Influence of high salinity and nitrogen limitation on package effect and C/N ratio in Dunaliella viridis

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1 Hydrobiologia 492: , Kluwer Academic Publishers. Printed in the Netherlands. 201 Influence of high salinity and nitrogen limitation on package effect and C/N ratio in Dunaliella viridis Carlos Jiménez & F. X. Niell Department of Ecology, Faculty of Sciences, University of Málaga, Málaga, Spain Tel Fax Received 6 June 2001; in revised form 17 December 2002; accepted 8 March 2003 Key words: Dunaliella viridis, salt stress, nitrogen limitation, cell carbon, cell nitrogen, package effect Abstract Variations in salinity and nitrate concentration of the growth medium were responsible for changes in growth rate, cell volume, pigment concentration, light harvesting efficiency and cell carbon and nitrogen content in Dunaliella viridis. Cell volume, Chl a/chl b, Car/Chla and C/N ratios increased in high salt- and low nitrogen-grown cells, while the contrary occurred to growth rate and package effect of pigments. After changing the osmotic pressure or the nitrate concentration, full adaptation of cell C and N content took approximately 24 h. It is concluded that high salinity and nitrogen deficiency induce similar responses in the phytoplankton to high light stress. Introduction Halotolerant algae of the genus Dunaliella are the most ubiquitous eukaryotic micro-organisms in hypersaline environments, and can survive even in saturated salt solutions ( 5.5 M NaCl) (Ben-Amotz & Avron, 1983, 1990). These organisms have to cope with sudden changes in salinity, irradiance and nutrient availability that usually occur in their natural habitat. The lack of a rigid cell wall permits rapid changes in cell shape and volume in response to osmotic shocks. After a change in the external salinity, Dunaliella osmoregulates by varying the intracellular concentration of glycerol (Ben-Amotz & Avron, 1973). Transition to the new osmotic conditions lasts 1 3 h, and during most of this period cell division does not occur (Avron, 1992). Change in pigment content and packing of pigments also proceeds rapidly in response to varying environmental conditions (Berner et al., 1989; Sukenik et al., 1990). In the present work, we studied pigment adaptation of D. viridis to a range of salinity (1 4 M NaCl) and nitrate concentration ( mm NO 3 ), and followed the time-course evolution of cell carbon and nitrogen when salinity or nitrogen availability were changed. Materials and methods Dunaliella viridis Teodoresco was grown axenically in a series of batch cultures. Cells were cultivated with continuous orbital shaking and continuous irradiance (150 µmol m 2 s 1 ), provided by commercial fluorescent lamps. Growth medium was prepared according to Johnson et al. (1968), at four salinities (1, 2, 3, 4 m NaCl) and four nitrate concentrations (0.5, 1.5, 5, 10 mm NO 3 ). Cells were harvested by centrifugation (1000 g, 10 min) every 24 h and resuspended in fresh medium to a cell density of cell ml 1, in order to maintain them in the exponential phase of growth. HPLC analysis of the pigments was performed according to Carnicas et al. (1999); pigments were extracted according to Jiménez & Pick (1993). In vivo absorption of the cultures was measured in cell suspensions with filtered growth medium as reference. Light scattering was reduced by placing an opal-glass transmission filter (Shibata, 1959) in front of the photomultiplier of a Beckman DU-7 spectrophotometer. In vivo optical absorption cross-sections normalized to chlorophyll a were calculated according to Berner et al. (1989). Chl a concentration was calculated using Jeffrey & Humphrey (1975) dichro-

2 202 matic equations after extraction from algal pellets in 80% acetone. Total cell carbon and nitrogen were estimated using a C:H:N Perkin-Elmer 2400 elemental analyzer. Replicate samples of 4 ml from each culture were filtered through Whatman GF/F filters, and dried at 60 C for 6 h before analysis. Results and discussion In a previous work (Jiménez & Niell, 1991), we determined that D. viridis grows optimally at 1 2 M NaCl, 5 mm NO 3 and 30 C, and that a clear limitation of cell growth occurred at 4 M NaCl and at mm NO 3. D. viridis is preferentially found in its natural habitat from late spring to late autumn (García-Jiménez, 1991), when salinity and temperature are high. Chl a and Chl b cell content also changed significantly as a function of salinity, decreasing at high salinity. Change in nitrate availability also determined significant changes in the cell content of photosynthetic pigments in this species, and both Chl a and b increased following an increase in nitrate, reaching maximal values at 5 mm NO 3.Itisworth noting that osmotic stress and N deficiency had similar effects on pigment composition. Cell Chl a and Chl b content decreased under N deficiency and at high salinity, but the loss of Chl b was more pronounced than that of Chl a in both cases. Carotenoids were less sensitive to stress than chlorophylls, so a sequential degradation of pigments in the order Chl b > Chl a > Car could be established in high salinity or nitrogen deficiency. The chromatographic analysis of pigments (Fig. 1) showed a significant increase in the concentration of lutein and zeaxanthin under nitrate limitation (Fig. 1a) and at high salinity (Fig. 1b). In optimal growth conditions (Fig. 1c) no zeaxanthin was detected. Moreover, a significant increase in α-carotene and ß-carotene was produced in nitrogen limitation. It is also interesting to point out that the carotenoid zeaxanthin is involved in the operation of the xanthophyll cycle. It has its origin in the deepoxidation of the violaxanthin, and it has been shown to accumulate in chlorophytes (including Dunaliella) and higher plants both in response to salinity stress (Cowan & Rose, 1991) and high light (Ruban et al., 1994; Gordillo et al., 2001). Thus, higher zeaxanthin concentration may be expected in any stressed cell, as it occurred in this work. Changes in salinity and nitrate concentration induced not only a change in cell pigment but also in Figure 1. Chromatographic analysis of pigments of D. viridis grown under (a) nitrogen limitation (0.5 mm NO 3 ), (b) high salinity (4 M NaCl) and (c) optimal growth conditions (1M NaCl, 5 mm NO 3 ). (1- Lutein; 2- Zeaxanthin; 3- Chl b;4-chla;5-α-carotene; 6- all-trans ß-carotene; 7-9-cis ß-carotene). (n=3).

3 203 Figure 2. In vivo absorption cross-sections normalized to Chl a of D. viridis in function of nitrate availability and salinity. Spectra represent a representative experiment (n = 10). the in vivo absorption cross-sections normalized to Chl a. Both high salinity and nitrogen deficiency induced an increase of the absorption cross-section in Dunaliella (Fig. 2), as it was previously found in response to high irradiance (Berner et al., 1989). These results show that the package effect was smaller when cells were under osmotic stress or N limitation. Regarding the efficiency of light harvesting per unit chlorophyll a, it is evident that salinity and nutritional stress induced both a decrease in pigment content and a looser packing of the pigments. This led to an increase of the effective rate of light harvesting per unit chlorophyll a. Low salinity- and high nitrogen- grown cells showed higher pigment content and denser packing. According to Osborne & Raven (1986) and Berner et al. (1989), thylakoids of low light-grown plants become optically black and do not harvest more light per unit area of chlorophyll than cells with less pigmentation, i.e.they are less efficient.according to our results, salt or nitrogen-stressed algae had a similar response than high light-stressed ones. C/N ratio also increased in stress conditions (Fig. 3). Both high salinity (Fig. 3a) and nitrogen limitation (Fig. 3d) induced a significant increase of the C/N ratio. This change was due to variation of both cell C and N (Fig. 3b, e). An increase in salinity up to 3 M NaCl led to concomitant increases of cell C and N (Fig. 3b); however, N content did not change at salinity above 3 M NaCl, while cell C still continued to increase, leading to a significant increase of the C/N ratio at 4 M NaCl. In addition, cell carbon was maximum and cell nitrogen minimum under N limitation (Fig. 3e). Due to the change of cell volume with the change of salinity and N concentration (Jiménez & Niell, 1991), cell C and N were referred to cell volume. Figure 3c shows that both cell C and N content (fg µm 3 ) were maximum at 2 M NaCl, decreasing at 1 M and 4 M NaCl. Only cell N increased with increasing N concentration (Fig. 3f) while carbon content remained almost constant in the range of N concentration applied in this work (220 and 240 fg C µm 3 at 0.5 mm and 10 mm NO 3, respectively). Saturation of N concentration was reached at 5mMNO 3. In order to know the dynamics of the acclimation of cell C and N content to new salinity and N concentration, cells of D. viridis were transferred from low (0.5 mm) to high (5 mm) nitrate, and viceversa, and from low (1 M NaCl) to high salinity (3 M NaCl), and viceversa. The variation of salinity resulted in rapid changes of the C and N content (Fig. 4a, b). It was found that both cell C and N rapidly increased after a rise of the salinity. However, after a decrease in salinity there was an initial drop of both cell C and N. Initial concentration was recovered after 1 h, followed by a steady decrease of both elements. Thus, adaptation of cell C and N in D. viridis to the new salinity conditions seemed to take place in h. When the NO 3 concentration was raised from 0.5 to 5 mm, an increase of cell C occurred in the first hour (Fig. 4d), after which it continuously decreased to a level similar to that of long-term adapted cells. Nitrate limitation (from 5 to 0.5 mm) induced an immediate increase of cell carbon during the first 12 h after the transfer (Fig. 4d); following this period, C content remained steady. Cell N (Fig. 4e) followed a similar dynamic in both cases, showing a maximum after 1 h and a second peak after 12 h. Total adaptation to the new conditions was achieved within 24 h. Thus, C/N ratio in D. viridis (Fig. 4c, f) fully adapted within h when either nitrogen concentration or salinity were changed. It is important to point out that the responses of C and N

4 204 Figure 3. C/N ratio, total cell carbon and nitrogen, and carbon and nitrogen per unit volume, as a function of salinity (a, b, c) and nitrate concentration (d, e, f). (n=5; bars indicate starndard deviations). started immediately after the transition. According to Berner et al. (1989), 24 h is also the time needed for a complete rearrangement of the thylakoid membranes following a light intensity transition in D. tertiolecta. D. viridis adapts to new salt and nitrogen concentration by varying its growth parameters and biochemical composition, completing its acclimation to new growth conditions in 24 h. Falkowski & Owens (1980) determined that both cell volume and C/N ratio increased in high light-stressed cells of the marine microalga Dunaliella tertiolecta, in agreement with our data for salt and nitrogen-stressed cells. Thus, it is possible to conclude that different kind of stress induce similar responses in Dunaliella. Among others, there is a significant reduction of the growth rate and of the package effect, and an increase of the cell volume, the Chl a/chl b and Car/Chl a ratios, and of the C/N ratio. The response of the pigments also involves an increase of the ratio lutein/chl a and of the concentration of zeaxanthin.

5 205 Figure 4. Acclimation of cell carbon, nitrogen and C/N ratio in D. viridis after hyperosmotic (1 3 M NaCl) and hypoosmotic (3 1 M NaCl) shocks (a, b, c), and after increasing (0.5 to 5 mm) and decreasing (5 0.5 mm) the nitrate concentration of the medium (d, e, f). (n=3; bars indicate standard deviations). Acknowledgements This work was supported by project REN /MAR of the CICYT (Spanish Ministry of Science and Technology). References Avron, M., Osmoregulation. In Avron, M. & A. Ben-Amotz (eds) Dunaliella: Physiology, Biochemistry, and Biotechnology. CRC Press, Boca Raton: Ben-Amotz, A. & M. Avron, The role of glycerol in the osmotic regulation of the halophilic alga Dunaliella parva. Plant Physiol. 51:

6 206 Ben-Amotz, A. & M. Avron, Accumulation of metabolites by halotolerant algae and its industrial potential. Ann. Rev. Microbiol. 37: Ben-Amotz, A. & M. Avron The biotechnology of cultivating the halotolerant alga Dunaliella. Tibtechnology 8: Berner, T., Z. Dubinsky, K. Wyman & P. G. Falkowski, Photoadaptation and the package effect in Dunaliella tertiolecta (Chlorophyceae). J. Phycol. 25: Carnicas, E., C. Jiménez & F. X. Niell, Effects of changes of irradiance on the pigment composition of Gracilaria tenuistipitata var. liui Zhang et Xia. J. Photochem. Photobiol. 50: Cowan, A. K. & P. D. Rose, Abscisic acid metabolism in saltstressed cells of Dunaliella salina. Plant Physiol. 97: Falkowski, P. G. & T. G. Owens, Light-shade adaptation. Plant Physiol. 66: García-Jiménez, C. M., Estudio de un Medio Acuático Fluctuante: la Laguna Atalasohalina de Fuente de Piedra (Málaga). Ph.D. Thesis. University of Málaga. 300 pp. Gordillo, F. J. L., C. Jiménez, J. Chavarría & F. X. Niell, Photosynthetic acclimation to photon irradiance and its relation to chlorophyll fluorescence and carbon assimilation in the halotolerant green alga Dunaliella viridis. Photos. Res. 68: Jeffrey, S. W. & G. F. Humphrey, New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167: Jiménez, C. & F. X. Niell, Growth of Dunaliella viridis Teodoresco: effect of salinity, temperature and nitrogen concentration. J. appl. Phycol. 3: Jiménez, C. & U. Pick, Differential reactivity of ß-carotene isomers from Dunaliella bardawil toward oxygen radicals. Plant Physiol. 101: Johnson, M. K., E. J. Johnson, R. D. MacElroy, H. L. Speer & B. S. Bruff, Effects of salts on the halophilic alga Dunaliella viridis. J. Bacteriol. 95: Osborne, B. A. & J. A. Raven, Light absorption by plants and implications for photosynthesis. Biol. Rev. 61: Ruban, A. V., A. J. Young, A. A. Pascal & P. Horton, The effects of illumination on the xanthophyll composition of the Photosystem II light-harvesting complexes of spinach thylakoid membranes. Plant Physiol. 104: Shibata, K., Spectrophotometry of translucent biological materials-opal glass transmission method. Meth. Biochem. Anal. 7: Sukenik, A., J. Bennett, A. Mortain-Bertrand & P. G. Falkowski, Adaptation of the photosynthetic apparatus to irradiance in Dunaliella tertiolecta. Plant Physiol. 92:

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