DON as a source of bioavailable nitrogen for phytoplankton
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Abstract. Relative to inorganic nitrogen, concentrations of dissolved organic nitrogen (DON) are often high, even in regions believed to be nitrogen-limited. The persistence of these high concentrations led to the view that the DON pool was largely refractory and therefore unimportant to plankton nutrition. Any DON that was utilized was believed to fuel bacterial production. More recent work, however, indicates that fluxes into and out of the DON pool can be large, and that the constancy in concentration is a function of tightly coupled production and consumption processes. Evidence is also accumulating which indicates that phytoplankton, including a number of harmful species, may obtain a substantial part of their nitrogen nutrition from organic compounds. Ongoing research includes ways to discriminate between autotrophic and heterotrophic utilization, as well as a number of mechanisms, such as cell surface enzymes and photochemical decomposition, that could facilitate phytoplankton use of DON components.
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Ahlgren, N. A., Rocap, G., and Chisholm, S. W.: Measurement of \\textitProchlorococcus ecotypes using real-time polymerase chain reaction reveals different abundances of genotypes with similar light physiologies, Environ. Microbiol., 8, 441–454, 2005.
Aiken, G. R.: A critical evaluation of the use of macroporous resins for the isolation of aquatic humic substances, John Wiley and Sons, New York, 1988.
Alberts, J. J. and Takács, M.: Importance of humic substances for carbon and nitrogen transport into southeastern United States estuaries, Organ. Geochem., 30, 385–395, 1999.
Algeus, S.: The deamination of glycocoll by green algae, Physiologia Plantarum, 1, 343–409, 1948.
Allen, A. E., Booth, M. G., Frischer, M. E., Verity, P. G., Zeh,r J. P., and Zani, S.: Diversity and detection of nitrate assimilation genes in marine bacteria, Appl. Environ. Microbiol., 67, 5343–5348, 2001.
Allen, A. E., Howard-Jones, M. H., Booth, M. G., Frischer, M. E., Verity, P. G., Bronk, D. A., and Sanderson M. P.: Importance of heterotrophic bacterial assimilation of ammonium and nitrate in the Barents Sea during summer, J. Mar. Syst., 38, 93–108, 2002.
Aluwihare, L., Repeta, D., and Chen, R.: A major biopolymeric component to dissolved organic carbon in surface seawater, Nature, 387, 166–169, 1997.
Aluwihare, L. I., Repeta, D. J., Pantoja, S., and Johnson, C. G.: Two chemically distinct pools of organic nitrogen accumulate in the ocean, Science, 308(5724), 1007–1010, 2005.
Amador, J. A., Alexander, M., and Zika, R. G.: Sequential photochemical and microbial degradation of organic molecules bound to humic acid, Appl. Environ. Microbiol., 55, 2843–2849, 1989.
Antia, N. J., Harrison, P. J., and Oliveira, L.: Phycological Reviews 2: The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology, Phycologia, 30, 1–89, 1991.
Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martinez, D., Putnam, N. H., Zhou, S., Allen, A. E., Apt, K. E., Bechner, M., Brzezinski, M., Chaal, B. K., Chiovitti, A., Davis, A. K., Demarest, M. S., Detter, J. C., Glavina ,A. K., Goodstein, D., Had, M. Z., et al.: The genome of the diatom \\textitThalassiosira pseudonana: Ecology, evolution, and metabolism, Science, 306, 79–86, 2004.
Beck, G. M., Reuter, J. H., and Perdue, E. M.: Organic and inorganic geochemistry of some coastal plain rivers of the southeastern United States, Geochim. Cosmochim. Acta, 38, 341–364, 1974.
Benner, R.: Chemical composition and reactivity, in: Biogeochemistry of Marine Dissolved Organic Matter, edited by: Hansell, D. A. and Carlson, C. A., Academic Press, San Diego, pp 59–90, 2002.
Benner, R., Pakulski, J. D., McCarthy, M., Hedges, J. I., and Hatcher, P. G.: Bulk chemical characteristics of dissolved organic matter in the ocean, Science, 255, 1561–1564, 1992.
Berg, G. M., Glibert, P. M., Lomas, M. W., and Burford, M. A.: Organic nitrogen uptake and growth by the chrysophyte \\textitAureococcus anophagefferens during a brown tide event, Mar. Biol., 129, 377–387, 1997.
Berg, G. M., Glibert, P. M., Jørgensen, N. O. G., Balode, M., and Purina, I.: Variability in inorganic and organic nitrogen uptake associated with riverine nutrient input in the Gulf of Riga, Baltic Sea, Estuaries, 24, 204–214, 2001.
Berg, G. M., Balode, M., Purina, I., Bekere, S., Béchemin, C., and Maestrini, S. Y.: Plankton community composition in relation to availability and uptake of oxidized and reduced nitrogen, Aquat. Microb. Ecol., 30, 263–274, 2003a.
Berg, G. M., Repeta, D. J., and La Roche, J.: The role of the picoeukaryote \\textitAureococcus anophagefferens in cycling of marine high-molecular weight dissolved organic nitrogen, Limnol. Oceanog., 48, 1825–1830, 2003b.
Berges, J. and Mulholland, M.: Enzymes and cellular N cycling, in: Nitrogen in the Marine Environment, edited by: Capone, D. G., Bronk, D. A., Mulholland, M., and Carpenter, E. J., Elsevier, San Diego, in press, 2008.
Berman, T. and Chava, S.: Algal growth on organic compounds as nitrogen sources, J. Plankton Res., 21, 1423–1437, 1999.
Berman, T. and Bronk, D. A.: Dissolved organic nitrogen: A dynamic participant in aquatic ecosystems, Aquat. Microb. Ecol., 31, 279–305, 2003.
Bronk D. A.: Dynamics of DON, in: Biogeochemistry of Marine Dissolved Organic Matter, edited by: Hansell, D. A. and Carlson, C. A., Academic Press, San Diego, pp 153–249, 2002.
Bronk, D. and Glibert, P.: Application of a 15N tracer method to the study of dissolved organic nitrogen uptake during spring and summer in Chesapeake Bay, Mar. Biol., 115, 501–508, 1993.
Bronk, D. A. and Ward, B. B.: Inorganic and organic nitrogen cycling in the Southern California Bight, Deep Sea Res. I., 52, 2285–2300, 2005.
Bronk, D. A., Glibert, P. M., Malone, T. C., Banahan, S., and Sahlsten, E.: Inorganic and organic nitrogen cycling in Chesapeake Bay: autotrophic versus heterotrophic processes and relationships to carbon flux, Aquat. Microb. Ecol., 15, 177–189, 1998.
Bronk, D. A., Sanderson, M. P., Mulholland, M. R., Heil, C. A., and O'Neil, J. M.: Organic and inorganic nitrogen uptake kinetics in field populations dominated by \\textitKarenia brevis, in: Harmful Algae 2002, edited by: Steidinger, K., Vargo, G. A., and Heil, C. A., Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, St Petersburg, FL, pp 80–82, 2004.
Bushaw-Newton, K. L. and Moran, M. A.: Photochemical formation of biologically available nitrogen from dissolved humic substances in coastal marine systems, Aquat. Microb. Ecol., 18, 285–292, 1999.
Bushaw, K. L., Zepp, R. G., Tarr, M. A., Schulz-Jander, D., Bourbonniere, R. A., Hodson, R., Miller, W. L., Bronk, D. A., and Moran, M. A.: Photochemical release of biologically labile nitrogen from dissolved organic matter, Nature, 381, 404–407, 1996.
Campbell, L.: Flow cytometric analysis of autotrophic picoplankton, in: Marine Microbiology, edited by: Paul, J. H., Academic Press, San Diego, pp 317–343, 2001.
Carlson, C. A. and Ducklow, H. W.: Dissolved organic carbon in the upper ocean of the central equatorial Pacific Ocean, 1992: Daily and fine scale vertical variations, Deep-Sea Res. II, 42, 639–656, 1995.
Carlsson, P. and Granéli, E.: Availability of humic bound nitrogen for coastal phytoplankton, Est. Coast. Shelf Sci., 36, 433–447, 1993.
Carlsson, P., Granéli, E., Tester, P., and Boni, L.: Influences of riverine humic substances on bacteria, protozoa, phytoplankton, and copepods in a coastal plankton community, Mar. Ecol. Prog. Ser., 127, 213–221, 1995.
Carlsson, P., Edling, H., and Bechemin, C.: Interactions between a marine dinoflagellate (\\textitAlexandrium catenella) and a bacterial community utilizing riverine humic substances, Aquat. Microb. Ecol., 16, 65–80, 1998.
Carlsson, P., Granéli, E., and Segatto, A. Z.: Cycling of biologically available nitrogen in riverine humic substances between marine bacteria, a heterotrophic nanoflagellate and a photosynthetic dinoflagellate, Aquat. Microb. Ecol., 18, 23–36, 1999.
Casey, J., Lomas, M. W., Mandecki, J., and Walker, D.: \\textitProchlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum, Geophys. Res. Lett., in press, 2007.
Chisholm, S. W., Olson, R. J., Zettler, E. R., Goerick, R., Waterbury, J. B., and Welschmeyer, N. A.: A novel free-living prochlorophyte abundant in the oceanic euphotic zone, Nature, 334, 340–343, 1988.
Cho, B., Park, M., Shim, J., and Azam, F.: Significance of bacteria in urea dynamics in coastal surface waters, Mar. Ecol. Prog. Ser., 142, 19–26, 1996.
Chróst, R. J.: Environmental control of the synthesis and activity of aquatic microbial ectoenzymes, in: Microbial Enzymes in Aquatic Environments edited by: Chróst, R. J., Springer, New York, pp 25–59, 1991.
Church, M. J., Ducklow, H. W.. and Karl, D. M.: Multiyear increases in dissolved organic matter inventories at Station ALOHA in the North Pacific Subtropical Gyre, Limnol. Oceanogr., 47(1), 1–10, 2002.
Collier, J. L.: Flow cytometry and the single compound in plankton ecology, J. Phycol., 40, 805–807, 2004.
Collier, J. L., Brahamsha, B., and Palenik, B.: The marine cyanobacterium \\textitSynechococcus sp. WH7805 requires urease (urea amidohydrolase, EC 3.5.1.5) to utilize urea as a nitrogen source: molecular-genetic and biochemical analysis of the enzyme, Microbiol.-Sgm., 145, 447–459, 1999.
Cottrell, M. and Kirchman, D. L.: Natural assemblages of marine proteobacteria and members of the \\textitCytophaga-Flavobacter cluster consuming low-and high-molecular-weight dissolved organic matter, Appl. Environ. Microb., 66(4), 1692–1697, 2000.
Doblin, M., Legrand, C., Carlsson, P., Hummert, C., Granéli, E., and Hallegraeff, G.: Uptake Of Humic Substances By the Toxic Dinoflagellate \\textitAlexandrium cantenella, in: Harmful Algal Blooms, edited by: Hallegraeff, G., Blackburn, S. I., Bolch, C. J., and Lewis, R. J., Intergovernmental Oceanographic Commission of Unesco, Paris, pp 336–339, 2000.
Dubelaar, G. B. J. and Jonker, R. R.: Flow cytometry as a tool for the study of phytoplankton, Scientia Marina, 64, 135–156, 2000.
Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I. M., Galperin, M. Y., Koonin, E. V., Le Gall, F., Makarova, K. S., Ostrowski, M., Robert, C., Rogozin, I. B., Scanlan, D. J., Tandeau de Marsac, N., Weissenbach, J., Wincker, P., Wolf, Y. I., and Hess, W. R.: Genome sequencing of the cyanobacterium \\textitProchlorococcus marinus SS120, a nearly minimal oxyphototrophic genome, Proc. Nat. Acad. Sci., 100, 10 020–10 025, 2003.
Dugdale, R. C. and Goering, J. J.: Uptake of new and regenerated forms of nitrogen in primary productivity, Limnol. Oceanog., 12, 196–206, 1967.
Dyhrman, S. T. and Anderson, D. M.: Urease activity in cultures and field populations of the toxic dinoflagellate, \\textitAlexandrium, Limnol. Oceanogr., 48, 647–655, 2003.
Eppley, R. W., Sharp, J. H., Renger, E. H., Perry, M. J., and Harrison, W. G.: Nitrogen assimilation by phytoplankton and other microorganisms in the surface waters of the central north Pacific Ocean, Mar. Biol., 39, 111–120, 1977.
Eppley, R. W. and Peterson, B. J.: Particulate organic matter flux and planktonic new production in the deep ocean, Nature, 282, 677–680, 1979.
Fan, C., Glibert, P., and Burkholder, J.: Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for \\textitProrocentrum minimum in natural blooms and laboratory cultures, Harmful Algae, 2, 283–299, 2003a.
Fan, C., Glibert, P. M., Alexander, J., and Lomas, M. W.: Characterization of urease activity in three marine phytoplankton species, \\textitAureococcus anophagefferens, \\textitProrocentrum minimum, and \\textitThalassiosira weissflogii, Mar. Biol., 142, 949–958, 2003b.
Fuhrman, J.: Close coupling between release and uptake of dissolved free amino acids in seawater studied by an isotope dilution approach, Mar. Ecol. Prog. Ser., 37, 45–52, 1987.
Gagnon, R., Levasseur, M., Weise, A. M., and Fauchot, J.: Growth stimulation of \\textitAlexandrium tamarense (Dinophyceae) by humic substances from the Manicouagan River (eastern Canada), J. Phycol., 41, 489–497, 2005.
Gallagher, E., McGuinness, L., Phelps, C., Young, L. Y., and Kerkhof, L. J.: $^13$C-Carrier DNA shortens the incubation time needed to detect benzoate-utilizing denitrifying bacteria by stable-isotope probing, Appl. Environ. Microb., 71(9), 5192–5196, 2005.
Gao, H. and Zepp, R. G.: Factors influencing photoreactions of dissolved organic matter in a coastal river of the Southeastern United States, Environ. Sci. Technol., 32, 2940-2946, 1998.
Gardner, W. S., Seitzinger, S. P., and Malczyk, J. M.: The effects of sea salts on the forms of nitrogen released from estuarine and freshwater sediments: Does ion pairing affect ammonium flux?, Estuaries, 14, 157–166, 1991.
Gardner, W. S., Cavaletto, J. F., Bootsma, H. A., Lavrentyev, P. J., and Tanvone, F.: Nitrogen cycling rates and light effects in tropical Lake Maracaibo, Venezuela, Limnol. Oceanogr., 43, 1814–1825, 1998.
Gasol, J. M. and Morán, X. A. G.: Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry, Aquat. Microb. Ecol., 16, 251–264, 1999.
Glibert, P. M. and Terlizzi, D. E.: Cooccurrence of elevated urea levels and dinoflagellate blooms in temperate estuarine aquaculture ponds, Appl. Environ. Microbiol., 65(12), 5594–5596. 1999.
Glibert, P. M., Garside, C., Fuhrman, J. A., and Roman, M. R.: Time-dependent coupling of inorganic and organic nitrogen uptake and regeneration in the plume of the Chesapeake Bay estuary and its regulation by large heterotrophs, Limnol. Oceanogr., 36, 895–909, 1991.
Glibert, P. M., Heil, C. A., Hollander, D., Revilla, M., Hoare, A., Alexander, J., and Morasko, S.: Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay, Mar. Ecol. Prog. Ser., 280, 73–83, 2004.
Gobler, C. J. and Sañudo-Wilhelmy, S. A.: Effects of organic carbon, organic nitrogen, inorganic nutrients, and iron additions on the growth of phytoplankton and bacteria during a brown tide bloom, Mar. Ecol. Prog. Ser, 209, 19–34, 2001.
Gobler, C. J., Renaghan, M. J., and Buck, N. J.: Impacts of nutrients and grazing mortality on the abundance of \\textitAureococcus anophagefferens during a New York brown tide bloom, Limnol. Oceanogr., 47, 129–141, 2002.
Goldman, J. C.: Potential role of large oceanic diatoms in new primary production, Deep-Sea Res. I, 40, 159–168, 1993.
Hansell, D. A., Williams, P. M., and Ward, B. B.: Measurements of DOC and DON in the Southern California Bight using oxidation by high temperature combustion, Deep-Sea Res., 40(2), 219–234, 1993.
Harrison, W. G., Head, E. J. H., Conover, R. J., Longhurst, A. R., and Sameoto, D. D.: The distribution and metabolism of urea in the eastern Canadian Arctic, Deep-Sea Res. I, 32, 23–42, 1985.
Harrison, W. G., Platt, T., and Lewis, M. R.: f-Ratio and its relationship to ambient nitrate concentration in coastal waters, J. Plankton Res., 9, 235–248, 1987.
Hattori, A.: Studies on the metabolism of urea and other nitrogenous compounds in \\textitChlorella ellipsoidea. I. Assimilation of urea and other nitrogenous compounds by nitrogen-starved cells, J. Biochem. (Tokyo), 44, 253–273, 1957.
Hedges, J. I. and Hare, P. E.: Amino acid adsorption by clay minerals in distilled water, Geochim. Cosmochim. Acta., 51, 255–259, 1987.
Herndon, J. and Cochlan, W. P.: Nitrogen utilization by the raphidophyte \\textitHeterosigma akashiwo: Growth and uptake kinetics in laboratory cultures, Harmful Algae, 6, 260–270, 2007.
Hildebrand, M. and Dahlin, K.: Nitrate transporter genes from the diatom \\textitCylindrotheca fusiformis (Bacillariophyceae): mRNA levels controlled by nitrogen source and by the cell cycle, J. Phycol., 36, 702–713, 2000.
Hildebrand, M.: Cloning and functional characterization of ammonium transporters from the marine diatom \\textitCylindrotheca fusiformis (Bacillariophyceae), J. Phycol., 41, 105–115, 2005.
Hoch, M. P. and Kirchman, D. L.: Ammonium uptake by heterotrophic bacteria in the Delaware Estuary and adjacent coastal waters, Limnol. Oceanogr., 40, 886–897, 1995.
Howard, M. D. A., Cochlan, W. P., Ladizinsky, N., and Kudela, R. M.: Nitrogenous preference of toxigenic \\textitPseudo-nitzschia australis (Bacillariophyceae) from field and laboratory experiments, Harmful Algae, 6, 206–217, 2007.
Jacobsen, T. and Rai, H.: Aminopeptidase activity in lakes of differing eutrophication, in: Microbial Enzymes in Aquatic Environments, edited by: Chróst, R., Springer-Verlag, New York, pp 155–164, 1991.
Jeong, H. J., Yoo, Y. D., Park, J. Y., Song, J. Y., Kim, S. T., Lee, S. H., Kim, K. Y., and Yih, W. H.: Feeding by phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic, Aquat. Micro. Ecol., 40, 133–150, 2005a.
Jeong, H. J., Park, J. Y., Nho, J. H., Park, M. O., Ha, J. H., Seong, K. A., Jeng, C., Seong, C. N., Lee, K. Y., and Yih, W. H.: Feeding by red-tide dinoflagellates on the cyanobacterium \\textitSynechococcus, Aquat. Microb. Ecol., 41, 131–143, 2005b.
Joint, I., Henriksen, P., Fonnes, G. A., Bourne, D., Thingstad, T. F., and Riemann, B.: Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms, Aquat. Microb. Ecol., 29, 145–159, 2002.
Jørgensen, N. O. G.: Uptake of urea by estuarine bacteria, Aquat. Microb. Ecol., 42, 227–242, 2006.
Jørgensen, N. O. G., Kroer, N., Coffin, R. B., Yang, X.-H., and Lee, C.: Dissolved free amino acids, combined amino acids, and DNA as sources of carbon and nitrogen to marine bacteria, Mar. Ecol. Prog. Ser., 98, 135–148, 1993.
Jørgensen, N. O. G., Tranvik, L., Edling, H., Granéli, E., and Lindell, M.: Effects of sunlight on occurrence and bacterial turnover of specific carbon and nitrogen compounds in lake waters, FEMS Microbiol. Ecol., 25, 217–227, 1998.
Jørgensen, N. O. G., Kroer, N., Coffin, R. B., and Hoch, M. P.: Relations between bacterial nitrogen metabolism and growth efficiency in an estuarine and an open-water ecosystem, Aquat. Microb. Ecol., 18, 247–261, 1999.
Keil, R. G. and Kirchman, D. L.: Contribution of dissolved free amino acids and ammonium to the nitrogen requirements of heterotrophic bacterioplankton, Mar. Ecol. Prog. Ser., 73, 1–10, 1991.
Kieber, D. J.: Photochemical production of biological substrates, in: The effects of UV radiation in the marine environment, edited by: de Mora, S., Demers S., and Vernet, M., Cambridge University Press, Cambridge, pp 131–148, 2000.
Kirchman, D. L., Keil, R. G., and Wheeler, P. A.: The effect of amino acids on ammonium utilization and regeneration by heterotrophic bacteria in the subarctic Pacific, Deep-Sea Res., 36, 1763–1776, 1989.
Kirchman, D. L., Suzuki, Y., Garside, C., and Ducklow, H. W.: High turnover rates of dissolved organic carbon during a spring phytoplankton bloom, Nature, 352, 612–614, 1991.
Kirchman, D. L., Moss, J., and Keil, R. G.: Nitrate uptake by heterotrophic bacteria: Does it change the f-ratio?, Arch. Hydrobiol., 37, 129–138, 1992.
Kirchman, D. L. and Wheeler, P. A.: Uptake of ammonium and nitrate by heterotrophic bacteria and phytoplankton in the sub-Arctic Pacific, Deep-Sea Res. I, 45, 347–365, 1998.
Kirchman, D. L.: Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria, in: Microbial Ecology of the Oceans, edited by: Kirchman, D. L., Wiley-Liss, Inc., New York, pp 261–288, 2000.
Kivic, P. A. and Vesk, M. J.: Pinocytotic uptake of protein from the reservoir in \\textitEuglena, Arch. Microbiol., 96, 155–159, 1974.
Klut, M., Bisalputra, T., and Anita, N. J.: Some observations on the structure and function of the dinoflagellate pusule, Can. J. Botany, 65, 736–744, 1987.
Koopmans, D. J. and Bronk, D. A.: Photochemical production of inorganic nitrogen from dissolved organic nitrogen in waters of two estuaries and adjacent surficial groundwaters, Aqua. Micro. Eco., 26, 295–304, 2002.
Kristiansen, S.: Urea as a nitrogen source for the phytoplankton in the Oslofjord, Mar. Biol., 74(1), 17–24, 1983.
Kroer, N., Jørgensen, N. O. G., and Coffin, R. B.: Utilization of dissolved nitrogen by heterotrophic bacterioplankton: A comparison of three ecosystems, Appl. Env. Microbiol., 60, 4116–4123, 1994.
Kudela, R. W. and Cochlan, W. P.: Nitrogen and carbon uptake kinetics and the influence of irradiance for a red tide bloom off southern California, Aquat. Microb. Ecol., 21, 31–47, 2000.
Langheinrich, U.: Plasma membrane-associated aminopeptidase activities of \\textitChlamydomonas reinhardtii and their biochemical characterization, Biochim. Biophysica Acta, 1249(1), 45–57, 1995.
Lee, C., Hedges, J. I., Wakeham, S. G., and Zhu, N.: Effectiveness of various treatments in retarding microbial activity in sediment trap material and their effects on the collection of swimmers, Limnol. Oceanogr., 37, 117–130, 1992.
Lee, S. and Fuhrman, J. A.: Relationship between biovolume and biomass of naturally derived bacterioplankton, Appl. Env. Microbiol., 53, 1298–1303, 1987.
Lee, S., Kang, Y.-C., and Fuhrman, J. A.: Imperfect retention of natural bacterioplankton cells by glass fiber filters, Mar. Ecol. Prog. Ser., 119, 285–290, 1995.
Legrand, C. and Carlsson, P.: Uptake of high molecular weight dextran by the dinoflagellate \\textitAlexandrium catenella, Aquat. Microb. Ecol, 16, 81–86, 1998.
Legrand, C., Granéli, E., and Carlsson, P.: Induced phagotrophy in the photosynthetic dinoflagellate \\textitHeterocapsa triquetra, Aquat. Microb. Ecol., 15, 65–75, 1998.
Lewitus, A. J.: Osmotrophy in marine microalgae, in: Algal cultures analogues and blooms, edited by: Subba Rao, D. V., Science Publishers, Inc., Enfield, New Hampshire, 2005.
Li, A., Stoecker, D. K., and Coats, D. W.: Spatial and temporal aspects of \\textitGyrodinium galatheanum in Chesapeake Bay: distribution and mixotrophy, J. Plankton Res., 22, 2105–2124, 2000a.
Li, A., Stoecker, D., and Coats, D.: Mixotrophy in \\textitGyrodinium galatheanum (Dinophyceae); responses to light intensity and inorganic nutrients, J. Phycol., 36, 33–45, 2000b.
Li, W. K. W.: Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting, Limnol. Oceanogr., 39, 169–175, 1994.
Libby, P. and Wheeler, P.: Particulate and dissolved organic nitrogen in the central and eastern equatorial Pacific, Deep-Sea Res., 44(2), 345–361, 1997.
Lipschultz, F.: Nitrogen-specific uptake rates of marine phytoplankton isolated from natural populations of particles by flow cytometry, Mar. Ecol. Prog. Ser., 123, 245–258, 1995.
Lomas, M. W.: Nitrate reductase and urease enzyme activity in the marine diatom \\textitThalassiosira weissflogii (Bacillariophyceae): interactions among nitrogen substrates, Mar. Biol., 144, 37–44, 2004.
Lomas, M. W., Glibert, P. M., Berg, G. M., and Burford, M.: Characterization of nitrogen uptake by natural populations of \\textitAureococcus anophagefferens (Chrysophyceae) as a function of incubation duration, substrate concentration, light, and temperature, J. Phycol., 32, 907–916, 1996.
Lomas, M. and Glibert, P.: Temperature regulation of nitrate uptake: A novel hypothesis about nitrate uptake and reduction in cool-water diatoms, Limnol. Oceanogr., 44, 556–572, 1999a.
Lomas, M. W. and Glibert, P. M.: Interactions between NH$_4^+$ and NO$_3^-$ uptake and assimilation: Comparison of diatoms and dinoflagellates at several growth temperatures, Mar. Biol., 133, 541–551, 1999b.
Lomas, M. W., Trice, T. M., Glibert, P. M., Bronk, D. A., and McCarthy, J. J.: Temporal and spatial dynamics of urea uptake and regeneration rates and concentrations in Chesapeake Bay, Estuaries, 25, 469–482, 2002.
Lopez-Lozano, A., Diez, J., El Alaoui, S., Moreno-Vivian, C., and Garcia-Fernandez, J. M.: Nitrate is reduced by heterotrophic bacteria but not transferred to \\textitProchlorococcus in non-axenic cultures, FEMS Microbiol. Ecol., 41, 151–160, 2002.
Marie, D., Brussaard, C. P. D., Thyrhaug, R., Bratbak, G., and Vaulow, D.: Enumeration of marine viruses in culture and natural samples by flow cytometry, Appl. Env. Microbiol., 65(1), 45–52, 1999.
McCarthy, J. J.: Uptake of urea by natural populations of marine phytoplankton, Limnol. Oceanog., 17, 738–748, 1972a.
McCarthy, M., Hedges, J., and Benner, R.: Major biochemical composition of dissolved high molecular weight organic matter in seawater, Mar. Chem., 55, 281–297, 1996.
Middelburg, J. J. and Nieuwenhuize, J.: Uptake of dissolved inorganic nitrogen in turbid, tidal estuaries, Mar. Ecol. Prog. Ser., 192, 79–88, 2000a.
Middelburg, J. J. and Nieuwenhuize, J.: Nitrogen uptake by heterotrophic bacteria and phytoplankton in the nitrate-rich Thames estuary, Mar. Ecol. Prog. Ser., 203, 13–21, 2000b.
Monger, B. C. and Landry, M. R.: Flow cytometric analysis of marine bacteria with Hoechst 33342, Appl. Environ. Microbiol., 59, 905–911, 1993.
Moore, L. R., Post, A. F., Rocap, G., and Chisholm, S. W.: Utilization of different nitrogen sources by the marine cyanobacteria \\textitProchlorococcus and \\textitSynechococcus, Limnol. Oceanogr., 47, 989–996, 2002.
Mulholland, M. and Lomas, M.: Nitrogen uptake and assimilation, in: Nitrogen in the Marine Environment, edited by: Capone, D. G., Bronk, D. A., Mulholland, M., and Carpenter, E. J., Elsevier, San Diego, in press, 2008.
Mulholland, M. R., Glibert, P. M., Berg, G. M., Van Heukelem, L., Pantoja, S., and Lee, C.: Extracellular amino acid oxidation by microplankton: a cross-system comparison, Aquat. Microb. Ecol., 15, 141–152, 1998.
Mulholland, M. R., Gobler, C. J., and Lee, C.: Peptide hydrolysis, amino acid oxidation, and nitrogen uptake in communities seasonally dominated by \\textitAureococcus anophagefferens, Limnol. Oceanogr., 47, 1094–1108, 2002.
Mulholland, M. R., Lee, C., and Glibert, P. M.: Extracellular enzyme activity and uptake of carbon and nitrogen along as estuarine salinity and nutrient gradient, Mar. Ecol. Prog. Ser., 258, 3–17, 2003.
Olson, R. J., Frankel, S. L., and Chisholm, S. W.: An inexpensive flow cytometer for the analysis of fluorescence signals in phytoplankton: Chlorophyll and DNA distributions, J. Exp. Mar. Biol. Ecol., 68, 129–144, 1983.
Olson, R. J., Vaulot, D., and Chisholm, S. W.: Marine phytoplankton distributions measured using shipboard flow cytometry, Deep-Sea Res., 32, 1273–1280, 1985.
Oremland, D. S. and Capone, D.: Use of specific inhibitors in biogeochemistry and microbial ecology, Adv. Microb. Ecol., 10, 285–383, 1988.
Paerl, H. W.: Ecophysiological and trophic implications of light-stimulated amino acid utilization in marine picoplankton, Appl. Environ. Microbiol., 57, 473–479, 1991.
Paerl, H. W.: Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as "new" nitrogen and other nutrient sources, Limnol. Oceanogr., 42, 1154–1165, 1997.
Palenik, B. and Morel, F. M. M.: Comparison of cell-surface L-amino acid oxidases from several marine phytoplankton, Mar. Ecol. Prog. Ser., 59, 195–201, 1990a.
Palenik, B. and Morel, F. M. M.: Amino acid utilization by marine phytoplankton: A novel mechanism, Limnol. Oceanogr., 35, 260–269, 1990b.
Palenik, B. and Morel, F. M. M.: Amine oxidases of marine phytoplankton, Appl. Environ. Microbiol., 57, 2440–2443, 1991.
Palenik, B., Brahamsha, B., Larimer, F. W., Land, M., Hauser, L., Chain, P., Lamerdin, J., Regala, W., Allen, E. E., McCarren, J., Paulsen, I., Dufresne, A., Partensky, F., Webb, E. A., and Waterbury, J.: The genome of a motile marine \\textitSynechococcus, Nature, 424, 1037–1042, 2003.
Pantoja, S. and Lee, C.: Cell-surface oxidation of amino acids in seawater, Limnol. Oceanogr., 39, 1718–1726, 1994.
Pehlivanoglu-Mantas, E. and Sedlak, D. L.: Wastewater-Derived Dissolved Organic Nitrogen: Analytical Methods, Characterization, and Effects: A Review, Crit. Rev. Env. Sci. Technol., 36, 261–285, 2006.
Pel, R., Floris, V., Gons, H. J., and Hoogveld, H. L.: Linking flow cytometric cell sorting and compound-specific $^13$C-analysis to determine population-specific isotopic signatures and growth rates in cyanobacteria-dominated lake plankton, J. Phycol., 40, 857–866, 2004.
Peuravuori, J., Lohtonen, T., and Pihlaja, K.: Sorption of aquatic humic matter by DAX-8 and XAD-8 resins. Comparative study using pyrolysis gas chromatography, Anal. Chim. Acta, 471, 219–226, 2002.
Radajewski, S., Ineson, P., Parekj, N. R., and Murrell, J. C.: Stable-isotope probing as a tool in microbial ecology, Nature, 403, 646–649, 2000.
Rashid, M. A.: Contribution of humic substances to the cation exchange capacity of different marine sediments, Maritime Sediments, 5, 44–50, 1969.
Repeta, D. J., Quan, T. M., Aluwihare, L. I., and Accardi, A. M.: Chemical characterization of high molecular weight dissolved organic matter in fresh and marine waters, Geochim. Cosmochim. Acta, 66(6), 955–962, 2002.
Rivkin, R. B., Phinney, D. A., and Yentsch, C. M.: Effects of flow cytometric analysis and cell sorting on photosynthetic carbon uptake by phytoplankton in cultures and from natural populations, Appl. Environ. Microbiol., 52, 935–938, 1986.
Rocap, G., Larimer, F., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N., Arellano, A., Coleman, M., Hauser, L., Hess, W., Johnson, Z., Land, M., Lindell, D., Post, A., Regala, W., Shah, M., Shaw, S., Steglich, C., Sullivan, M., Ting, C., Tolonen, A., Webb, E., Zinser, E., and Chisholm, S. W.: Genome divergence in two \\textitProchlorococcus ecotypes reflects oceanic niche differentiation, Nature, 424, 1042–1047, 2003.
Rodrigues, R. M. N. V. and Williams, P. J. B.: Inorganic nitrogen assimilation by picoplankton and whole plankton in a coastal ecosystem, Limnol. Oceanogr., 47, 1608–1616, 2002.
Rosenfeld, J. K.: Ammonium adsorption in nearshore anoxic sediments, Limnol. Oceanogr., 24, 356–364, 1979.
Sanders, R. and Porter, K.: Phagotrophic phytoflagellates, Adv. Microb. Ecology, 10, 167–192, 1988.
Schnitzer, M.: Nature of nitrogen in humic substances, in: Humic substances in soil, sediment, and water, edited by: Aiken, G. R., McKnight, D. M., and Wershaw, R. L., John Wiley and Sons, New York, pp 303–328, 1985.
See, J. H.: Availability of humic nitrogen to phytoplankton, Ph.D. Dissertation, Physical Sciences, The College of William and Mary, Williamsburg, pp 164, 2003.
See, J. H. and Bronk, D. A.: Changes in molecular weight distributions, C:N ratios, and chemical structures of estuarine humic substances with respect to season and age, Mar. Chem., 97, 334–346, 2005.
See, J. H., Bronk, D. A., and Lewitus, A. J.: Uptake of \\textitSpartina-derived humic nitrogen by estuarine phytoplankton in axenic and non-axenic culture, Limnol. Oceanogr., 51, 2290–2299, 2006.
Seitzinger, S. and Sanders, R.: Contribution of dissolved organic nitrogen from rivers to estuarine eutrophication, Mar. Ecol. Prog. Ser., 159, 1–12, 1997.
Sinsabaugh, R. L., Findlay, S., Franchini, P., and Fischer, D.: Enzymatic analysis of riverine bacterioplankton production, Limnol. Oceanogr., 42, 29–38, 1997.
Smalley, G., Coats, D., and Adam, E.: A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate \\textitCeratium furca, Aquat. Microb. Ecol., 17, 167–179, 1999.
Smayda, T. J.: Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea, Limnol. Oceanogr., 42, 1137–1153, 1997.
Stepanauskas, R., Laudon, H., and Jørgensen, N. O. G.: High DON bioavailability in boreal streams during a spring flood, Limnol. Oceanogr., 45, 1298–1307, 2000.
Stephens, G. C. and North, B. B.: Extrusion of carbon accompanying uptake of amino acids by marine phytoplankters, Limnol. Oceanogr., 16, 752–757, 1971.
Stoecker, D. K., Li, A., Coats, D. W., Gustafson, D. E., and Nannen, M. K.: Mixotrophy in the dinoflagellate \\textitProrocentrum minimum, Mar. Ecol. Prog. Ser., 152, 1–12, 1997.
Stoecker, D. K. and Gustafson, D. E.: Cell-surface proteolytic activity of photosynthetic dinoflagellates, Aquat. Microb. Ecol., 30, 175–183, 2003.
Syrett, P. J.: Uptake and utilization of nitrogen compounds, in: Biochemistry of the Algae and Cyanobacteria, edited by: Rogers, L. J. and Gallon, J. R., Oxford University Press, New York, pp 23-39, 1988.
Tamminen, T. and Irmisch, A.: Urea uptake kinetics of a midsummer planktonic community on the SW coast of Finland, Mar. Ecol. Prog. Ser., 130, 201–211, 1996.
Thurman, E. M., Wershaw, R. L., Malcolm, R. L., and Pinckney, D. J.: Molecular size aquatic humic substances, Organic Geochem., 4, 27–35, 1982.
Veldhuis, M. J. W. and Kraay, G. W.: Application of flow cytometry in marine phytoplankton research: current applications and future perspectives, Scientia Marina, 64, 121–134, 2000.
Veuger, B., Middelburg, J. J., Boschker, H. T. S., Nieuwenhuize, J., van Rijswijk, P., Rocchelle-Newall, E. J., and Navarro, N.: Microbial uptake of dissolved organic and inorganic nitrogen in Randers Fjord, Est. Coast. Shelf Sci., 61, 507–515, 2004.
Vives-Rego, J., Lebaron, P., and Nebe-von Caron, G.: Current and future applications of flow cytometry in aquatic microbiology, FEMS Microbiol. Rev., 24, 429–448, 2000.
Wallner, G., Fuchs, B., Spring, S., Beisker, W., and Amann, R.: Flow sorting of microorganisms for molecular analysis, Appl. Environ. Microb., 63, 4223–4231, 1997.
Wheeler, P. A. and Kirchman, D. L.: Utilization of inorganic and organic nitrogen by bacteria in marine systems, Limnol. Oceanogr., 31, 998–1009, 1986.
Wheeler, P. A., North, B. B., and Stephens, G. C.: Amino acid uptake by marine phytoplankters, Limnol. Oceanogr., 19, 249–259, 1974.
Wheeler, P. A., North, B., Littler, M., and Stephens, G.: Uptake of glycine by natural phytoplankton communities, Limnol. Oceanogr., 22, 900–910, 1977.
Wiegner, T. N., Seitzinger, S. P., Glibert, P., and Bronk, D. A.: Bioavailability of dissolved organic nitrogen and carbon from nine rivers in the Eastern United States, Aquat. Microb. Ecol., 43, 277–287, 2006.
Yentsch, C. M., Horan, P. K., Muirhead, K., Dortch, Q., Haugen, E., Legendre, L., Murphy, L. S., Perry, M. J., Phinney, D. A., Pomponi, S. A., Spinrad, R. W., Wood, M., Yentsch, C. S., and Zahuranec, B. J.: Flow cytometry and cell sorting: A technique for analysis and sorting of aquatic particles, Limnol. Oceanogr., 28, 1275–1280, 1983.
Zehr, J. P. and Ward, B. B.: Nitrogen cycling in the ocean: new perspectives on processes and paradigms, Appl. Environ. Microb., 68, 1015–1024, 2002.
Zinser, E. R., Coe, A., Johnson, Z. I., Martiny, A. C., Fuller, N. J., Scanlan, D. J., and Chisholm, S. W.: \\textitProchlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improve quantitative PCR method, Appl. Environ. Microb., 72, 723–732, 2006.