Aquatic Botany, 36 (1990) 127-138 127 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

Short-Term Pigment Response of Corallina elongata Ellis et Solander to Light Intensity

PATRICIA ALGARRA and F. XAVIER NIELL

l)epartamento de Eeologia, Facultad de Ciencias Universidad de Mdlaga, Campus de" "l'eatin¢~.* 29071, Malaga (Spain)

( Accepted fl)r publication 29 August 1989 )

ABSTRACT

Algarra, P. and Niell, F.X., 1990. Short-term pigment response of Corallina elongata Ellis el Solander to light intensity. Aquat. Bot., 36: 127-138.

The responses of the light-harvesting antenna (phycobiliproteins and chlorophyll a) of the Rhodophycean algae Corallina elongata Ellis et Solander, have been studied in relation to irradi- ante. Laboratory and field experiments reveal a short-term (0 5 h) accommodation mechanism. After 5 h of light treatment, pigments reach a stable state under constant laboratory c~,nditions. Phycobiliproteins decrease when irradiance increases and chlorophyll a shows the reverse. The mechanism leading to this stable state is oscillatory. The oscillations are damped through time. Extreme conditions (conditions which induce a decrease in the pigment pool) enhance the oscil- latory behaviour. In the field, where irradiance is not constant, the oscillations are enhanced. This behaviour, already described in other related areas of research, allows a swift accommodation ol the algae to rapid changes in environmental irradiances.

INTRODUCTION

The study of short-term variations in physiological responses of algae is a subject of special interest. In phytoplankton, diel periodicity has been observed in photosynthesis-irradiance curves (Prezelin and Sweeney, 1977) and in cel- lular pigment content (Yentsch and Ryther, 1957; Harris, 1980; Owens et al.. 1980; Auclair et al., 1982). More recently, studies have related the daily fluc- tuating pattern of phytoplankton photosynthesis to a time series of irradiance variations, and attractive time-dependent models have been established (Fal- kowski and Wirick, 1981; Marra and Heinemann, 1982; Marra et al., 1985: Neale and Marra, 1985). In macroalgae this type of work is scarce and only recently have some authors studied short-term variation of photosynthesis (Pregnall and Rudy, 1985; Coutinho and Zingmark, 1987); however, the pig- ment variations in macroalgae have received less attention.

In macroalgae, ontogenetic adaptation (Kirk, 1983 ) has been studied through

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128 P. ALGARRA AND F.X. NIELL

"in situ" experiments (Ramus et al., 1976a,b, 1977; Kosovel and Talarico, 1979; Wheeler, 1980) or using laboratory cultures (Waaland et al., 1974; Yu et al., 1981). In all cases, macroalgae were sampled after they had adapted to the controlled or environmental light conditions, over long times (6-12 days).

Some authors have determined the time course of pigment synthesis under different light conditions (Mohr, 1980; Oelze-Karow et al., 1983). In general, the plants studied were etiolated and as Rudiger and Benz ( 1984 ) pointed out, extrapolation from etiolated to green plants must be made with caution.

The aim of this paper, is to describe the changes in pigment content of the alga at different irradiances over short time scales (0-5 h). Changes in the light-harvesting pigments were studied in the alga Corallina elongata Ellis et Solander brought from the field into the laboratory. The observed changes are compared with those detected in field plants.

MATERIAL AND METHODS

Specimens of C. elongata, which grows in the rocky intertidal were collected at "Punta Carnero" in the bay of Algeciras (Southern Spain).

The plants were incubated for 24 h in seawater at an irradiance of 600 zmol m -2 s-1 in order to decrease pigment concentrations and obtain standard initial conditions prior to the application of the different light treatments.

Cool-white fluorescent lamps were used (75, 400 and 1050/~mol m -2 s-1). Photon flux was measured with a Licor model SPH. Quantum SPQA0521 radiometer. Incubations were made under constant air flow and temperature (18 + 1 ° C ) Nutrient depletion and the consequent damage to the pigment pool was avoided by adding 5 ttM NO~- to the incubation batches. Approximately 4 g fresh weight of plant was introduced into 600 ml of seawater.

Laboratory sampling times chosen were 0.5, 1, 2, 3 and 5 h. A preliminary experiment revealed that after 5 h of light treatment, pigment concentrations were constant.

Field experiments were designed to compare the data from the short-term laboratory experiments with those obtained in natural conditions. For this purpose, pigment samples were taken between 0800 and 1100 h from plants in a homogeneous community of C. elongata. The sampling period was limited by the tidal range and the course of irradiance was measured during the sampling period with a radiometer as described above.

Chlorophyll a (Chl a) samples were extracted, in duplicate, by grinding the alga in 100% acetone saturated with MgCO3. The extinction coefficient of Tal- ling and Driver (1963) was used to calculate Chl a concentrations.

Phycobiliproteins were extracted in parallel on duplicate samples by grind- ing in phosphate buffer (0.1 M, pH 6.5) at 4°C. The homogenate was then centrifuged (Beckman, Rotor JA 21, 45 000 g, 0.5 h). The trichromatic equa- tions of Rosenberg (1981) were used to calculate the concentrations of R-phy-

PIGMENT RESPONSE OF CORALLINA TO LIGHT INTENSITY 129

coerythrin (PE), R-phycocyanin (PC) and allophycocyanin (APC). The ex- istence of these pigments in the alga had been shown by hydroxylapatite chromatography (Algarra, 1986).

Pigment concentration was expressed in mg g-1 dry weight. The synthesis rate (TS) (mg g-1 h-1 ) was calculated by the increase of pigment concentra- tion in successive samples.

The relationship between the different pigments was calculated using the number of chromophores (Kursar and Alberte, 1983) instead of units such as mg g- 1 or mol g- 1. This was done to avoid an overestimation of phycobilipro- teins, which are covalently linked to the protein fraction, whereas the weight of Chl a is calculated without the protein fraction. The equivalence of total phycobiliproteins (PE, PC, APC) to phycobilin chromophores was taken from O'Carra and O'Heocha (1976).

All the data were tested with a Model 1 one-way or two-way ANOVA (Sokal and Rohlf, 1969).

To describe the short-term response of photosynthetic systems two major aspects have been considered: (1) the pigment concentrations obtained after 5 h of light treatments, when algae had adapted to irradiance (pigment con- tent); (2) the oscillatory mechanism leading to it.

RESULTS

The changes in pigment concentrations as a function of time do not have a linear but an oscillatory response (Figs. 1 and 2 ).

Time and irradiance account independently for different percentages of the total variance of the experiments (Table 1 ). There is also an interactive influ- ence (significant values of variance owing to interaction) which controls the short-term response of pigment content to different light regimes (ix < 0.05).

Pigment content

Pigment concentrations obtained after 5 h of light t reatments are expressed in Fig. 3. One-way ANOVA, calculated for each pigment, indicates that irra- diance controlled pigment content significantly (a < 0.05). Phycobiliprotein concentrations decreased when irradiance increased. On the other hand, Chl a behaves in the opposite way; the maximal concentration being obtained at 1050/~mol m -2 s -1. These data gave PE/Ch l a, PC/Chl a and APC/Chl a declining ratios related to irradiance, which suggested the existence of a com- plementary pigment adaptation after 5 h of light treatment.

Although the concentration of phycobiliproteins increased when light inten- sity decreased, the ratios among the different water-soluble pigments indicate that PC and APC were present in a greater proportion than PE at low irradi- ance. In all the cases, the data fit well with exponential expressions (Table 2 ).

130

- 6 4

"7' 2

0

6

4

2

0

PE Chl a 0.6

0.4 "~

0.2

0.0

0.6

0.4

0.2 ~, t,o

0.0 ~"

0 1 2 3 4 5 Hours

P. ALGARRA AND F.X. NIELL

PC APC 1.2 0.6

0 . 8 ~ 0 . 4 ~

0.4 0.2

0.0 0.0 . . . . . ~&

~ ~ ~ 1.2 0 . 6 g

"~ 0.8 0.4

0.4 0.2

0.0 0.0 ~ ,

0.6 1.2 0.6

0.8 0.4 0.4

0.2 ~ 0.4 0.2

0.0 ~ 0.0 0.0 0 1 2 3 4 5 0 1 2 3 4 5 0 1 2 3 4 5 --

Hours Hours Hours

Fig. 1. Variations of PE (R-phycoerythrin) and Chl a (mg g-1 dry weight) concentrations as a function of time (h) at different irradiances. £ + standard deviation (n -- 2 )

Fig. 2. Variations of PC (R-phycocyanin) and APC (allophycocyanin) (mg g-1 dry weight) con- centrations as a function of t ime (h) at different irradiances, x +_ standard deviation (n -- 2 )

TABLE 1

Percentage of variance explained by the experimental control variables, light intensity and time, calculated by a two-way ANOVA with replication for the different pigments of the light-harvesting system ~

PE PC APC Chl a

Time 30.1 55.1 24.1 22.2 Light intensity 23.6 14.1 28.4 40.1 Interaction 43.3 26.9 35.3 31.7 Error 2.9 3.9 12.2 6.0

1R-phycoerythrin ( PE ), R-phycocyanin (PC), allophycocyanin ( APC ) and chlorophyll a ( C hl a ) (in all cases ol<0.05).

P I G M E N T R E S P O N S E O F CORALLINA T O L I G H T I N T E N S I T Y 131

~t 3 f r~

E

.tz ca | ~e

o, ~_" f , ' - ' 0

• C h l 2a

o P E

• P C

o A P C

1 . 5

1.0

0 . 5

0 . 0

®

• P E / C h l

• P C / C h l a

o A P C / C h l a

6o] @

• P E / P C

2 a P C / A P C

5 0 0 1 0 0 0

- 2 - 1 ~tmol rn s

Fig. 3. Variat ions o fp igment concentra t ions (no. o f c h r o m o p h o r e s g - l d r y w e i g h t ) (A) andra t ios between the different p igment concentrat ions, expressed as no. of chromophores g - 1 dry weight, (B and C) as a function in irradiance. These data were obtained after 5 h of light t rea tment , x, mean values ( n = 2 ). n -phycoery thr in (PE) , R-phycocyanin (PC) , allophycocyanin (APC) and chlorophyll a (Chl a).

TABLE 2

Exponent ia l fi t t ing of data presented in Fig. 3. Variation of p igment concentra t ions expressed in no. of chromophores g-1 and relat ionship between the different pigments in function of light intensi ty (/~mol m-2 s - 1 ). Data are obta ined after 5 h of adapta t ion to different light t rea tments

r Value

C h l a = 1 . 0 2 " 1 0 1 7 " x ° '16 0.97 PE = 4.64.1017.x o.lo 0.98 PC = 0 . 8 6 " 1 0 1 7 " X - 0 1 8 1.00 APC = 0.43"101V'x -°'12 1.00 P E / C h l a = 4 . 1 8 " x - ° ' 2 3 0.99 P C / C h l a = 0.36.x o.12 0.98 A P C / C h l a = 3.45.x -°19 0.97 P E / P C = 4.83-x °'2° 0.96 P E / A P C = 10.49"x °'is 0.95 P C / A P C = 4.57-x o.ls 0.96

R-phycoerythrin (PE) , R-phycocyanin (PC) , al lophycocyanin ( A P C ) a n d chlorophyll a (Chl a) ( in all cases c~ < 0.05 ).

132

Accommodation mechanism

P. ALGARRA AND F.X. NIELL

The oscillations observed (Figs. 1 and 2) allow some descriptions of the accommodation mechanism.

The phycobiliprotein oscillations were more pronounced at high than at low irradiances. At 1050/zmol m -2 s -1 the maximal (5.6; 1.01 and 0.58 mg g-1 of PE, PC and APC, respectively) and also, minimal concentrations were mea- sured (2.9, 0.19 and 0.12, for the same pigments). Oscillations are greater at high than at low irradiances when light induces a decrease in the content of phycobiliproteins (Fig. 3).

Unlike the water-soluble pigments, Chl a showed pronounced oscillations at low light irradiance when this light regime induced a decrease of Chl a content after 5 h of light treatment. When light irradiance increased, oscillations were damped, but the concentrations obtained after 5 h were higher.

When the data were expressed as a synthesis or degradation rate (mg g-1 h - 1 ) results were very clear (Figs. 4 and 5 ): the oscillations were related to the

PE

-3 . . . . ,

~ 3 , , ,

C h l _a

0.1 ~

-0.1 3.

-0.3 ~,

PC

2

0

-1 , , , i r

7

0 . 1 ~ I

e ~ 0 -0.1 3, '

t~

-0.3 ~ , ~ -1

APC

0.8

0.4 ~

0.0

3 ,

-0.4 ~ J , , i w ~.

0.4 ~

0 . 0 3 .

t~

-0.4 ~Z,

3 0.3 2 0.8

l o , : 1 0 4 -

-0.1 0 -1 0.0 3

-3 . . . . . -0.3 -1 . . . . . -0.4

1 2 3 4 5 0 1 2 3 4 5 0 l 2 3 4 5 0 1 2 3 4 5

H o u r s H o u r s H o u r s H o u r s

Fig. 4. Rates of synthesis (rag g-1 dry weight h - i ) of PE (R-phycoerythrin) and Chl a as a function of time (h) at different irradiances.

Fig. 5. Rates of synthesis (mg g-1 dry weight h -1) of PC (R-phycocyanin) and APC (allophy- cocyanin) as a function of time (h) at different irradiances.

PIGMENT RESPONSE OF CORALLINA TO LIGHT INTENSITY 1:]:~

rate of synthesis followed by greater rates of degradation (in absolute values ) at high irradiances for the phycobiliproteins and at low irradiances for Chl a.

The oscillations were damped through time, independently of the light treat- ment used. The first oscillation was characterized by a higher rate of synthesis than the second. This phenomenon was observed in all the pigments studied and at the different light regimes and it could be argued that the oscillation process died out after 5 h when the concentration of pigments became stable.

Field study

Field experiments were designed to complement the results obtained in the laboratory. Short experiments from 0800 to 1100 h approximately, show the existence of oscillatory behaviour in the process of pigment adaptation in the algae in nature (Figs. 6 and 7).

Two phycobiliprotein peaks were detected during a period of 3 h. The second

". 2000 J y

eq '~ 1000

o 9 ' f o ' 1'1

PE Chl _a 6 0 . 6

"r. PC APC

, l °

~ 0.4 •

0 . 4 0 . 2

0 . 0 . . . . . 0 . . . . . . 9 10 11 9 10 11

"7, ,m

PE 6

PC

(?Ill : j

l . . . . . . 0.6 -- ----

APC

'¢t~ 0.21 0.

-0.2 -0.

-0.6| -1.2-~ 9 10 11 9 10 I1

H o u r s H o u r s Hour~ Hour~

Fig. 6. Variations of irradiance (/tmol m-2 s - 1 ) and pigment concentrations (mg g- ~ dry weight ) at different times (h), in field conditions. R-phycoerythrin (PE) , R-phycocyanin (PC) allophy- cocyanin (APC) and chlorophyll a (Chl a).

Fig. 7. Rates of synthesis (mg g- 1 dry weight h - 1 ) of the different pigments at different times ( h ) in field conditions. R-phycoerythrin (PE) , R-phycocyanin (PC), allophycocyanin (APC) and chlorophyll a (Chl a).

134 P. ALGARRA AND F.X. NIELL

is characterized by a higher rate of synthesis than the first. This pattern is, then, clearly different from those obtained in the laboratory where the second oscillation was always lower. In the field, irradiance is not constant but in- creasing during the experiments (Fig. 6); as a consequence the oscillations of phycobiliprotein concentrations are not damped but enhanced. For Chl a, a lower rate of synthesis was noted in the second oscillation, when irradiance increased, agreeing with the laboratory results.

It is also interesting to note that oscillations had a larger amplitude in field experiments suggesting that the amplitude of oscillations depends not only on the irradiance values, but also on the variation of this photon flux.

DISCUSSION

The results of experiments to determine the time-course of the pigment re- sponse of C. elongata indicate that this alga adjusts the content of its photo- synthetic pigments within 5 h of exposure to light. Low light favours an in- crease of phycobiliproteins and a decrease of Chl a. The opposite response is detected at high irradiance.

The short-term variation of pigment content to light intensity which could be called accommodation or adaptation, follows the same pattern as ontoge- netic adaptation (in the sense of Rabinowitch, 1945) observed when sun and shade morphotypes of C. elongata are compared (Algarra and Niell, 1987).

The mechanism described here is compatible with others manifested at longer time scales. In this way complementary behaviour between Chl a and PE has been detected during seasonal variations in Gracilaria foliifera (Forssk~l) B~rgesen by Rosenberg and Ramus (1982) and in Gracilaria verrucosa (Huds.) Papenfuss by Kosovel and Talarico (1979). In a shorter time-scale, 1-3 months (Beer and Levy, 1983 ) or 5-6 weeks (Waaland et al., 1974), the same reversal response of Chl a and PE content to light intensity was detected in Griffithsia pacifica Kylin and Gracilaria sp., respectively. According to Dring (1981) and Ramus (1983), these data are in partial agreement with the complementary theory of Engelmann (1883), because in these experiments the light parameter to which algae respond is quantum irradiance and not spectral distribution.

All phycobiliproteins are enhanced by low irradiance, APC and PC more so than PE. APC and PC are physically close to the reaction centre of PS II (P680) and are responsible for the canalization of photons towards it (Gantry, 1981 ). This function could explain their increase relative to the more distant PE, under conditions of light limitation. Nevertheless, further evidence is ne- cessary to determine if the number rather than size of phycobilisomes changes with variations in the pigment composition, as it has been shown in G. pacifica (Waaland et al., 1974).

The mechanism of short-term accommodation is an oscillatory process: fast synthesis and degradation rates are detected. Even though few data are found

PIGMENT RESPONSE OF CORALLINA TO LIGHT INTENSITY 135

in the literature, some comparisons can be made with Chl a synthesis rate of Chlamydomonas reinhardtii Dangeart (Hoober et al., 1982). These authors found a rate of 6.6 ttg mg-1 protein h-1. Transformation of the data using protein content in C. elongata (around 14 mg g- 1 dry weight, Vergara, personal communication, 1989), the synthesis rates for Chl a range between 3.5 and 20 /~g mg-1 protein h-1. So, the same order of values is evident in spite of the different degree of complexity of unicellular and pluricellular algae.

Auclair et al. (1982) also found an oscillatory process of Chl a synthesis in estuarine phytoplankton. One or two oscillations are detected in a lag of 5 h, characterized by successive high synthesis and degradation rates. Concentra- tions of Chl a (#g l - 1 rose four to ten-fold in a I h lag. As was stated previously (Riper et al., 1979; Owens et al., 1980) oscillatory changes in cellular content occur as a regulatory mechanism for maximizing the efficiency of the available light energy.

In aquatic angiosperms, Zostera noltii Hornem and Z. marina L. (Jimenez et al., 1987 ) similar synthesis and degradation rates (from 0.8 to - 0 . 8 mg Chl a g- 1 dry weight h - 1 ) are detected after short-term incubations (1 h ) made to estimate net assimilation rate.

As Sivak and Walker (1987) state, oscillations are common in biological as well as in chemical and physical processes and usually reflect the action of negative feed-back mechanisms.

Berge et al. (1984) cited, among other processes, the existence of oscillations in the synthesis of proteins, in glycolysis and photosynthesis, and agreed that the oscillatory nature arises from interaction of several self-regulated systems. Induction of oscillatory behaviour has recently received the attention of Sivak et al. (1985), Walker and Osmond (1986) and Stitt (1986). Oscillations are displayed in several phenomena related to energy input in plants; CO2 uptake, 02 evolution and fluorescence (Sivak and Walker, 1987, Walker and Osmond, 1986; Stitt, 1986). All these phenomena are directly or indirectly related to pigment synthesis. Oscillatory behaviour is favoured by high light irradiances, high CO2 concentrations or low 02 concentrations; in extreme conditions, such as those that favoured pigment oscillation in the experiments described in this paper.

Phycobiliproteins decrease at extremely high irradiances and this enhances the oscillatory mechanism of adaptation. In contrast, Chl a behaviour is com- plementary to that of phycobiliproteins. Low light irradiances then favour the oscillations.

In the laboratory experiments, at constant irradiance, the oscillations be- come damped to a stable level. However in natural conditions, the increase of irradiance through the day amplifies the oscillations, especially for phycobili- proteins whose pool concentration is drastically limited by high irradiance.

This kind of accommodation process provides an important advantage to algae. They can adapt rapidly to the natural variation of incident light and

136 P. ALGARRA AND F.X. NIELL

adjust pigment concentrations to the light environment and alleviate the effect of rapid changes of energy input.

From a thermodynamic point of view, this oscillatory behaviour could be considered as dissipative. The stable state is reached through partial successive stable states. Transient phases coincide with high input of energy giving a high synthesis rate, these are followed by low energy flow (low rate of synthesis). Each t ransient phase is then characterized by an energy dissipation and the different dissipative phases decrease in amplitude. This kind of behaviour has been described at different scales of time and space (Nicolis and Prigogine, 1977; Wagensberg and Lurie, 1979; Margalef, 1980; Niell, 1981; Niell and Var- ela, 1984) and could be at tr ibuted to a self-organization of the systems (Pri- gogine et al., 1977; Velarde, 1978).

The understanding of the physiological mechanism of this kind of process requires further specialized studies from a biochemical, physiological and physical perspective. But, its detection requires ecological observations under field conditions.

ACKNOWLEDGEMENTS

This work was supported by the CAICYT project no. 1063/85 of the Spanish Ministry of Education and Science.

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