Äîêóìåíò âçÿò èç êýøà ïîèñêîâîé ìàøèíû. Àäðåñ îðèãèíàëüíîãî äîêóìåíòà : http://library.biophys.msu.ru/matorin/3398.pdf Äàòà èçìåíåíèÿ: Mon Jun 15 17:40:36 2009 Äàòà èíäåêñèðîâàíèÿ: Mon Oct 1 19:54:59 2012 Êîäèðîâêà: Ïîèñêîâûå ñëîâà: dark energy

ISSN 0096-3925, Moscow University Biological Sciences Bulletin, 2007, Vol. 62, No. 3, pp. 111­116. © Allerton Press, Inc., 2007. Original Russian Text © L.V. Ilyash, T.A. Belevich, A.Yu. Ulanova, D.N. Matorin, 2007, published in Vestnik Moskovskogo Universiteta. Biologiya, 2007, No. 3, pp. 17­22.

Fluorescence Parameters of Marine Plankton Algae at the Assimilation of Organic Nitrogen
L. V. Ilyash, T. A. Belevich, A. Yu. Ulanova, and D. N. Matorin
Department of Hydrobiology and Department of Biophysics, Moscow State University, Vorob'evy Gory, Moscow, 119899 Russia; e-mail: matorin@biophys.bio.msu.su Abstract--fluorescence parameters of marine plankton algae Pseudo-nitzschis delicatissima, Thalassiosira weissflogii, and Tetraselmis viridis were estimated after the addition of organic (urea and glycine) and inorganic (nitrate and ammonia) nitrogen to nitrogen-limited cultures acclimated to limited and saturated irradiance. The photochemical efficiency of photosystem 2, the maximum relative electron transport, and the light saturation index increased in the algae assimilating organic nitrogen. The dynamics of parameters depended species specifically on the nitrogen source and irradiance. The ecological role of organic nitrogen in the seasonal dynamics and vertical distribution of phytoplankton is discussed. DOI: 10.3103/S0096392507030054

The primary production in most regions of the World Ocean is controlled by shortage of nitrogen (Glibert, 1988). Nitrogen deficiency leads to the decrease in the efficiency of light reactions of photosynthesis, in the rate of photosynthetic fixation of carbon, and of populational growth of algae (Flakowski and Raven, 1997). Under conditions of the shortage of mineral nitrogen, the significance of consumption of dissolved organic nitrogen (Norg) by planktonic algae increases. There is vast information on the capacity of various algae to assimilate organic substrata containing organic nitrogen (see, e.g., Antia et al., 1991) but no data on the dynamics of photosynthetic activity, in particular on light reactions of photosynthesis, at consumption of Norg. A widely used approach for determination of the efficiency of light reactions of photosynthesis is the estimation of fluorescent parameters of photoautotophs. In particular, the relative output of alternating fluorescence reflects the efficiency of photochemical transformation of energy in reaction centers of photosystem 2 (Falkowski and Raven, 1997). This parameter is used as a characteristic of the physiological state of phytoplankton and of its photosynthetic activity (Matorin and Venediktov, 1990; Falkowski and Raven, 1997). In natural ecosystems the concentration of Norg is significantly changing both in time and in space. A significant part in Norg consists of substances which can be assimilated by planktonic algae. For example, in the summer the part of nitrogen of urea in the total content of Norg may attain 48% and the part of nitrogen of free amino acids--over 25% (Flynn and Butler, 1986). Phytoplankton in natural ecosystems in the surficial layer experiences photoinhibition stress. At the intermediate depths of the photic zone, the illumination is close to

the saturation level for photosynthesis. At the lower boundary of the photic zone, the illumination limits photosynthesis. Different light energy resources of phytoplankton and the dependence of the rate of consumption of urea and amino acids by algae on illumination (Bonin et al., 1982; Wallen and Allan, 1987) indicate the investigation of the dynamics of photosynthetic activity in algae assimilating Norg at various illumination levels as an urgent problem. This approach acquires special urgency in the aspect of annual increase of organic nitrogen discharged to aquatic ecosystem from anthropogenic sources (Seitzinger and Sanders, 1999). The present study is aimed at elucidation of special traits of the dynamics of fluorescence parameters of marine planktonic algae Tetraselmis viridis, Thalassiosira weissflogii, and Pseudo-nitzschia delicatissima at assimilation of urea and glycine under conditions of illumination limiting and saturating photosynthesis. MATERIAL AND METHODS The material for the study was algological pure cultures of marine planktonic algae Pseudo-nitzschia delicatissima (Cleve) Heiden (Bacillariiphyta), Thalassisira weissflogii (Grunow) Freyxell et Hasle (Bacillariophyta), and Tetraselmis viridis (Rouch.) Morris (Prasinophyta). Experimental scheme. The algae were cultivated at illumination 115 (I1) and 38 (I2) µE/(m2s), duration of the light period was 14 h a day, and the temperature was 20 ± 1°C in media prepared with artificial sea water (Shubravyi, 1983) diluted to salinity 17. In the experiments the nitrogen-limited cultures of algae were used, acclimated to I1 or to I2. Such cultures were obtained by exposition of algae at a certain illumination during 2­ 3 weeks in the "nitrogen-free" medium. For prepara-

111


112

ILYASH et al.

tion of the latter, all ingredients were introduced to water except for nitrogen according to the recipe of medium f/2 (Guilliard and Ryther, 1962). In the nitrogen-limited algae acclimated to a certain level of illumination, the response to the addition of organic (urea and glycine) and mineral (nitrate and ammonia) nitrogen was estimated by fluorescent parameters. The additives were introduced at the concentration 0.18 or 0.89 mmol of nitrogen which corresponds to the content of this element in media f/10 and f/2. The cultures without additives were used as a control. The additives were introduced in the beginning of the light period. In a separate series of experiments, the additives were introduced in the beginning of the dark period to solve the question of if the algae are able to assimilate urea and glycine in darkness. Estimation of fluorescent parameters. The intensity of fluorescence at the level F0 (permanent fluorescence) was measured by means of a one-ray fluorometer (Matorin et al., 1992). The intensity of fluorescence at closed reaction centers of photosystem 2 (Fm, maximum fluorescence) was measured similarly in presence of 10­5 mol of diuron. The relative output of variable fluorescence Fv/Fm = (Fm ­ F0)/Fm is a measure of quantum efficiency of the work of reaction centers of photosystem 2 (RC PS 2) and characterizes the photosynthetic activity of algae (Matorin and Venediktov, 1990; Falkowski and Raven, 1997). Estimation of parameters describing dependence of photosynthetic activity on illumination (P/E curves). For the nitrogen-limited cultures of T. viridis and T. weissflogii grown at illuminations I1 and I2 and for the cultures of these algae in a day after the introduction of additives of urea, glycine, and nitrate at the concentration 0.18 mmol of nitrogen, the dependence of the photosynthetic activity on illumination was estimated (P/E curves). P/E curves were obtained on the basis of values of relative rate of electrons by the electron transport chain according to methods described by Lippemeier et al. (1999) with some modifications. Up to 10 ml of each variant of cultures were exposed for 30 minutes in test tubes at illuminations 43, 82, 122, 151, and 197 µE/(m2s). Within 30 minutes in each variant of cultures, the quantum efficiency of the work of RC PS 2 was measured directly at exposition illumination ( Pi ) using a fluorometer RAM-2000 (Walz, Germany). For each variant of cultures, Pi was measured in three replications. The relative rate of electron transport was calculated by the following equation (Lippemeier et al., 1999): Ji = Pi · Ei. According to recommendations (Van Liere and Walsby, 1982), Ei was calculated by the following equation: E1 = (E0 ­ Ez)/(lnE0 ­ lnEz), µE/(m2S), where E0 is illumination in front of the test tube with culture and Ez is illumination behind the test tube. With consideration of the obtained P/E curves, the coefficient of maximum utilization of light energy

(the angle of the slope of the P/E curve, ), the maximum rate or electrons by the electron transport chain (Jmax), and saturating light intensity (Es) were calculated. was calculated as the coefficient of linear regression plotted by points on the light-limited stretch of the P/E curve, Jmax--as an average by the values of Ji situated on the light saturating stretch (Jassby and Platt, 1976). Es was calculated by the equation (Platt et al., 1977) Es = Jmax/. In the nitrogen-limited cultures acclimated to illumination I2, the satiating light intensity was for T. viridis 105 µE/(m2s); for T. weissflogii it was 90 µE/(m2s). Consequently, I2 is the illumination limiting photosynthesis. In the nitrogen-limited cultures acclimated to illumination I1, Es was for T. viridis 97 µE/(m2s), and for T. weissflogii it was 95 µE/(m2s). At the illumination 122 µE/(m2s), there was a decrease in Jmax. Accordingly, I1 is the illumination exceeding Es and may partially inhibit the rate of electronic transport. The values of Es in pennate diatoms provided with components of mineral nutrition are within 42­150 µE/(m2s) (Geider et al., 1985; WillemoÊs and Monas, 1991). With consideration of published data and of the fact that in the nitrogen-limited algae Es are lower than those in the algae provided with biogenous elements (Kolber et al., 1988), it may be assumed that, for the diatom P. delicatissima, I2 is the illumination limiting photosynthesis and I1 exceeds Es and may partly inhibit the rate of electronic transport. RESULTS AND DISCUSSION Dynamics of the relative output of alternating fluorescence in the algae assimilating organic and mineral nitrogen. In the nitrogen-limited algae, the values Fv/Fm were 0.2 and less. Low values of Fv/Fm correspond to the general pattern of disturbance of action of the photosynthetic apparatus (PA) at limitation of nitrogen revealed earlier both in marine and freshwater algae of various taxonomic positions (Chemeris et al., 1989; Kolber et al., 1988; Geider et al., 1993; Falkowski and Raven, 1997; etc). After addition of both urea and glycine in all three algae, Fv/Fm increased. This indicates that the assimilated Norg was used for restoration of PA. Duration of the period before the increase of Fv/Fm (Tinc) at assimilation of Norg in most cases does not differ significantly from Tinc at assimilation of mineral nitrogen (Nmin) (Table 1). The exceptions are higher values of Tinc at growth with additions of urea and glycine than at growth with additions of nitrate in the alga P. delicatissima at I2 and lesser values of Tinc at assimilation of urea and glycine than at assimilation of nitrate in T. weissflogii at I1. For the increase of Fv/Fm in all three algae when the substrata are used with the same level of reduction of nitrogen (urea, glycine, and ammonium), approximately identical time is required. In a similar way, the values Tinc in the case of assimilation of reduced organic nitrogen did not differ significantly from those in the case of assimilation of
Vol. 62 No. 3 2007

MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN


FLUORESCENCE PARAMETERS OF MARINE PLANKTON ALGAE

113

Table 1. Duration of the period from the moment of introduction of additives of urea, glycine, nitrate, and ammonium at the concentration 0.89 mmol of nitrogen to the beginning of the increase of the quantum efficiency of photosystem 2 (Tinc) and the highest values attained by the quantum efficiency of photosystem 2 (Fv /Fm)max in the algae Tetraselmis viridis (Tv), Thalassiosira weissflogii (Tw), and Pseudo-nitzschia delicatissima (Pd) at the growth under conditions of illumination 115 (I1) and 38 (I2) µE/(m2 s) Algae Tv Nitrogen source Tinc, h Urea Glycine Nitrate Ammonium Tw Urea Glycine Nitrate Ammonium Pd Urea Glycine Nitrate Ammonium 3.7 (2.1) 4.2 (2.5) 1.8 (0.9) 3.0 (2.7) 4.5 (2.6) 4.0 (2.3) >11.5 5.5 (4.8) >10 >10 8.0 (2.0) >10 I1 (Fv /Fm)max 0.42 (0.08) 0.39 (0.04) 0.44 (0.10) 0.48 (0.06) 0.38 (0.07) 0.51 (0.06) 0.41 (0.02) 0.40 (0.05) 0.25 (0.05) 0.32 (0.04) 0.39 (0.08) 0.30 (0.04) Tinc, h 1.8 (1.5) 2.6 (2.0) 1.0 (0.8) 4.0 (0.7) 3.5 (2.8) 2.5 (1.9) 3.0 (2.4) 4.0 (0.6) >12 3.5 (2.0) 1.5 (0.8) >12 I2 (Fv /Fm)max 0.52 (0.09) 0.48 (0.01) 0.46 (0.03) 0.49 (0.01) 0.52 (0.09) 0.48 (0.01) 0.54 (0.03) 0.54 (0.01) 0.43 (0.07) 0.56 (0.01) 0.60 (0.03) 0.63 (0.01)

Note: In parentheses the value of standard deviation is indicated.

oxidized nitrate nitrogen, but only in algae at limiting illumination. The only exception was P. delicatissima in which restoration of Fv/Fm in the case of assimilation of urea required more time than in the case of assimilation of nitrate. At I1 the species specificity of algae manifests itself in the response to additives of Norg and nitrate. Thus, in T. viridis, Tinc does not differ significantly at assimilation of Norg and nitrate. In T. weissflogii the value Fv/Fm began to increase the earliest at growth with assimilation of urea, and in P. delicatissima--with assimilation of nitrate. The species specificity of algae also manifests itself in the highest value of the relative output of alternating fluorescence (Fv/Fm)max attained in the first three days of growth on various forms of nitrogen. The ratio of values (Fv/Fm)max at assimilation of Norg and Nmnr depends on illumination (Table 1). Thus, in T. viridis and T. weissflogii, the values (Fv/Fm)max at assimilation of urea and Nmnr did not differ significantly from each other at two levels of illumination. In P. delicatissima the values of (Fv/Fm)max at assimilation of urea were lower than those at assimilation of Nmnr. At assimilation of glycine, the highest values of Fv/Fm did not differ significantly from those at assimilation of Nmnr in T. viridis and P. delicatissima at both illuminations. The highest values of Fv/Fm in the cultures of T. weissflogii assimilating glycine at I1 were higher than (Fv/Fm)max at the assimilation of Nmnr. In addition, in P. delicatissima at both illuminations and in T. weissflogii at I1, the values (Fv/Fm)max at assimilation of glycine were higher

than at the assimilation of urea. The latter might depend on direct incorporation of glycine in protein without previous transformation in P. delicatissima and T. weissflogii, as this occurs, e.g., in the dinoflagellate Gymnodinium breve (Baden and Mende, 1979) and in the green alga Chlamydomonas reinhardtii (Kirk and Kirk, 1978). The increase in Fv/Fm started during the light period; in the first hours of it, the additives were introduced (except T. weissflogii assimilating nitrate at I1). If the additives of nitrogen were introduced in the dark period, then, in the beginning of the next light period, the higher values of Fv/Fm were noted in algae exposed with additives in comparison with the control cultures (Table 2). This points to assimilation by the algae T. viridis, T. weissflogii, and P. delicatissima of additives in the dark as the exposition of the algae at light before measurements did not exceed the values Tinc recorded at the introduction of additives in the beginning of the light period. The ability of Nmnr to assimilate in the dark increases with the increase of the nitrogen deficiency in the cells (Clark and Flynn, 2002). The dark assimilation occurs at the expense of energy and of the reducer formed in the mitochondrial electron transport chain (Van Lerberghe et al., 1992). As a substrata of the tricarbonic acid cycle in the dark, the products of glycolytic decomposition of reserve carbohydrates are used (Granum and Myklestad, 2001). If the reserve carbohydrates are the energy source at assimilation of mineral nitrogen in the dark, it may be assumed that the mitoVol. 62 No. 3 2007

MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN


114

ILYASH et al.

Table 2. The relative (in relation to the control) values of the quantum efficieny of photosystem 2 in the algae Tetraselmis viridis (Tv), Thalassiosira weissflogii (Tw), and Pseudonitzschia delicatissima (Pd) acclimated to illumination 115 (I1) and 38 (I2) µE/(m2 s) at the introduction of additives of urea, glycine, nitrate, and ammonium at the concentration 0.89 mmol of nitrogen in the beginning of the dark period Nitrogen source Urea Glycine Nitrate Ammonium Tv I1 1.52 1.45 1.13 1.52 I2 2.32 1.90 1.47 1.84 I1 1.36 1.91 1.55 1.59 Tw I2 1.67 1.83 1.88 1.79 I1 1.11 1.21 1.68 1.00 Pd I2 1.28 1.45 1.45 1.27

Note: Duration of the period from introduction of the additives was 10­11 hour, of which, in the latter 2­3 h, the algae were exposed to light.

Table 3. Parameters describing the dependence of the photosynthetic activity on illumination in the algae Tetraselmis viridis and Thalassiosira weissflogii acclimated to illumination 38 (I2) and 115 (I1) µE/(m2 s) in the 24 h after introduction of additives of urea, glycine, and nitrate at the concentration 0.18 mmol to the nitrogen-limited cultures (control) Additives , rel. units Jmax, rel. units Es, µE/(m2 s)

Tetraselmis viridis I2 Control Urea Glycine Nitrate I1 Control Urea Glycine Nitrate I2 Control Urea Glycine Nitrate I1 Control Urea Glycine Nitrate 0.17 (0.03) 0.26 (0.03) 0.32 (0.03) 0.38 (0.04) 0.17 (0.02) 0.19 (0.03) 0.23 (0.06) 0.22 (0.08) 0.30 (0.14) 0.34 (0.10) 0.36 (0.09) 0.56 (0.10) 0.20 (0.07) 0.33 (0.06) 0.35 (0.07) 0.34 (0.06) 18 (2.7) 37 (5.6) 43 (5.6) 44 (6.1) 16 (1.5) 37 (3.5) 35 (3.5) 39 (4.1) 27 (9.3) 57 (5.1) 62 (7.0) 88 (15.0) 19 (1.4) 40 (8.0) 42 (4.0) 43 (10.1) 105 (12) 142 (33) 134 (42) 116 (49) 97 (4) 195 (44) 152 (58) 177 (98) 90 (13) 168 (23) 172 (22) 157 (39) 95 (14) 114 (33) 120 (26) 126 (43)

chondrial NADP · H and ATP are used for assimilation in the dark of urea and glycine too. Parameters describing the dependence of the photosynthetic activity on illumination (P/E curves) in the algae T. viridis and T. weissflogii assimilating organic and mineral nitrogen. In the day after the introduction of both additives, Norg and Nmnr parameters describing P/E curves differed from those in the nitrogen-limited cultures (Table 3). This points to the change at assimilation of Norg of the intensity and direction of biophysical, biochemical, and metabolic processes regulating photosynthesis. In both algae growing with assimilation of Norg at illumination I1 and in T. viridis at I2, the increase in and Jmax, in comparison with the values of these parameters in the nitrogen-limited cultures, corresponded to the level of the increase at Nmnr assimilation. At illumination I2 in T. weissflogii, the greatest increase of and Jmax occurred in the cultures which grew with the assimilation of nitrate. The algae manifested a speciesspecific response of the parameter to additives of Norg depending on illumination. Thus, in T. weissflogii the values of increased more at I1, while in T. viridis--at I2. On the contrary, Jmax increased approximately equally at two illuminations both in T. viridis and in T. weissflogii. In the alga T. weissflogii assimilating Norg during 24 h, the values and Jmax corresponded to the values of parameters in the cultures of this alga provided with components of mineral nutrition and growing at 600 µE/(m2s) (Lippemeier et al., 1999). In both species of algae in the 24 h after the introduction of additives, the satiating light intensity increased too (Table 3). Inhibition of the relative rate of electron transport at illumination up to 150 µE/(m2s) was not observed. The values Es in T. viridis increased more at I1, and in T. weissflogii it increased at I2. CONCLUSIONS The marine planktonic algae Pseudo-nitzschia delicatissima, Thalassisira weissflogii, and Tetraselmis viridis are able to grow using urea and glycine as a sole source of nitrogen. These algae assimilate urea and glycine in the dark too. In this case the energy and substrate expenditures for consumption and intracellular transformation of the substrata are covered, obviously, by the oxidation of reserve polysaccharides as is the case at the dark assimilation of mineral nitrogen. In all three species of algae at a high level of cellular nitrogen deficiency, the assimilation of urea and glycine contributes to the increase of the relative output of alternating fluorescence, maximum relative rate of electrons via the electron transport chain, and the value of satiating light intensity. This indicated the use of the assimilating Norg for restoration of the normal action of the photosynthetic apparatus. The algae are characterized by the species-specific dependence of the dynamics of Fv/Fm on illumination. They are also characterVol. 62 No. 3 2007

Thalassiosira weissflogii

Note: is the cioefficient of maximum utilization of light energy, Jmax is the maximum relative rate of electrons via the electron transport chain, and Es is the satiating light intensity. In parentheses the value of standard deviation is indicated.

MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN


FLUORESCENCE PARAMETERS OF MARINE PLANKTON ALGAE

115

ized by the species-specificity in the ratio Fv/Fm at Norg and Nmnr. In many cases the dynamics of Fv/Fm at assimilation of urea and glycine did not differ from that at the assimilation of Nmnr. In natural ecosystems the mineral and organic resources of phytoplankton and the source of light energy vary in time and space. For example, in the seas with the expressed seasonal dynamics of abiotic factors, the development of phytoplankton in spring lead to a complete depletion of mineral nitrogen in the photic layer. The relative part of Nmnr in the total content of dissolved nitrogen decreases and the part of Norg increases (Mantoura et al., 1988). In the summer, the part of urea­nitrogen may attain 48% in the total content of dissolved nitrogen and the part of nitrogen of free amino acids may attain over 25% (Flynn and Butler, 1986). Under such conditions, in some cases, phytoplankton develops intensively. It is represented, as was shown, e.g., for the White Sea (Ilyash et al., 2003), principally by mixotrophic diatoms and flagellates. We revealed for the algal cultures the efficient restoration of the photosynthetic apparatus at the expense of assimilation of urea and glycine. It pointed to formation of the summer "bloom" of diatoms, and the mass development of flagellates may depend on their capacity for the assimilation of nitrogen-containing organic substrata and for support from resources of Norg of normal functioning of the photosynthetic apparatus and populational growth. The quantity of Norg of anthropogenous origin released to aquatic ecosystems increases every year (Seitzinger and Sanders, 1999). The increase in the abundance of organic resources available to algae may change the productivity of ecosystems. For example, during the recent decade, the biomass of the diatom Skeletonema costatum increased by more than an order of magnitude in the coastal waters of the White Sea. It may be attributed to greater discharge to the sea of organic nitrogen predominantly of anthropogenous origin (Ilyash et al., 2003). ACKNOWLEDGMENTS The study is supported by the Russian Foundation for Basic Research (grant no. 04-04-48565). REFERENCES
1. Antia, N.J., Harrison, J.P., and Oliveira, L., The Role of Dissolved Organic Nitrogen in Phytoplankton Nutrition, Phycologia, 1991, vol. 30, pp. 1­89. 2. Baden, D.G. and Mende, T.J., Amino Acid Utilization by Gymnodinium breve, Phytochemistry, 1979, vol. 18, pp. 247­251. 3. Bonin, D.J, Antia, N.J., and Pelaez-Hudlet, J., Influence of Temperature and Light Intensity on the Utilization of Glycine as Nitrogen Source for Photrophic Growth of Marine Unicellular Cyanophyte (Cyanobacterium), Bot. Mar., 1982, vol. 25, pp. 493­499.

4. Chemeris, Yu.K., Popova, A.V., Arytyunyan, A.A., and Venediktov, P.S., Influence of Deficiency of Mineral Nutrition on the Photosynthetic Apparatus of Chlorella, Fiziol. Rastenii, 1989, vol. 36, no. 1, pp. 57­66. 5. Clark, D.R. and Flynn, K.L., N­Assimilation in the Noxious Flagellate Heterosigma carterae (Raphidophyceae): Dependence on Light, N-Source, and Physiological State, J. Phycol., 2002, vol. 38, pp. 503­512. 6. Falkowski, P.G. and Raven, J.A., Aquatic Photosynthesis, Malden, Blackwell Science, 1997. 7. Flynn, K.J. and Butler, I., Nitrogen Sources for the Growth of Marine Microalgae: Role of Dissolved Free Amino Acids, Mar. Ecol. Progr. Ser., 1986, vol. 34, pp. 281­304. 8. Geider, R.J., Osborn, B.A., and Raven, J.A., Light Dependence of Growth and Photosynthesis in Phaeodactylum tricornutum (Bacillariophyceae), J. Phycol., 1985, vol. 21, pp. 600­619. 9. Geider, R.J., Roche, J., Greene, R., and Olaizola, M., Response of the Photosynthetic Apparatus of Phaeodactylum tricornutum to Nitrate, Phosphate, or Iron Starvation, J. Phycol., 1993, vol. 29, pp. 753­766. 10. Gilbert, P.M., Primary Productivity and Pelagic Nitrogen Cycling, Eds. Blackburn, T.H. and Sorensen, J., Nitrogen Cycling in Coastal Marine Environments, New York, 1988, pp. 3­31. 11. Granum, E. and Myklestad, S.M., Mobilization of -1,3Glucan and Biosynthesis of Amino Acids Induced by NH 4 Addition to N-Limited Cells of Marine Diatom Skeletonema costaum (Bacillariophyceae), J. Phycol., 2001, vol. 37, pp. 772­782. Guilliard, R.R.L. and Ryther, J.H., Studies on Marine Diatons. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran., Can. J. Microbiol., 1962, vol. 8, pp. 229­239. Ilyash, L.V., Zhitina, L.S., and Fedorova, V.D., Fitoplankton Belogo morya (Phytoplankton of the White Sea), Moscow, 2003 [in Russian]. Jassby, A.D. and Platt, T., Mathematical Formulation of the Repationship between Photosynthesis and Light for Phytoplabkton, Limnol Oceanogr., 1976, vol. 21, pp. 540­ 547. Kirk, D.L. and Kirk M.M., Carrier-Mediated Uptake of Arginin and Urea by Chlamydomonas reihardtii, Plant Physiol., 1978, vol. 61, pp. 556­560. Kolber, Z., Zehr, J., and Falkowski, P.G., Effects of growth Irradiance and Nitrogen Limitation on Photosynthetic Energy Conversion on Photosystem II, Plant Physiol., 1988, vol. 88, pp. 923­929. Lippemeier, S., Harting, P., and Colijn, F., Direct Impact of Silicate on the Photosynthetic Performance of the Diatom Thalassiosira weissflogii Assessed by On- and Off-Line PAM Fluorescence Measurements, J. Plankton Res., 1999, vol. 21, pp. 269­283. Mantoura, R.F.C., Owens, N.J.P., and Burkill, P.H., Nitrogen Biochemistry and Modelling of Carmarthen Bay, Eds. Blackburn, T.H. and Sorensen, J. Nitrogen Cycling in Coastal Marine Environments, New York, 1988, pp. 415­441. Matorin, D.N., Vasil'ev, I.R., and Vedernikov, V.I., Investigation of Photoinhibition of Primary Reactions of PhoVol. 62 No. 3 2007
+

12.

13. 14.

15. 16.

17.

18.

19.

MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN


116

ILYASH et al. tosynthesis in Natural Populations of Phytoplankton of the Black Sea, Fiziol. Rastenii, 1992, vol. 39, no. 3, pp. 455­463. Celled Organism Trichoplax and of Other Small Invertebrates, Zool. Zh., 1983, vol. 12, no. 4, pp. 618­621. Van Lerberghe, G.C., Huppe, H.C., Vlossak, K.D., and Turpin, D.H., Activation of Respiration to Support Dark ­ + NO 3 and NH 4 Assimilation in the Green Alga Selenastrum minutum, Plant physiol., 1992, vol. 99, pp. 495­ 500. Van Liere, L. and Walsby, A.E., Interactions of Cyanobacteria with Light, Eds. Carr, N.G. and Whitton, B.H., The Biology of Cyanobacteria, Oxford, 1982, pp. 9­45. Wallen, D.G. and Allan, R., Utilization of Amino Acids by Blue-Green Alga Synechococcus AN (Anacystis nidulans), Can. J. Bot., 1987, vol. 65, pp. 1133­1136. WillemoÊs, M. and Monas, E., Relationship between Growth Irradiance and the Xanthophyll Cycle in the Diatom Nitzschia palea, Physiol. Plant., 1991, vol. 83, pp. 433­456.

24.

20. Matorin, D.N. and Venediktov, P.S., Luminiscence of Chlorophyll in Cultures of Microalgae and in Natural Populations of Phytoplankton, Itogi Nauki Tekhn., Ser. Biophysics, VINITI, 1990, vol. 40, pp. 49­100. 21. Platt, T., Denman, K.L., and Jassby, A.D., Modelling the Productivity of Phytoplankton, Ed. Golberg, E.D., The Sea, New York, 1977, pp. 807­856. 22. Seitzinger, S.P. and Sanders, R.W., Atmospheric Input of Dissolved Organic Nitrogen Stimulates Estuarine Bacteria and Phytoplankton, Limnol. Oceanogr., 1999, vol. 44, pp. 721­736. 23. Shubravyi, O.I., The Aquarium with Artificial Sea Water for Keeping and Propagation of the Primitive Many25. 26. 27.

MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN

Vol. 62

No. 3

2007