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

Abstract

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.

Tracing inputs of terrestrial high molecular weight dissolved organic matter within the Baltic Sea ecosystem

“…Studies have shown that, especially during summer when nutrients are depleted, DOM can be an important nutrient fuelling primary production (Berg et al, 2003;Korth et al, 2011;Stepanauskas et al, 1999), and especially for sensible ecosystems like the Baltic Sea terrestrial DOM inputs are assumed to strongly influence the biogeochemistry.…”

DON as a source of bioavailable nitrogen for phytoplankton

“…It is likely that these enzymes are capable of cleaving the N from a wide range of additional DON compounds allowing phytoplankton to, in effect, "farm" N from these compounds while leaving the remainder of the compound external to the cell (Mulholland et al, 1998;Berg et al, 2003b;Stoecker and Gustafson, 2003).…”

Speciation and concentrations of dissolved nitrogen as determinants of brown tide Aureococcus anophagefferens bloom initiation

“…Unlike many co-occurring microalgal species, Aureococcus anophagefferens has qualities consistent with phytoplankton adapted to a more oligotrophic, deep-water environment, such as relatively sensitive functional responses to reduced nitrogenous nutrients (NH 4 + , glutamate, and urea) and relatively low light requirements (Dzurica et al 1989, Yentsch et al 1989, Lomas et al 1996, Milligan & Cosper 1997. While photoautotrophic and capable of growing solely on inorganic nutrients, A. anophagefferens also appears adept at utilizing a variety of dissolved organic nutrients, including proteins, which qualifies it as a mixotroph (Dzurica et al 1989, Lomas et al 1996, Berg et al 1997, 2003b, Mulholland et al 2002. Despite A. anophagefferens' rather modest growth potentials (μ max ≤ 0.80 d -1 ), its unique combination of attributes may provide competitive advantages over other species and permit the occupation of a turbid niche dominated by reduced nitrogen species.…”

“…All results reported above are consistent with the hypothesis that moderate effluxes of reduced N from sediments favor BT proliferation in Long Island estuaries over blooms of competing phytoplankters (LaRoche et al 1997, Gobler & Sañudo-Wilhelmy 2001a). In addition to reduced nitrogen, A. anophagefferens growth may also be stimulated by organic carbon enrichments provided by porewater amendments (Burdige & Homstead 1994, Lomas et al 1996, Berg et al 1997, 2003b.…”