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SCIENTIFIC CORRESPONDENCE

Solar UV Radiation Drives CO₂ Fixation in Marine Phytoplankton: A Double-Edged Sword¹

Marine Biology Institute, Shantou University, Shantou, Guangdong 515063, China (K.G., Y.W., G.L., H.W.); State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, China (K.G.); State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei 430072, China (K.G.); and Estación de Fotobiología Playa Unión and Consejo Nacional de Investigaciones Científicas y Técnicas, 9103 Rawson, Chubut, Argentina (V.E.V., E.W.H.)

Photosynthesis by phytoplankton cells in aquatic environments contributes to more than 40% of the global primary production (Behrenfeld et al., 2006). Within the euphotic zone (down to 1% of surface photosynthetically active radiation [PAR]), cells are exposed not only to PAR (400–700 nm) but also to UV radiation (UVR; 280–400 nm) that can penetrate to considerable depths (Hargreaves, 2003). In contrast to PAR, which is energizing to photosynthesis, UVR is usually regarded as a stressor (Häder, 2003) and suggested to affect CO₂-concentrating mechanisms in phytoplankton (Beardall et al., 2002). Solar UVR is known to reduce photosynthetic rates (Steemann Nielsen, 1964; Helbling et al., 2003), and damage cellular components such as D1 proteins (Sass et al., 1997) and DNA molecules (Buma et al., 2003). It can also decrease the growth (Villafañe et al., 2003) and alter the rate of nutrient uptake (Fauchot et al., 2000) and the fatty acid composition (Goes et al., 1994) of phytoplankton. Recently, it has been found that natural levels of UVR can alter the morphology of the cyanobacterium Arthrospira (Spirulina) platensis (Wu et al., 2005b).

On the other hand, positive effects of UVR, especially of UV-A (315–400 nm), have also been reported. UV-A enhances carbon fixation of phytoplankton under reduced (Nilawati et al., 1997; Barbieri et al., 2002) or fast-fluctuating (Helbling et al., 2003) solar irradiance and allows photorepair of UV-B-induced DNA damage (Buma et al., 2003). Furthermore, the presence of UV-A resulted in higher biomass production of A. platensis as compared to that under PAR alone (Wu et al., 2005a). Energy of UVR absorbed by the diatom Pseudo-nitzschia multiseries was found to cause fluorescence (Orellana et al., 2004). In addition, fluorescent pigments in corals and their algal symbiont are known to absorb UVR and play positive roles for the symbiotic photosynthesis and photoprotection (Schlichter et al., 1986; Salih et al., 2000). However, despite the positive effects that solar UVR may have on aquatic photosynthetic organisms, there is no direct evidence to what extent and how UVR per se is utilized by phytoplankton. In addition, estimations of aquatic biological production have been carried out in incubations considering only PAR (i.e. using UV-opaque vials made of glass or polycarbonate; Donk et al., 2001) without UVR being considered (Hein and Sand-Jensen, 1997; Schippers and Lürling, 2004). Here, we have found that UVR can act as an additional source of energy for photosynthesis in tropical marine phytoplankton, though it occasionally causes photoinhibition at high PAR levels. While UVR is usually thought of as damaging, our results indicate that UVR can enhance primary production of phytoplankton. Therefore, oceanic carbon fixation estimates may be underestimated by a large percentage if UVR is not taken into account.

	DIRECT AND INDIRECT EVIDENCE OF UV-DRIVEN CARBON FIXATION

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There was a significant photosynthetic carbon fixation (Fig. 1A ) when surface phytoplankton assemblages (collected during summer 2005 and summer 2006) were exposed to solar UVR alone (i.e. when PAR was filtered out). The rate of carbon fixation per unit chlorophyll (Chl) was significant (P < 0.05) even under low levels of UVR (i.e. <5 W m^–2). UVR-energized CO₂ fixation increased linearly with increasing UVR, and it was not saturated at 33.3 W m^–2 (i.e. about half of the noontime irradiance, about 100 µmol photons m^–2 s^–1). The apparent UVR utilization efficiency (i.e. the initial slope of the carbon fixation versus UVR relationship) was about 8 x 10^–3 and 6 x 10^–3 µg C (µg Chl a)^–1 h^–1 (µmol photons m^–2 s^–1)^–1 for UV-A and UVR, respectively. The difference in the rate of carbon fixation between samples receiving UV-A + UV-B or merely UV-A was only significant at UVR levels >13.3 W m^–2, with samples receiving UV-B reducing photosynthesis up to 20% (P < 0.05) at the highest radiation tested (i.e. approximately 25.0 W m^–2).

View larger version (13K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 1. A, CO2-fixation rates measured in phytoplankton assemblages as a function of solar UVR (280–400 nm, black symbols) or UV-A (320–400 nm, white symbols) on August 4, 2005, September 27, 2005, and July 8 to 10, 2006. The solid and dashed lines represent a linear fit of the data (P < 0.0001), while the dotted lines are the 95% confidence limit. Mean solar irradiances ranged from 312.0 to 486.5, 44.6 to 59.2, and 1.97 to 2.56 W m–2 for PAR, UV-A, and UV-B, respectively, throughout the incubations. B, CO2-fixation rates of phytoplankton assemblages exposed to PAR + UV-A + UV-B (280–700 nm) and PAR + UV-A (320–700 nm) as compared to those exposed only to PAR. The mean irradiances of PAR, UV-A, and UV-B during the incubations were 224.3, 37.2, and 1.76 W m–2 on the cloudy days (July 29, September 10, and September 22, 2005), and 318.3, 50.1, and 2.33 W m–2 on the sunny days (August 4 and September 27, 2005). The mean photosynthetic carbon fixation rates under PAR alone were 7.16 and 4.98 µg C (µg Chl a)–1 h–1 on cloudy and sunny days, respectively. The vertical bars represent SD (n = 4 to approximately 6).

	ENHANCEMENT AND INHIBITION OF PRIMARY PRODUCTION IN THE WATER COLUMN

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Photosynthesis versus irradiance (P-E) curves were obtained for these phytoplankton assemblages under solar radiation with or without UVR (Fig. 2A ); positive and negative impacts of UVR were evidenced similarly to those determined during cloudy and sunny days. The apparent light utilization efficiency was 0.078 and 0.046 µg C (µg Chl a)^–1 h^–1 (µmol photons m^–2 s^–1)^–1 for samples receiving PAR + UVR or PAR alone, respectively. The maximum photosynthetic rate, however, was approximately 20% lower under UVR + PAR [7.13 µg C (µg Chl a)^–1 h^–1] than under PAR alone [8.90 µg C (µg Chl a)^–1 h^–1]. The photosynthetic carbon fixation became saturated at PAR irradiances of 135 and 275 µmol photons m^–2 s^–1 for samples receiving PAR + UVR or only PAR, respectively. At PAR irradiances lower than 300 µmol photons m^–2 s^–1, there was a significant utilization of UVR (P < 0.05), and phytoplankton assemblages had a higher rate of photosynthesis than when samples were exposed only to PAR. On the other hand, at PAR irradiances higher than 680 µmol photons m^–2 s^–1, a significant UVR-induced photosynthetic inhibition (P < 0.05) was observed and increased with increasing irradiance.

View larger version (9K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 2. A, Photosynthesis versus irradiance curve under PAR (white circles) and PAR + UVR (black circles) conditions; dotted lines represent 95% confident limit. The mean irradiances (PAR, UV-A, and UV-B) during the incubations (August 6 and 8, 2005) were 321, 50.5, and 2.1 W m–2, respectively. B, Vertical distribution of estimated daily photosynthetic production on a sunny day (black symbols; July 5, 2006) and a cloudy (white symbols; August 13, 2006) day. The doses (and mean irradiances) of PAR for these days were 14 (280 W m–2) and 0.9 MJ m–2 (19.6 W m–2), respectively. Note that even on the sunny day without cloud coverage, UVR-enhanced production (shaded areas) is larger than the UVR-related reduction (open area enclosed by the lines). C, Daily primary production (PP) ratios of samples exposed to the full solar spectrum compared to those exposed to PAR only. The estimation of PP was based on the P versus E curves. The relationship of solar daily dose with PP ratio is significant (P < 0.001; y = 0.91xexp[3.19/(x + 5.82)]); R2 = 0.99.

	PHYTOPLANKTON COMPOSITION AND UV-ABSORBING COMPOUNDS

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During the study period, microplankton cells (>20 µm) accounted for 18% and 38% of total Chl a concentration (that ranged from 1.12 to approximately 7.79 and 6.79 to approximately 8.50 µg L^–1 during the summers of 2005 and 2006, respectively). The microplankton species were mainly represented by the diatom genera Chaetoceros, Rhizosolenia, Pseudonitzschia, and Skeletonema, whereas piconanoplankton (<20 µm) was represented by unidentified monads and flagellates. Absorption of the methanolic extracts of the phytoplankton assemblages showed a distinguishable absorption peak between 330 to 340 nm, indicating the presence of UV-absorbing compounds (Fig. 3 ).

View larger version (12K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 3. Optical density of methanol extracts from the natural phytoplankton assemblages (July 8–10, 2006). Vertical bars represent SD (n = 3).

	DATA EVALUATION, POSSIBLE MECHANISMS INVOLVED, AND IMPLICATION

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UVR can be absorbed by a number of cellular substances, such as proteins and ATP (Kondo et al., 1979). Even Chl a has a partial absorption of the near UV range (Harris and Zscheile, 1943). However, the dominant UV-absorbing compounds found in phytoplankton cells are MAAs (absorption range 310–360 nm) in eukaryotic cells (Dunlap et al., 1995) and scytonemin (absorption peak at 370 nm) in prokaryotic species (Garcia-Pichel et al., 1992). An oligosaccharide-mycosporine amino acid with absorption peaks of 312 nm and 335 nm was also reported in a cyanobacterium (Böhm et al., 1995). MAAs are known to play an important role as a cellular screen to filter UVR, limiting its harmful effects (Dunlap et al., 1995). Mycosporine-like Gly, shinorine, and mycosporine-Gly/Val were found to be able to transmit absorbed UVR energy to Chl a in the haptophyte Phaeocystis antarctica (Moisan and Mitchell, 2001). In the diatom P. multiseries, absorbed UVR energy was also evidenced to generate Chl fluorescence (Orellana et al., 2004). The UV energy absorbed by the corals and their algal symbiont was found to emit fluorescence (Schlichter et al., 1986; Salih et al., 2000). It is thus possible that quanta in the UVR region that caused photosynthetic carbon fixation by the phytoplankton assemblage (Fig. 1A) could be absorbed by MAAs (Fig. 3) and then transferred to Chl a; the transferred energy is utilized to drive the photosynthetic carbon fixation (Figs. 1, A and B, and 2A). In fact, theoretically, and from an evolutionary point of view, phytoplankton cells may have devised the use of short wavelengths down to 300 nm for photosynthesis (Neori et al., 1988; Holm-Hansen et al., 1993).

UV-A and blue light are known to signal photoresponses via two types of photoreceptors, cryptochromes and phototropins (Brunner et al., 2000; Lin, 2002; Huang et al., 2004). Previous studies have shown that low levels of UVR can enhance CO₂ acquisition in the diatom Skeletonema costatum by stimulating the extracelluar (periplasmic) carbonic anhydrase (data not shown). Blue light was demonstrated to increase the activity of plasma membrane H⁺-ATPase in a brown alga, Laminaria digitata (Klenell et al., 2002). UV-A, as a neighboring radiation of blue light, may serve a similar function and accelerate CO₂ acquisition and fixation. Intracellular inorganic carbon concentration increased, though photosynthetic carbon fixation was inhibited, in the marine green alga Dunaliella tertiolecta when exposed to UV-B (Beardall et al., 2002). CO₂-concentrating mechanisms (Giordano et al., 2005) in phytoplankton may be affected by UVR.

Phytoplankton cells, circulating up and down by waves or mixing in the ocean, are frequently exposed to reduced levels of solar radiation even at noontime; thus, they tend to be less photoinhibited by high levels of UVR and PAR (due to short exposures) than previously suggested. Because attenuations of PAR and UVR are not the same in any marine habitat so far examined, effects of UVR on primary production could differ between oceanic and coastal waters. Nevertheless, total oceanic primary production in tropical areas could have been previously underestimated for the euphotic zone. Since UVR may affect the new (potentially sedimentable) productivity of the ocean via influencing phytoplankton photosynthesis, the marine biological removal of dissolved inorganic carbon with UVR being considered would add to the oceanic sink of CO₂ approximated to date (Sabine et al., 2004). Taking into account our data for the summers of 2005 and 2006, we calculated that the daily primary production for the tropical coastal euphotic zone would be underestimated by as much as 13% if solar UVR is not considered. This proportion of "unaccounted" CO₂ fixation would be higher in seasons with more cloudy days.

	MATERIALS AND METHODS

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Study Area and Sampling

This study was performed in a coastal area of the South China Sea (23°29'N, 117°06'E) during the summers of 2005 and 2006. Surface seawater samples were collected 500 m offshore with a 10-L acid-cleaned (1 N HCl) carboy in the morning and returned to the laboratory (within 15 min) of the Marine Biological Station of Shantou University, where the experiments were carried out as described below.

Solar Radiation Treatments and Monitoring

To determine UVR effects upon phytoplankton assemblages, solar radiation treatments were implemented (duplicate or triplicate) as follows: (1) PAR + UV-A + UV-B uncovered quartz tubes; (2) PAR + UV-A quartz tubes covered with Folex 320 filter (to filter out UV-B); (3) PAR-alone quartz tubes covered with Ultraphan 395 filter (to filter out UVR); (4) UV-A + UV-B quartz tubes covered with UG11 filter (to filter out PAR); (5) UV-A quartz tubes covered with UG11 + Folex 320 filter (to filter out PAR and UV-B); and (6) darkness quartz tubes covered with UG11 filter and Ultraphan 395 (control A) or covered with aluminum foil (control B).

The transmission spectra of the filters Folex 320 (Montagefolie; no. 10155099; Folex) and Ultraphan 395 (UV Opak; Digefra) are given by Figueroa et al. (1997). UG11 filter (Schott) cuts off 100% PAR and transmits 53.7% of UV-A and 63.8% of UV-B (when measured at noontime under sunlight). The uncovered quartz containers received 4% higher PAR radiation in water (measured by inserting a PAR sensor inside the quartz container) compared with the covered tubes with 395 or 320 filters due to the reflection caused by these filters. This was calibrated for establishment of the photosynthesis versus irradiance (P-E) relationship.

To determine the UVR-only impacts on carbon fixation, quartz tubes containing surface seawater were placed in a PAR-opaque box with UG11 filter sandwiched and sealed in the cover. Thus, the P-E curves were obtained in the absence of PAR under no and up to five layers of neutral density screens so that UVR irradiance varied from 53.7 to <1.6%. To calculate the apparent utilization efficiency of UVR, UVR irradiance was converted from W m^–2 to photon flux by multiplying by 3.02 according to Neale et al. (2001) and solar spectrum estimated using the STAR software (Ruggaber et al., 1994). To determine the impacts of PAR with and without UVR, measurements of the photosynthetic carbon fixation were carried out in different weather conditions (i.e. cloudy and sunny) under the radiation treatments as described above.

Incident solar radiation (UV-B: 280–315 nm; UV-A: 315–400 nm; PAR: 400–700 nm) was continuously monitored using a broadband solar radiometer (ELDONET; Real Time Computer). This instrument measures every second direct and indirect radiation (Ulbrich integrating sphere) and records the averaged data at 1-min intervals (Häder et al., 1999).

Determination of Photosynthetic Carbon Fixation and Estimation of Primary Production

Photosynthetic carbon-fixation rates were determined as follows: Water samples, pre-filtered by a 180-µm-pore mesh (to eliminate large zooplankton specimens) were dispensed into 20-mL quartz tubes and inoculated with 0.1 mL of 5 µCi (0.185 MBq) of labeled sodium bicarbonate (Amersham). Then the samples were incubated for 3 h centered on local noon to determine photosynthetic rates in a water bath with running surface seawater to control temperature (27°C–30°C). After incubation, samples were filtered onto Whatman GF/F glass fiber filters (25 mm), and filters were placed into 20-mL scintillation vials, exposed to HCl fumes overnight, and dried (45°C). Scintillating cocktail (PerkinElmer) were added to the filters and the incorporated ¹⁴C counted using a liquid scintillation counter (LS 6500; Beckman Coulter; Holm-Hansen and Helbling, 1995).

P versus E curves, under PAR + UVR and PAR only, were obtained on August 6 and 8, 2005, under six light levels. The data for the curves were fitted according to the model of Eilers and Petters (1988) as:

where P is the production [µg C (µg Chl a)^–1 h^–1], E is the irradiance (µmol m^–2 s^–1), and a, b, and c are the adjustment parameters. Since the uncovered quartz containers received 4% higher PAR than those covered with the cutoff filters either under low or high levels of solar radiation and this higher portion of PAR might affect the comparison of irradiance-limiting photosynthetic rate with or without UVR, the PAR values were calibrated by multiplying by 0.96 for the P-E curve with Ultraphan 395 filter. The daily primary production (PP) was estimated over the period (July 1–September 30, 2005) according to the P-E curves and time- and depth-integrated models (Behrenfeld and Falkowski, 1997), assuming constant PAR attenuation coefficient K_d of 0.7 m^–1 (on August 4, 2006), vertical Chl a distribution (mean of 1.6 µg L^–1), and photosynthetic characteristics. The daily photosynthetic production was integrated per minute according to the irradiance values and the P-E curves, and this was then integrated per 10% of PAR every depth interval (at the depths <10% surface PAR, 7%, 4%, 2%, and 1% were employed). The daily photosynthetic production was subsequently integrated for the euphotic zone as follows:

where a, b, and c are the adjustment parameters in the P-E curve.

Measurements of Pigments

At the beginning of experiments, samples were taken to determine absorption of methanolic extract, Chl a concentration, and species composition. Two liters of seawater were filtered onto a Whatman GF/F glass fiber filter (47 mm), and then the filtrate was extracted with absolute methanol for 3 h at room temperature. The extract was subsequently determined for the optical density using a scanning spectrophotometer (UV 2501-PC; Shimadzu). Chl a concentration was calculated according to Porra (2002). To determine Chl a in the piconanoplankton fraction, a subsample was prefiltered through a Nitex mesh (20 µm) and the extraction of photosynthetic pigments was done as described above. The quantity and quality analysis of phytoplankton cells fixed with buffered formalin (final concentration of 0.4% in the sample) was carried out using an inverted microscope (Olympus IX51) after settling 10 mL of sample for 24 h (Villafañe and Reid, 1995).

Data Analysis

The Kruskal-Wallis nonparametric test was used to determine significant differences between the estimated parameters (confidence level = 0.05); the correlation between variables were established using a Kendall's test.

	ACKNOWLEDGMENTS

 
We thank John Raven and Mario Giordano for helpful comments on the data.

Received February 23, 2007; accepted March 23, 2007; published May 8, 2007.

	FOOTNOTES

 
¹ This work was supported by the National Natural Science Foundation of China (grant no. 90411018), the Natural Science Foundation of Guangdong Province, and Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina).

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Kunshan Gao (ksgao{at}stu.edu.cn).

www.plantphysiol.org/cgi/doi/10.1104/pp.107.098491

^* Corresponding author; e-mail ksgao{at}stu.edu.cn; fax 86–754–290–3977.

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