Rhythms in the photosynthetic system

Diurnal rhythms in photosynthetic capacity (photosynthetic rate per unit biomass at light saturation) have been described for phytoplankton 318,530, 1085,677,858 (reviewed by Sournia, 1974, and Prezelin, 1992) and for multicellular benthic algae.167,461,665 Photosynthetic capacity rises, often several-fold, during the early part of the day to a maximum that can be reached any time from about mid-morning to mid-afternoon and then declines during the rest of the day and remains low during the night. Figure 12.21 shows the time course of variation in P*m for the phytoplankton in the St Lawrence estuary during the course of a week.302 In some species, both benthic and planktonic, it has been shown that this diurnal variation is not directly controlled by environmental parameters but is a true circadian rhythm that continues for several cycles in cells kept in the dark.

With cultures, a daily periodicity in P*m has been shown to be present in some, but not all, marine diatom, dinoflagellate and chrysophyte species:529 the species that showed no day/night differences in P*m were small, rapidly dividing types, whereas larger, slower growing cells almost uniformly showed marked changes. Detailed studies of this rhythm in marine dinoflagellates have been carried out by Sweeney and coworkers. The photosynthetic rate per cell in cultured Glenodinium and Ceratium varies two- to six-fold during the cycle, when measured under light-limiting as well as light-saturating conditions.1084,1086 The fact that the rate variation occurs under light-limited conditions led Prezelin and Sweeney (1977) to conclude that it is variation in the light reactions rather than the dark reactions of photosynthesis that are primarily responsible for the diurnal rhythm: it had previously been shown that carboxylase activity does not vary during the cycle.190 There is no significant change in the pigment content or the absorption spectrum of the cells during the cycle, but the initial slope (a) of the photosynthesis versus irradiance curve varies in parallel with the photosynthetic capacity. This implies that the quantum yield of photosynthesis - the efficiency with which the cells use the quanta that have absorbed - changes in a cyclical manner. For natural phytoplankton populations also, off the Southern California coast, Harding et al. (1982a) found that a and P*m varied (three- to ninefold) in parallel during the day: this applied to both diatom- and dinofla-gellate-dominated assemblages. Changes in chlorophyll content were much smaller and did not correlate with the changes in photosynthetic activity (which was, in any event, expressed per unit chlorophyll). Prezelin and Sweeney suggest that there is a cyclical variation in the proportion of the total photosynthetic units present that are functional.

In the multicellular brown alga Spatoglossum pacificum the mechanism may be different. There is evidence that the approximately two-fold daily variation in photosynthetic capacity in this alga is due to variation in the activity of the CO2-fixing enzyme system.1480 In the tropical red macro-alga, Kappaphycus alvarezii, grown on a 12 h light: 12 h dark cycle, Granbom et al. (2001) observed a regular rhythm in photosynthetic activity, consisting of an increase in oxygen evolution rate towards noon, followed by a decrease of about one third in the afternoon. When the plants were transferred to continuous light the circadian rhythm in photosynthetic activity continued, with a period of ~19 to 23 h, for several cycles. Schubert et al. (2004) found that the diminution in O2 evolution in the afternoon was accompanied by decreases in both photo-synthetic capacity (Pm) and a, and these continued to decrease (when measured in the light) during the 12 h dark period, levelling off at their minimum values about half way through. The troughs in the continued rhythm of photosynthetic activity in continuous light were also accompanied by drastic falls in photosynthetic capacity (Pm) and a. The fall in a was proportionately greater than the fall in P*m, so that the light saturation onset parameter, Ek (which is equal to P*m/a), rose to a peak in each trough of the cycle. Since a = df*fm (§10.3), the cyclical decrease in a must correspond to a cyclical decrease in the quantum yield of photosynthesis or of the specific absorption coefficient of the alga (§9.4) for PAR (m2mgchl a-1). Pigment ratios (chl a/phycoerythrin, chl a/carotenoid) did not change during the cycle, indicating that it was the quantum yield that was changing. Fluorescence emission spectra of frozen samples indicated that in the troughs of the cycle the phycobilisomes were, proportionately, transferring much more of their energy to photosystem II than to photosystem I. The fundamental mechanism underlying this circadian rhythm remains unclear: changes in the quantum efficiency of photosystem II or I, and/or changes in excitation energy distribution to the reaction centres, are possibilities, but a cyclical change in carboxylase (which was not measured) is also a possibility.

The red alga, Grateloupia turuturu, shows a similar circadian rhythm in photosynthetic activity to that described above for Kappaphycus. Goulard et al. (2004) investigated the concurrent changes in the levels of the gene transcripts (mRNA) encoding the a and ß subunits of phycoerythrin and subunits of Rubisco. Abundance of both transcripts exhibited diurnal and circadian changes, implying control of transcription by the circadian clock. In light-dark cycles the Rubisco transcript peaked around midday, and the phycoerythrin transcript peaked between midday and afternoon. The authors suggest that the correlation of the oscillations of mRNA abundance with the rhythm of photosynthetic oxygen evolution is likely to be of physiological relevance.

What, if any, advantage algae derive from cyclical variations in their photosynthetic capability remains unknown. Conceivably, after the main photosynthetic period is finished each day, certain proteins of the photo-synthetic apparatus might be broken down so that their amino acids can be used for other cellular purposes: the proteins would then be resynthe-sized each morning. These daily variations in photosynthetic properties may affect the amount of primary production that is actually carried out. The effect of variation in light-saturated photosynthetic rate may be, at least in part, offset by the fact that solar irradiance itself varies roughly in parallel. The rate of light-limited photosynthesis also shows diurnal variation, however, and this may reduce the amount of primary production that the cells achieve early and late in the day. Harding et al. (1982b) calculated, for Californian coastal phytoplankton, that as a result of the daily periodicity in the parameters of the photosynthesis versus irradi-ance curves, the primary production achieved would be 19 to 39% less than if the values of P*m and a remained constant all day at their maximum values.

In calculations of integral daily photosynthesis, although the diurnal variation of solar irradiance is taken into account, it is commonly assumed that the values of a and P*m observed at midday apply throughout the day. Making this assumption for the Californian phytoplankton yielded values for daily integral photosynthesis ranging from 15% greater to 20% less than values calculated taking account of periodicities in a and P*m. The variation in size and direction of the discrepancy is caused by variation in the timing of the photosynthetic activity maximum: when this is not at midday, the midday values of a and P*m come closer to the mean values, and so the errors may not be so great. For phytoplankton in the St Lawrence estuary (Canada), Vandevelde et al. (1989) found that calculations of integral daily photosynthesis made using the midday values of a and P*m gave production estimates 15 to 43% greater than those that took into account the variation in these photosynthetic parameters during the day.

Ramus and Rosenberg (1980) measured the actual photosynthetic rate of five intertidal species (two green, two brown, one red) at hourly intervals during the day in seawater tanks (such that Ed was 70% of the subsurface value) exposed to ambient sunlight. The most common behaviour pattern on sunny days was for the photosynthetic rate (per unit chlorophyll a) to reach its peak in the morning, while solar irradiance was still well below its daily maximum, to decline somewhat during the middle part of the day under the most intense Sun, and then sometimes to show a partial recovery late in the afternoon, before declining again to zero, with falling light levels, towards sunset. Ramus and Rosenberg concluded that an afternoon depression in photosynthesis must be of normal occurrence (on sunny days) in these five species in their intertidal habitat. On cloudy days, when light saturation does not occur, the curve of photosynthetic rate is approximately symmetrical about the time of the Sun's zenith, and in the case of the most light-sensitive species (the rhodophyte Gracilaria foliifera) it seemed that total daily production would actually be higher than on sunny days. The characteristic sunny-day diurnal pattern observed in this work is likely to result from the simultaneous operation of a number of independent processes, particularly photoinhibition coming into operation when solar intensities are at their highest, together with the underlying circadian rhythm in photosyn-thetic capacity with its pre-midday morning peak.167,665

Although, as we have seen, no diurnal fluctuation in pigment content was observed in marine dinoflagellates under laboratory conditions, Yentsch and Scagel (1958) have described such a fluctuation in a natural phytoplankton population dominated by diatoms. In a North American coastal (Pacific) water they found that the chlorophyll content per cell fell by 50 to 60% during late morning, remained approximately constant during the afternoon, and then rose again during the evening. Auclair et al. (1982) studied fluctuations in chlorophyll content of estuar-ine phytoplankton under semi-natural conditions. Water from the St Lawrence estuary was transferred to a 1200 litre tank, exposed to sunlight and the chlorophyll content per litre of water was followed over the next 45 h. Cell numbers showed little change. Chlorophyll content fluctuated up and down in a cyclical manner, through an approximately two-fold range with maxima in chlorophyll content occurring about every 6 h. Auclair et al. were able to correlate the variation in pigment content with tidal movements. Assuming the rhythm in the tank was a continuation of that in the estuary, it seemed that the times of maximum chlorophyll content corresponded to the periods of maximum current speed and turbulence and therefore probably, as a result of enforced circulation, to periods of lower average irradiance on the cells. The times of minimum chlorophyll content corresponded to periods of slack water in which a stability gradient was established resulting in a higher irradiance on the cells. It makes sense that the cells should increase their light-harvesting capacity during periods of low light intensity: what is noteworthy about this system is that they do it so rapidly, doubling their chlorophyll content in 2 to 3 h. Regular cyclical changes in phytoplankton pigment content may be more common in nature than we realize. The patchiness of the horizontal distribution of phytoplankton and the additional complicating factor of water movement make it difficult to unequivocally demonstrate such changes in large water bodies.

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