrateful thanks to Silvio Pantoja for amino acid measurements, Silke Nissen for help with culture work, and Uwe Rabsch for help with logistics. This work was funded by grants OCE-9730015 and the Suffolk County Department of Health Services, Office of Ecology to D.J.R. and J.L.R., Deutsche Forschungsgemeinschaft grant RO 2138/3 to J.L.R., and a grant from the Alexander von Humboldt foundation to G.M.B.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

The role of the picoeukaryote Aureococcus anophagefferens in cycling of marine high—molecular weight dissolved organic nitrogen

Berg

Repeta

LaRoche

2003

Limnology & Oceanography

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“…Nevertheless, Aureococcus has been hypothesized to form brown tides using DON (Berg et al 1997;Lomas et al 2001). Subsequently, axenic cultures of Aureococcus were shown to utilize highmolecular-weight (HMW) DON and sustain growth on it (Berg et al 2002). Comparing Aureococcus and its nitrogen utilization capabilities with those of the prasinophyte Ostreococcus demonstrates how organisms lumped together at a broad functional level (e.g., photoautotrophs) often reside in different niches and will be subject to different long-and short-term ecological constraints.…”

Section: Photoautotrophsmentioning

confidence: 99%

Ecology and Diversity of Picoeukaryotes

Worden

Not

2008

Microbial Ecology of the Oceans

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105

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“…Growth on urea, urea uptake, or urease activity have been demonstrated for many different phytoplankton species (Carpenter et al 1972;Antia et al 1991;Collier et al 1999;Palinska et al 2000;Berg et al 2002), although not for many dinoflagellates. Urea is assimilated by hydrolysis to ammonia via either the enzyme urease or adenosine triphosphate (ATP) urea amidolyase in marine phytoplankton (Antia et al 1991).…”

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confidence: 99%

“…For instance, dinoflagellates have been associated with low nitrate and high ammonium or high dissolved organic nitrogen (DON) concentrations, which suggests that some species within this phytoplankton class may selectively use organic nitrogen sources (Paerl 1988;Berg et al 1997;Glibert and Terlizzi 1999). DON often represents a significant proportion of the total dissolved nitrogen pool (reviewed in Antia et al 1991).…”

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Urease activity in cultures and field populations of the toxic dinoflagellate Alexandrium

Dyhrman

Anderson

2003

Limnology & Oceanography

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Nitrogen availability is an important factor controlling phytoplankton abundance and species composition in marine waters. In addition to inorganic nitrogen, some phytoplankton species can use dissolved organic nitrogen sources such as urea for growth. Herein we demonstrate that axenic laboratory cultures of the toxic dinoflagellate, Alexandrium fundyense strain CB301A and A. catenella strain TN9A were able to grow on urea as a sole nitrogen source in the presence of nickel. This nickel dependence suggests that these Alexandrium species hydrolyze urea into ammonia with the enzyme urease rather than adenosine triphosphate urea amidolyase. Cells grown on urea had lower toxin content (15%-30%) than f/2-grown cells. In A. fundyense the urease enzyme appears to be nitrogenregulated. In culture experiments, enzyme activity was highest in nitrate-starved and urea-grown (replete) cells, whereas activity was undetectable in f/2-grown (replete) and phosphate-starved cells. Urease activity in ammoniagrown (replete) cells was also depressed. Urease activity also appeared to increase with decreasing nitrate-limited growth rate in semicontinuous cultures. May and June cruises in the Gulf of Maine followed the yearly bloom of A. fundyense. On average, inorganic nitrogen concentrations in May were higher than in June, whereas cell abundances, urea concentrations, and urease activity in May were lower than in June. The latter measurements relied on an immunomagnetic bead separation to isolate living A. fundyense cells from mixed phytoplankton samples for analysis. The differences between May and June suggest that urea may be important for Alexandrium nutrition as inorganic nitrogen concentrations in surface water decline.Harmful algal blooms cause serious public health and economic impacts on a global scale (Hallegraeff 1993;Anderson et al. 2000). For example, species within the marine dinoflagellate genus Alexandrium are responsible for paralytic shellfish poisoning (PSP) along the coastlines of the United States, Canada, and many other countries (Hallegraeff 1993;Anderson 1997). PSP can result in serious illness or death if humans ingest sufficient shellfish contaminated with the dinoflagellate toxins (Van Dolah 2000). Observations of Alexandrium fundyense and PSP outbreaks in the northeastern United States indicate that populations accumulate in a variety of oceanographic habitats (Anderson 1997). There is considerable interest in the environmental factors that affect the growth of this genus in field populations. For example, A. fundyense populations in the western Gulf of Maine are often found in surface waters where inorganic nitrogen concentrations are low (Ͻ2 mol L Ϫ1 ) to undetectable, particularly in the late spring (Martorano 1997;Poulton 2001). In this system it is unclear whether A. fun-1 Corresponding author (sdyhrman@whoi.edu). AcknowledgmentsWe thank Dave Kulis, Jody Donahue, Mike Lomas, Bruce Keafer, Liz Jablonski, and Dave Townsend for technical assistance and sample processing. Special thanks also go t...

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Dissolved Organic Nitrogen Hydrolysis Rates in Axenic Cultures of Aureococcus anophagefferens (Pelagophyceae): Comparison with Heterotrophic Bacteria

Cited by 84 publications

References 29 publications

The role of the picoeukaryote Aureococcus anophagefferens in cycling of marine high—molecular weight dissolved organic nitrogen

The role of the picoeukaryote Aureococcus anophagefferens in cycling of marine high—molecular weight dissolved organic nitrogen

Ecology and Diversity of Picoeukaryotes

Urease activity in cultures and field populations of the toxic dinoflagellate Alexandrium

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