1State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361005, China 2Key Lab of Marine Biotechnology of Jiangsu Province, Huaihai Institute of Technology, Lianyungang, 222005, China
Solar visible radiation (400-700 nm, photosynthetically active radiation, PAR) drives photosynthesis and, therefore, is indispensable for all forms of life. In aquatic ecosystems, photosynthetic carbon fixation contributes to nearly 50% of the global primary production (Behrenfeld et al., 2006). Within the euphotic zone (down to 1% of surface PAR), cells receive not only PAR but also ultraviolet radiation (UVR, 280-400 nm), which can penetrate to considerable depths (Har-greaves, 2003). UVR is usually considered harmful at either organism or community levels (Häder et al., 2007). However, UV-A can be utilized for photosynthetic carbon fixation by phytoplankton, playing negative (at high levels) and positive roles like a double-edged sword (Gao et al., 2007).
Solar UVR can reduce photosynthetic rate (Helbling et al., 2003), damage cellular components such as D1/D2 protein (Sass et al., 1997) and DNA molecule (Buma et al., 2003), alter the rate of nutrient uptake (Fauchot et al., 2000), and affect growth (Villafane et al., 2003) and fatty acids composition (Goes et al., 1994) of algae. Recently, it has been found that natural levels of UVR can even alter the morphology of the cyanobacterium Arthrospira (Spirulina) platensis (Wu et al., 2005; Gao and Ma, 2008). On the other hand, positive effects of UV-A (315-400 nm) have also been reported. UV-A enhances carbon fixation under reduced (Barbieri et al., 2002) or fast-fluctuating (Helbling et al., 2003) solar radiation and allows photorepair of UV-B-induced DNA damage (Buma et al., 2003); it can even drive photosynthetic carbon fixation in the absence of PAR (Gao et al., 2007). However, to date, 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) (van Donk et al., 2001) without UVR being considered (Hein and Sand-Jensen, 1997; Schippers et al., 2004; Zou and Gao, 2002). Seaweeds, as the major group of primary producers in coastal waters, experience dramatic changes of solar radiation during a day or through their different life stages. It is of general concern to know how macroalgal species respond to fluctuation or changes of the solar radiation from a physiological or photobio-logical point of view. In addition, UV-B (280-315 nm) irradiance at the surface of the earth has been raised due to the reduction of stratospheric ozone layer associated with the CFC pollutants (Kerr and McElroy, 1993; Aucamp, 2007). Therefore, impacts of solar UVR as well as enhanced levels of UV-B on macroalgae have also been widely investigated.
2. Physiological Responses to short- and Long-Term Exposures
Growth is an important parameter that incorporates stress effects in biochemical and physiological processes within the cell. Growth measurements are useful in estimating possible change in productivity due to enhanced UV-B irradiance associated with ozone depletion. UVR is generally known to inhibit macroalgal growth (Dring et al., 1996; Altamirano et al., 2000; Henry and Van Alstyne, 2004; Han and Han, 2005; Davison et al., 2007). Enhanced levels of UV-B can further inhibit macroalgal growth as found in the brown algae Ectocarpus rhodochondroi-des (Santas et al., 1998) and Dictyota dichotoma (Kuhlenkamp et al., 2001). Michler et al. (2002) reported that most of the investigated 13 macroalgal species showed reduced growth rates in the presence of UVR. On the other hand, UVR resulted in a higher growth rate in Gracilaria lemaneiformis under reduced levels (25%) of solar radiation (Xu, J and Gao, K, unpublished data). UVR was found to result insignificant impact on the growth of Ulva lactuca during winter period (Xu and Gao, 2007), whereas growth of Ulva expansa was largely inhibited by UV-B during the summer period (Grobe and Murphy, 1998). It is possible that UVR-related impacts on macroalgal growth depend on seasonal environmental changes, such as temperature, which is much lower during winter season. UVR-induced inhibition of photosynthetic O2 evolution in a Gracilaria plant increased with increased seawater temperature (Gao and Xu, 2008).
UVR affects macroalgal growth to different degrees. UV-B radiation, though with the strength of less than 1% of the total solar radiation, can significantly reduce the growth rates of most of the species investigated so far (Grobe and Murphy, 1994; Pang et al., 2001; Michler et al., 2002; Jiang et al., 2007; Gao and Xu, 2008). In contrast to the impacts of UVR in short-term experiments, hardly any lasting difference was found in growth between samples exposed to solar radiations with or screened off UV-B in long-term experiments in Ulva rigida (Altamirano et al., 2000) and Fucus serratus (Michler et al., 2002). Nevertheless, UVR was found to affect the growth in long-term and field experiments in Laminaria spp. (Michler et al., 2002; Roleda et al., 2006a) and Gracilaria lemaneiformis (Gao and Xu, 2008). In the green alga, Codium fragile, no change in the biomass was observed during the first week; however, when exposed to UVR, it increased by about 70% in the following 16 days (Michler et al., 2002). In another green alga, Ulva lactuca, presence of UV-B only caused inhibition of photochemical yield in the initial 2 days, whereas UV-A showed insignificant effect; solar PAR resulted in most of the inhibition during noon time (Xu and Gao, 2007). UV-A was shown to reduce the photosynthetic rate at higher irradi-ance levels around noontime, but enhanced it during sunrise at low irradiance levels in Gracilaria lemaneiformis (Gao and Xu, 2008). Photosynthesis in macroalgae is known to be negatively affected by UV-B as well as UV-A (Cordi et al., 1997; Aguilera et al., 1999b; Han et al., 2003). However, short-term experiments about the responses to UVR do not usually provide enough information to relate to the long-term effects. For example, Laminaria ochroleuca showed partial acclimation to chronic UVR exposure in photosynthesis, but did not in growth (Roleda et al., 2004). On the other hand, solar UV-B radiation could play a role in the recovery process of the inhibited photosynthesis in a brown alga Dictyota dichotoma (Flores-Moya et al., 1999), and UV-A (315-400 nm) radiation could aid in DNA repair (Pakker et al., 2000a,b) and enhance growth (Henry and Van Alstyne, 2004) in macroalgae.
Species of macroalgae are distributed to different depths in the intertidal zone and exposed to different levels of PAR and UVR because of the attenuation of seawater. Their vertical distribution is closely related to their sensitivity to UV-B (Hanelt et al., 1997; Bischof et al., 1998) as well as to their recovery capacity after being damaged by UVR (Gomez and Figueroa, 1998). Upper species are more resistant to solar UVR. UV-B had little effect on eulittoral species but significantly inhibited the growth of sublittoral red macrophytes (van de Poll et al., 2001).
3. UV-Regulated Photosynthetic Performance Under the sun
Solar UV radiation is a permanently existing environmental factor that macroalgae are usually exposed to. However, photosynthetic performance under the sun has been mainly investigated in the absence of UVR owing to the ignorance of the transmitting characteristics of vessels used (glass, polyethylene, and polycarbonate materials do not allow UV-B and part of UV-A to penetrate, Van Donk et al., 2001).
In the studies without considering the effects of UVR, diurnal photosynthesis of macroalgae was depressed in the afternoon on sunny days in Macrocystis pyrifera surface canopy (Gerard, 1986), Sargassum spp. (Gao and Umezaki, 1989; Gao, 1990), Ulva curvata, Codium decorticatum, Dictyota dichotoma, Petalonia fascia, and Gracilaria foliifera (Ramus and Rosenberg, 1980). The photosynthetic efficiency of O2 evolution was found to be higher in the morning than in the afternoon in Ulva rotundata (Henley et al., 1991) and Sargassum horneri (Gao, 1990) under solar PAR. Such an afternoon photosynthetic depression was not found on rainy or highly cloudy days (Gao and Umezaki, 1989) and may be largely removed by superimposing a light fluctuation on the diurnal regime as demonstrated in phytoplanktons (Marra, 1978). Contrarily, the red alga Gelidiella acerosa was found to photosynthesize inefficiently in the morning compared with that of midday and afternoon (Ganzon-Fortes, 1997). Owing to light-transmission characteristics of the incubation vessels used, these previous findings demonstrated the asymmetrical diurnal photosynthesis under PAR only, without UV-B or UVR being considered. Although both UV-A and UV-B might cause less damages than PAR under natural solar radiation (Dring et al., 2001), the highest photoinhibition was found at noon in macroalgae under full spectrum of solar radiation (Huppertz et al., 1990; Hanelt, 1992). However, the effects caused by UVR have only infrequently been differentiated from that of PAR (Hanelt et al., 1997; Flores-Moya et al., 1999).
Recently, it has been found that involvement of UV-B depressed the apparent photosynthetic efficiency on sunny days, whereas UV-A enhanced the apparent photosynthetic efficiency during sunrise period in Gracilaria lema-neiformis (Gao and Xu, 2008). Daytime photosynthetic performance usually depends on the extent and pattern of fluctuating solar irradiance, especially that of UV-A, which can refurbish damaged photosynthetic apparatus and ameliorate the afternoon Pmax depression in view of the balance between damage and repair. High levels of UV-A radiation at midday caused photosynthetic inhibition of some macroalgae (Hader et al., 2001), but low levels of UV-A radiation have been found to enhance the growth of the brown alga Fucus gardneri embryos (Henry and Van Alstyne, 2004) as well as photosynthetic CO2 fixation by phytoplanktons (Gao et al., 2007). Recently, absorption of UV-A energy has been found to be transferred to Chl. a in a diatom (Orellana et al., 2004) and Porphyra spp. (Zheng, Y and Gao, K, unpublished data). It has been recently proved that both Gracilaria and Porphyra plants can utilize UV-A for photosynthesis (Xu, J and Gao, K, unpublished data). The double-edged (positive at low and negative at high levels) effects of UV-A could magnify the discrepancy between the estimations of photosyn-thetic production and growth according to weather conditions.
Different life stages of macroalgae showed different sensitivity to irradiation stress (Dring et al., 1996; Hanelt et al., 1997; Altamirano et al., 2003; Roleda et al., 2004; Véliz et al., 2006). Most studies conducted to evaluate the impact of UV-B on seaweeds used macro-thallus stages; however, early developmental life stages of intertidal algae seemed to be more sensitive to UVR than adult stages (Major and Davison, 1998; Coelho et al., 2000; Hoffman et al., 2003; Véliz et al., 2006). Studies to establish the sensitivity of early developmental stages are critical, since the survival and growth of these stages will determine the recruitment of a species and thus productivity.
Different life stages of Porphyra plants have been found to exhibit different photosynthetic characteristics.
Light utilization efficiency in thallus was much higher than that in conchocelis stage of P. yezoensis (Zhang et al., 1997), and maximal net photosynthetic rate of the conchocelis was lower than that of the thalli (Tanaka, 1985; Gao and Aruga, 1987). Electron transfer inhibitor DCMU blocked the energy transfer from PS II to PS I in the thalli, but not in the conchocelis of P. yezoensis (Pan et al., 2001). UVR was found to degrade photosynthetic pigments in both P leucosticta (Figueroa et al., 1997) and P umbilicalis (Aguilera et al., 1999a) and to reduce the effective quantum yield of P leucosticta (Figueroa et al., 1997), but it resulted in insignificant photoinhibition in P umbilicalis (Gröniger et al., 1999). These studies have focused on the thallus stage of Porphyra spp. In nature, Porphyra-conchocelis lives in shells, which are often found in shallow coastal waters (Jao, 1936) and must be exposed to certain extent of UVR. The conchocelis stage of Porphyra haitanensis contained much less UV-screening compounds and its PSII activity was more damaged even under reduced levels of solar radiation compared with the thallus stage (Jiang and Gao, 2008).
UVR is known to affect early development (Huovinen et al., 2000; Henry and Van Alstyne, 2004; Roleda et al., 2005, 2007; Wiencke et al., 2006, 2007) and spore germination (Wiencke et al., 2000; Altamirano et al., 2003; Han et al., 2004; Steinhoff et al., 2008) of macroalgae. It can effectively delay photosynthetic recovery in arctic kelp zoospores following photo-exposures (Roleda et al., 2006b). UV-B rather than UV-A negatively affected the germination of the zygotes of Fucus serratus (Altamirano et al., 2003) and the zoospores of Laminaria hyperborean (Steinhoff et al., 2008). Different life stages of some macroalgal species showed different degrees of enduring UVR, with increased tolerance as individuals differentiate. UV-A was found to play an important role in the morphogenesis of sporelings in Porphyra haitanensis, enhancing transverse cell division from conchospores (Jiang et al., 2007). Morphological differences among life stages can affect the energy transfer of PAR and UVR in the tissue, resulting in different responses to UVR in Laminaria spp. (Dring et al., 1996; Roleda et al., 2006c) as well as Porphyra haitanensis (Jiang and Gao, 2008). Longer path-length for the absorbed UVR energy in tissues can reduce its damaging effects.
5. Accumulation of UV-Absorbing compounds as a strategy Against UVR
Adaptation to UVR has equipped macroalgae with defensive mechanisms to minimize UV-induced damages. Macroalgae can protect themselves via avoidance, repair, and screening mechanisms (Karentz, 1994; Franklin and Foster, 1997; Kar-entz, 2001). In addition to photoreactivation and nucleotide excision repair of UV-induced DNA damage (Buma et al., 1995; Pakker et al., 2000a; Lud et al., 2001), an important mechanism to reduce the damaging impact of UVR in marine mac-roalgae is the synthesis and accumulation of UV-absorbing compounds (UVAC) (Karsten et al., 1998). These compounds, such as mycosporine-like amino acids (MAAs) (Karentz et al., 1991; Dunlap and Shick, 1998), scytonemin (Garcia-Pichel and Castenholz, 1991; Dillon et al., 2002), and phlorotannins (Pavia et al., 1997; Pavia and Brock, 2000), have been found in many photosynthetic organisms.
They increased in cellular content with increased UV exposure (Brenowitz and Castenholz, 1997; Pavia et al., 1997; Han and Han, 2005; Zheng and Gao, 2009) to reduce UV-related photoinhibition and damage, playing a protective role against solar UVR (Oren and Gunde-Cimerman, 2007).
Seaweeds often exhibit high levels of UVAC, such as MAAs in the red alga Porphyra columbina (Korbee-Peinado et al., 2004), an unknown UV-B absorbing substance in the green alga Ulva pertusa (Han and Han, 2005), and phlorotannin in the brown algae Ascophyllum nodosum and Fucus gardneri (Pavia et al., 1997; Henry and Van Alstyne, 2004). Higher levels of UVAC have been found in the red alga Gracilaria lemaneiformis under full spectrum of solar radiation than UVR-free treatments, reflecting a responsive induction (Gao and Xu, 2008). Synthesis of UVAC has been found to be induced by UV-B in Chondrus crispus (Karsten et al., 1998), Porphyra columbina (Korbee-Peinado et al., 2004), and Ulvapertusa (Han and Han, 2005). Such stimulation is dependent on both dose and wavelength, with higher accumulation of UVAC under high daily doses (Karsten et al., 1998; Franklin et al., 2001). UVR was suggested to trigger some photoreceptors (active wavelengths between 280 and 320 nm) in the algae to sense the need for UVAC synthesis (Han and Han, 2005; Oren and Gunde-Cimerman, 2007). Accumulation of UVAC is often associated with decreased Chl a, resulting in an increased ratio of UVAC to Chl a (Gao and Xu, 2008).
MAAs, the most common UV-screening compounds, are water-soluble substances with absorption maxima ranging from 310 to 360 nm (Nakamura et al., 1982). Although their UVR-protective function is not yet completely clear, the most acceptable interpretation is that they play a role as a screen against UVR (Conde et al., 2000; Karsten et al., 2005). Some of these compounds may also function as antioxidants (Dunlap and Yamamoto, 1995; Suh et al., 2003), osmosis-regulating substances (Oren, 1997), antenna pigments channeling the energy to the photosynthetic apparatus (Sivalingam et al., 1976; Gao et al., 2007), or an intracellular nitrogen storage (Korbee-Peinado et al., 2004; Korbee et al., 2006). Accumulation of MAAs could be induced by different radiation treatments (Karsten et al., 1999; Korbee-Peinado et al., 2004; Karsten et al., 2005) or affected by osmotic stress (Oren, 1997; Klisch et al., 2002) and nutrient availability (Korbee-Peinado et al., 2004; Korbee et al., 2005; Zheng and Gao, 2009). The accumulation of MAAs was found to be dependent on both dose and wavelength of incident solar radiation, with higher accumulation of MAAs associated with high daily doses in Chondrus crispus (Karsten et al., 1998; Franklin et al., 2001). Nutrient availability was also found to affect the accumulation of MAAs (Karsten and Wiencke, 1999; Korbee-Peinado et al., 2004); enrichment of nitrate enhanced the content of MAAs in Gracilaria tenuistipitata (Zheng and Gao, 2009). Porphyra plants contain high levels of MAAs (up to 1% of the dry weight), mainly porphyra-334, which accumulates to the highest concentrations among the species of red algae studied so far (Gröniger et al., 1999; Hoyer et al., 2001). However, some studies showed that contents of MAAs did not increase in response to UVR or PAR and could not completely protect Porphyra umbilicalis and Gracilaria cornea against UVR (Gröniger et al., 1999; Sinha et al., 2000).
Distribution of seaweed at different zonational depths affects the accumulation of MAAs. Intertidal species are usually more resistant to UV stress (i.e., inhibition of photosynthesis) than subtidal species that have less or no MAAs (Maegawa et al., 1993). It was found that deep-water polar macroalgal species did not have MAAs, whereas supra- and eulittoral species contained MAAs to high concentrations (Hoyer et al., 2002). Total MAAs content in Mastocarpus stellatus was sixfold higher than in Chondrus crispus that was generally found at a greater depth; quantum yield and maximal electron transport rate were more reduced in C. crispus than M. stellatus by UV-B radiation (Bischof et al., 2000). MAAs content in Devaleraea ramentacea increased with decreased depth, being correlated with a higher photosynthetic capacity under UVR treatment (Karsten et al., 1999). The macroalgal zonation patterns relate to their ability to resist high radiation stress (Hanelt, 1998).
Macroalgal species distributed at the upper part of intertidal zone may be exposed to much higher solar radiation during emersion if the low tide coincides with local noon. Recently, it was shown that desiccation or dehydration of Porphyra haitanensis thalli led to higher absorptivity of the UVAC (Jiang et al., 2008). The ability for Porphyra haitanensis thalli to increase its cellular content of UVAC during such emersion period allows them to cope with UVR stress. The possible strategy for macroalgal species to survive at the upper levels of intertidal zone is to increase its content of UVAC, which play roles in both sunscreening and osmosis regulation.
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