Abstract
The effect of preconditioning nitrogen source and growth rate on the interaction between nitrate and ammonium uptake was determined inThalassiosira pseudonana (Clone 3H). A new method, using cells on a filter (Parslow et al. 1985), allowed continuous measurement of uptake from 0.5 to 9 min after the addition of nitrate, ammonium, or both, with no variation in concentration during the course of the experiment. For each preconditioning N source and growth rate, a series of uptake experiments was conducted, including controls with only nitrate or only ammonium, and others with different combinations of concentrations of nitrate and ammonium. For the first time, preference for ammonium was separated from inhibition of nitrate uptake by ammonium. Ammonium was the preferred N source, i.e. if nitrate and ammonium were presented separately, ammonium uptake rates exceeded nitrate uptake rates. Preference for ammonium varied with both preconditioning N source and growth rate. Inhibition of nitrate uptake by ammonium, determined by comparing nitrate uptake in the presence and absence of ammonium, was observed at ammonium concentrations > 1µM, but was rarely complete. Inhibition of nitrate uptake by ammonium was less in the ammonium-limited culture than in the cultures growing on nitrate, but invariant with growth rate in the nitrate-grown cultures. Below 1µM ammonium, nitrate uptake was often stimulated and rates exceeded those in the controls without ammonium. Ammonium uptake was not inhibited by the presence of nitrate.T. pseudonana fits the classical view of the interaction between nitrate and ammonium uptake in some respects, such as preference for ammonium, and inhibition of nitrate uptake by ammonium concentrations > 1µM. However, at ammonium concentrations typical of most marine environments, nitrate uptake occurs at rapid rates. In other respects, N uptake inT. pseudonana deviates from the classical view in the following ways: (1) stimulation of nitrate uptake by low concentrations of ammonium; (2) lack of inhibition of nitrate uptake by ammonium at low nitrate concentrations; and (3) variation in preference and inhibition with preconditioning, which is markedly different for other species. Because of the apparent enormous species variation in the interaction between nitrate and ammonium uptake and the lack of detailed information for a variety of species, it is difficult to generalize about the effect of ammonium on nitrate uptake, especially in the field, where prior N availability and species composition are not usually addressed.
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Balch, W. M. (1987). Studies of nitrate transport by marine phytoplankton using36C-ClO3 − as a transport analogue. I. Physiological findings. J. Phycol. 23: 107–118
Bienfang, P. K. (1975). Steady-state analysis of nitrate-ammonium assimilation by phytoplankton. Limnol. Oceanogr. 20: 402–411
Blasco, D., Conway, H. L. (1982). Effect of ammonium on the regulation of nitrate assimilation in natural phytoplankton populations. J. exp. mar. Biol. Ecol. 61: 157–168
Butz, R. G., Jackson, W. A. (1977). A mechanism for nitrate transport and reduction. Phytochemistry 16: 409–417
Caperon, J., Meyer, J. (1972). Nitrogen-limited growth of phytoplankton. II. Uptake kinetics and their role in nutrient limited growth of phytoplankton. Deep-Sea Res. 19: 619–632
Caperon, J., Ziemann, D. A. (1976). Synergistic effects of nitrate and ammonium ion on the growth and uptake kinetics ofMonochrysis lutheri in continuous culture. Mar. Biol. 36: 73–84
Collos, Y. (1982). Transient situations in nitrate assimilation by marine diatoms. 3. Short-term uncoupling of nitrate uptake and reduction. J. exp. mar. Biol. Ecol. 62: 285–295
Collos, Y. (1989). A linear model of external interactions during uptake of different forms of inorganic nitrogen by microalgae. J. Plankton Res. 11: 521–533
Collos, Y., Slawyk, G. (1976). Significance of cellular nitrate content in natural populations of marine phytoplankton growing in shipboard cultures. Mar. Biol. 34: 27–32
Conover, S. A. M. (1975). Nitrogen utilization during spring blooms of marine phytoplankton in Bedford Basin, Nova Scotia, Canada. Mar. Biol. 32: 247–261
Conway, H. L. (1977). Interactions of inorganic nitrogen in the uptake and assimilation by marine phytoplankton. Mar. Biol. 39: 221–232
Cresswell, R. C., Syrett, P. J. (1979). Ammonium inhibition of nitrate uptake by the diatom,Phaeodactylum tricornutum. Pl. Sci. Lett. 14: 321–325
Cresswell, R. C., Syrett, P. J. (1981). Uptake of nitrate by the diatom,Phaeodactylum tricornutum. J. exp. Bot. 32: 19–26
DeManche, J. M., Curl, H. C., Jr., Lundy, D. W., Donaghay, P. L. (1979). The rapid response of the marine diatomSkeletonema costatum to changes in external and internal nutrient concentration. Mar. Biol. 53: 323–333
Dortch, Q. (1982). Effect of growth conditions on accumulation of internal nitrate, ammonium, amino acids, and protein in three marine diatoms. J. exp. mar. Biol. Ecol. 61: 243–264
Dortch, Q. (1990). The interaction between ammonium and nitrate uptake in phytoplankton. Mar. Ecol. Prog. Ser. 61: 183–201
Dortch, Q., Ahmed, S. I., Packard, T. T. (1979). Nitrate reductase and glutamate dehydrogenase activities inSkeletonema costatum as measures of nitrogen assimilation rates. J. Plankton Res. 1: 169–186
Dortch, Q., Clayton, J. R., Jr., Thoresen, S. S., Ahmed, S. I. (1984). Species differences in accumulation of nitrogen pools in phytoplankton. Mar. Biol. 81: 237–250
Dortch, Q., Clayton, J. R., Jr., Thoresen, S. S., Bressler, S. L., Ahmed, S. I. (1982). Response of marine phytoplankton to nitrogen deficiency: decreased nitrate uptake vs enhanced ammonium uptake. Mar. Biol. 70: 13–19
Dortch, Q., Conway, H. L. (1984). Interactions between nitrate and ammonium uptake: variation with growth rate, nitrogen source and species. Mar. Biol. 79: 151–164
Dortch, Q., Thompson, P. A., Harrison, P. J. (1991). Variability in nitrate uptake kinetics inThalassiosira pseudonana (Bacillariophyceae) J. Phycol. 27: 35–39
Eppley, R. W., Coatsworth, J. L. (1968). Uptake of nitrate and nitrite byDitylum brightwellii — kinetics and mechanisms. J. Phycol. 4: 151–156
Eppley, R. W., Renger, E. H. (1974). N assimilation of an oceanic diatom in N limited continuous culture. J. Phycol. 10: 15–23
Falkowski, P. G. (1975). Nitrate uptake in marine phytoplankton: (NO -3 , Cl−)-activated ATPase forSkeletonema costatum (Bacillariophyceae). J. Phycol. 11: 323–326
Friederich, G. E., Whitledge, T. E. (1972). AutoAnalyzer procedures for nutrients. In: Pavlov, S. P. (ed.) Phytoplankton growth dynamics. Technical Series 1. Chemostat methodology and chemical analyses. Spec. Rep. Dep. Oceanogr. Univ. Wash. 52: 38–55
Glibert, P. M., Biggs, D. C., McCarthy, J. J. (1982). Utilization of ammonium and nitrate during austral summer in the Scotia Sea. Deep-Sea Res. 29: 837–850
Harrison, P. J., Conway, H. L., Dugdale, R. C. (1976). Marine diatoms grown in chemostats under silicate or ammonium limitation. I. Cellular chemical composition and steady-state growth kinetics ofSkeletonema costatum. Mar. Biol. 35: 177–186
Harrison, P. J., Waters, R. E., Taylor, F. J. R. (1980). A broad spectrum artificial seawater medium for coastal and open ocean phytoplankton. J. Phycol. 16: 28–35
Jones, G. J., Morel, F. M. M. (1988). Plasmalemma redox activity in the diatomThalassiosira. Pl. Physiol. 87: 143–147
Kuenzler, E. J., Stanley, D. W., Koenings, J. P. (1979). Nutrient kinetics of phytoplankton in the Pamlico River, North Carolina. Water Resources Research Institute of the University of North Carolina, Chapel Hill (Project No. B-0920-NC)
Lund, B. A. (1987). Mutual interference of ammonium, nitrate, and urea on uptake of15N sources by the marine diatomSkeletonema costatum (Grev.) Cleve. J. exp. mar. Biol. Ecol. 113: 167–180
Ohmori, M., Ohmori, K., Strotmann, H. (1977). Inhibition of nitrate uptake by ammonia in a blue-green alga,Anabaena cylindria. Archs. Microbiol. 114: 225–229
Parslow, J. S., Harrison, P. J., Thompson, P. A. (1984a). Development of rapid ammonium uptake during starvation of batch and chemostat cultures of the marine diatomThalassiosira pseudonana. Mar. Biol. 83: 43–50
Parslow, J. S., Harrison, P. J., Thompson, P. A. (1984b). Saturated uptake kinetics: transient response of the marine diatomThalassiosira pseudonana to ammonium, nitrate, silicate or phosphate starvation. Mar. Biol. 83: 51–59
Parslow, J. S., Harrison, P. J., Thompson, P. A. (1985). Ammonium uptake by phytoplankton cells on a filter: a new high-resolution technique. Mar. Ecol. Prog. Ser. 25: 121–129
Parsons, T. R., Maita, Y., Lalli, C. M. (1984). A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford
Serra, J. L., Llama, M. J., Cadenas, E. (1978). Nitrate utilization by the diatomSkeletonema costatum. I. Kinetics of nitrate uptake. Pl. Physiol. 62: 987–990
Syrett, P. J., Flynn, K. J., Molloy, C. J., Dixon, G. K., Peplinska, A. M., Cresswell, R. C. (1986). Effects of nitrogen deprivation on rates of uptake of nitrogenous compounds by the diatomPhaeodactylum tricornutum Bohlin. New Phytol. 102: 39–44
Terry, K. L. (1982). Nitrate uptake and assimilation inThalassiosira weissflogii andPhaeodactylum tricornutum: interactions with photosynthesis and with the uptake of other ions. Mar. Biol. 69: 21–30
Thompson, P. A., Levasseur, M. A., Harrison, P. J. (1989). Lightlimited growth on ammonium vs. nitrate: what is the advantage for marine phytoplankton? Limnol. Oceanogr. 34: 1014–1024
Tischner, R. (1981). The regulation of the nitrate metabolism inChlorella sorokiniana. Ber. dt. bot. Ges. 94S: 635–645
Yin, K. (1988). The interaction between nitrate and ammonium uptake for a marine diatom grown under different degrees of light limitation. M. Sc. thesis. University of British Columbia, Vancouver
Zevenboom, W., Mur, L. R. (1981). Simultaneous short-term uptake of nitrate and ammonium byOscillatoria agardhii grown in nitrate- or light-limited continuous culture. J. gen. Microbiol. 126: 355–363
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Communicated by J.M. Lawrence, Tampa
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Dortch, Q., Thompson, P.A. & Harrison, P.J. Short-term interaction between nitrate and ammonium uptake inThalassiosira pseudonana: Effect of preconditioning nitrogen source and growth rate. Mar. Biol. 110, 183–193 (1991). https://doi.org/10.1007/BF01313703
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DOI: https://doi.org/10.1007/BF01313703