MAA Synthesis and Accumulation in Polar Macroalgae are Controlled by Abiotic Factors

Mycosporine‐like amino acids (MAAs) are regarded as powerful sunscreens protecting the algae against harmful UV radiation. The MAA protection efficiency was tested in algal samples by measuring the optimum quantum yield of photosynthesis using photosystem II fluorescence. It could be demonstrated that the recovery of photosynthesis after exposure to enhanced UV radiation is faster in individuals with high MAA content. MAAs can be synthesized in several polar macroalgae in response to different radiation conditions. Although MAA induction patterns are very species‐specific, some similarities can be found. Field studies indicate that plants from different growth habitats providing distinct radiation climate can be grouped into three physiological categories depending on their MAA content. The first group (I) includes mainly deep‐water species, typically lacking MAAs. The second group (II), algal species found in a broad range of water depths (eu‐ and sublittoral), which are able to flexibly synthesize and accumulate MAAs. The third group (III) includes supra‐ and eulittoral taxa, which always contain high MAA concentrations. In laboratory studies, we showed that taxa of group II and III responded in three different ways based on MAA accumulation when exposed to different radiation conditions (PAR, PAR + UVA, PAR + UVA + UVB). Either they: (a) exhibit highest total MAA concentration under the full artificial spectrum; (b) increase their MAA concentration after exposure to PAR and PAR + UVA or (c) MAA concentration declines after exposure to the full spectrum. Our studies have indicated that when coupled with UVR, exposure to temperature fluctuations ranging from 0 to 10 °C also affect MAA biosynthesis.     

Mycosporine-like amino acids in Antarctic sea ice algae,and their response to UVB radiation

Mycosporine like amino acids (MAAs) were detected in low concentration in sea ice algae growing in situ at Cape Evans, Antarctica. Four areas of sea ice were covered with plastics of different UV absorption exposing the bottom- ice algal community to a range of UV doses for a period of 15 days. Algae were exposed to visible radiation only; visible + UV radiation; and visible + enhanced UV radiation. MAA content per cell at the start of the experiment was low in snow-covered plots but higher in samples from ice with no snow cover. During the study period, the MAA content per cell reduced in all treatments, but the rate of this decline was less under both ambient UV and visible radiation than under snow covered plots. While low doses of UVB radiation may have stimulated some MAA production (or at least slowed its loss), relatively high doses of UVB radiation resulted in almost complete loss of MAAs from ice algal cells. Despite this reduction in MAA content per cell, the diatoms in all samples grew well, and there was no discernible effect on viability. This suggests that MAAs may play a minor role as photoprotectants in sea ice algae. The unique structure of the bottom ice algal community may provide a self-shading effect such that algal cells closest to the surface of the ice contain more MAAs than those below them and confer a degree of protection on the community as a whole.     

Occurrence and induction of a ultraviolet‐absorbing substance in the cyanobacterium Fischerella muscicola TISTR8215

The filamentous cyanobacterium Fischerella muscicola TISTR8215 was tested for the presence of ultraviolet (UV)‐absorbing mycosporine‐like amino acids (MAAs) and their induction by UV radiation. Reverse‐phase high performance liquid chromatographic coupled with photodiode‐array detection studies revealed the presence of a MAA having an absorption maximum at 332 nm and a retention time of around 16.1 min. Based on absorption maximum, the compound was designated as M‐332. This is the first report for the occurrence of a MAA and its inducibility as influenced by UV radiation in Fischerella strains studied so far. Photosynthetically active radiation (PAR) had no significant impact on MAA induction. PAR + UV‐A radiation significantly induced the synthesis of M‐332; however, PAR + UV‐A + UV‐B radiation conferred highest impact on MAA synthesis. The cultures exposed to alternate light and dark conditions showed the induction of M‐332 synthesis mostly during the light period in contrast to the decreased levels of M‐322 during the dark period suggesting a circadian induction of its synthesis. Overall results indicate that F. muscicola may protect itself from deleterious short wavelength UV radiation by synthesizing the photoprotective compounds particularly during summer time in its natural brightly‐lit habitats.     

Low temporal dynamics of mycosporine‐like amino acids in benthic cyanobacteria from an alpine lake

1. Cyanobacteria are one of the oldest organisms on Earth and they originated at a time when damaging ultraviolet (UV) C radiation still reached the surface. Their long evolution led to several adaptations to avoid deleterious effects caused by exposure to solar UV radiation. Synthesis of sunscreen substances, such as mycosporine‐like amino acids (MAAs), allows them to photosynthesise with reduced risk of cell damage. The interplay of solar UV radiation and MAAs is well documented for cyanobacteria in the plankton realm, but little is known for those in the benthic realm, particularly of clear alpine lakes.
2. Here, we assessed the temporal dynamics of MAAs in the benthic algal community of one clear alpine lake dominated by cyanobacteria during the ice‐free season and along a depth gradient using state‐of‐the‐art analytical methods (high‐performance liquid chromatography, nuclear magnetic resonance, liquid chromatography–mass spectrometry). We differentiated between the epilithic cyanobacterial community and the overlying loosely attached filamentous cyanobacteria, as we expected they will have an important shielding/shading effect on the former. We hypothesised that in contrast to the case of phytoplankton, benthic cyanobacteria will show less pronounced temporal changes in MAAs concentration in response to changes in solar UV exposure.
3. Three UV‐absorbing substances were present in both types of communities, whereby all were unknown. The chemical structure of the dominant unknown substance (maximum absorption at 334 nm) resulted in the identification of a novel MAA that we named aplysiapalythine‐D for its similarity to the previously described aplysiapalythine‐C.
4. Chlorophyll‐a‐specific MAA concentrations for epilithic and filamentous cyanobacteria showed a significant decrease with depth, although only traces were found in the former community. The temporal dynamics in MAA concentrations of filamentous cyanobacteria showed no significant variations during the ice‐free season.
5. Our result on the low temporal MAA dynamics agrees with the reduced growth rates of benthic cyanobacteria reported for cold ecosystems. The permanent presence of this community, which is adapted to the high UV levels characteristic of clear alpine lakes, probably represents the most important primary producers of these ecosystems.

     

Chemical profiling of mycosporine‐like amino acids in twenty‐three red algal species

Rhodophyta produce a variety of chemically different mycosporine‐like amino acids (MAAs), compounds that are known as some of the strongest ultraviolet (UV) absorbing molecules in nature. Accordingly, they primarily act as photoprotectants against harmful levels of solar ultraviolet radiation in the UV‐A and UV‐B range. In order to get a deeper understanding of the chemical diversity of MAAs in red algae, pure standards of eleven mycosporine‐like amino acids were isolated from three different species (Agarophyton chilense, Pyropia plicata and Champia novae‐zelandiae) using various chromatographic methods. Their structures were confirmed by nuclear magnetic resonance and mass spectrometry. Four out of the eleven MAAs are reported for the first time in algae. In addition, a new high‐performance liquid chromatography method was developed for the separation of all isolated MAAs and successfully applied for the analysis of twenty‐three red algal species of marine origin. All of them contained MAAs, the most abundant compounds were shinorine, palythine, asterina‐330 and porphyra‐334. For some samples, the direct assignment of MAAs based on their UV spectra was not possible; therefore, the target analytes were enriched by a simple concentration step, followed by liquid chromatography‐mass spectrometry analysis of the extracts. This approach enabled a deeper insight into the MAA pattern of red algae, indicating that not only the four dominant ones are synthesized but also many others, which were often described as unknown compounds in previous studies.     

Mycosporines: Detection Methodologies and Assessment

Mycosporine‐like amino acids (MAAs) are found in a variety of prokaryotic and eucaryotic algae, as well as higher plants, fungi, and animals. These compounds function as a photoprotective sunscreen to prevent ultra‐violet light damage. MAAs may thus be one of the competitive advantages that facilitated development of ozone (by oxytrophs), and thereby may be a competitive advantage for the proliferation of cyanobacteria and other harmful algal species. Numerous difficulties exist with assessment of MAAs, including identification of the compounds, conversion of isomers during HPLC preparation as a result of pH shifts, as well as the ecological implications of the presence, concentration, and forms of these compounds (see J Phycology 1999; 35, for relevant papers). This symposium will provide opportunities for intercalibration of laboratories involved in MAA analyses, suggestions regarding standardization of extraction protocols, as well as results from field‐ and laboratory‐based studies.     

Mycosporine-like amino acids from coral dinoflagellates

Coral reefs are one of the most important marine ecosystems, providing habitat for approximately a quarter of all marine organisms. Within the foundation of this ecosystem, reef-building corals form mutualistic symbioses with unicellular photosynthetic dinoflagellates of the genus Symbiodinium. Exposure to UV radiation (UVR) (280 to 400 nm) especially when combined with thermal stress has been recognized as an important abiotic factor leading to the loss of algal symbionts from coral tissue and/or a reduction in their pigment concentration and coral bleaching. UVR may damage biological macromolecules, increase the level of mutagenesis in cells, and destabilize the symbiosis between the coral host and their dinoflagellate symbionts. In nature, corals and other marine organisms are protected from harmful UVR through several important photoprotective mechanisms that include the synthesis of UV-absorbing compounds such as mycosporine-like amino acids (MAAs). MAAs are small (<400-Da), colorless, water-soluble compounds made of a cyclohexenone or cyclohexenimine chromophore that is bound to an amino acid residue or its imino alcohol. These secondary metabolites are natural biological sunscreens characterized by a maximum absorbance in the UVA and UVB ranges of 310 to 362 nm. In addition to their photoprotective role, MAAs act as antioxidants scavenging reactive oxygen species (ROS) and suppressing singlet oxygen-induced damage. It has been proposed that MAAs are synthesized during the first part of the shikimate pathway, and recently, it has been suggested that they are synthesized in the pentose phosphate pathway. The shikimate pathway is not found in animals, but in plants and microbes, it connects the metabolism of carbohydrates to the biosynthesis of aromatic compounds. However, both the complete enzymatic pathway of MAA synthesis and the extent of their regulation by environmental conditions are not known. This minireview discusses the current knowledge of MAA synthesis, illustrates the diversity of MAA functions, and opens new perspectives for future applications of MAAs in biotechnology.     

Multiple Strategies of Bloom-Forming Microcystis to Minimize Damage by Solar Ultraviolet Radiation in Surface Waters

The occurrence of bloom-forming cyanobacteria is one of the most obvious sign of eutrophication in freshwaters. Although in eutrophic lakes water transparency in the ultraviolet (UV) region is strongly reduced, bloom-forming cyanobacteria are exposed to high solar UV radiation at the surface. Here, we show that, in a natural phytoplankton community from a very eutrophic lake, Microcystis synthesizes UV sunscreen compounds identified as mycosporine-like amino acids (MAAs). The biomass-specific MAA concentration was significantly correlated with the occurrence of Microcystis but not with other algal groups, even though they were dominant in terms of biomass. Based on a photo-optical model, we estimated that the maximum MAA concentration per cell observed (2.5% dry weight) will confer only ~40% of internal screening to a single layer of Microcystis cells. Thus, the formation of a colony with several layers of cells is important to afford an efficient UV screening by internal self-shading. Overall, we propose that Microcystis uses a combination of photoprotective strategies (MAAs, carotenoids) to cope with high solar UV radiation at the water surface. These strategies include also the screening of UV radiation by d-galacturonic acid, one of the main chemical components of the slime layer in Microcystis.     

The influence of environmental features in the content of mycosporine‐like amino acids in red marine algae along the Brazilian coast

Mycosporine‐like amino acids (MAA) are ultraviolet screen substances synthesized by marine algae. The physiological function of these substances is related to cellular protection against UV radiation and as a protective mechanism against oxidative stress. These substances can be found mainly in the ocean, among red seaweeds. Its concentration in organisms has been related to ultraviolet radiation and availability of inorganic nitrogen in the environment. We start our study of MAA content in different species to understand if environmental conditions influence the concentration of MAAs in red seaweeds. The Brazilian coast presents abiotic factors that interact to create different physical‐chemical features in the environment. We collected 441 samples from 39 species of red seaweed easily found in the intertidal zone, in low tide, during the summer of 2015. The sampling encompassed a latitudinal gradient (3° S to 28°5′ S) at 23 points along the coast. We quantified and identified the content of MAAs in species through the method of high performance liquid chromatography. We detected for the first time the occurrence of MAAs in certain species of red algae that have not been reported to contain MAAs before. We confirmed that some environmental factors influenced the content of MAAs. Enhanced MAA contents, for example, were found in environments with a basic pH, a high ultraviolet index, and high concentrations of phosphate and nitrate. Salinity, dissolved oxygen and variations of sea surface temperature also influenced, in a secondary way, MAA content in algae in their natural environments.     

Photoprotective compounds in weakly and strongly pigmented copepods and co-occurring cladocerans

1. The prevalence of mycosporine‐like amino acids (MAAs) – a group of potential ultraviolet (UV)‐photoprotective compounds – was surveyed across 11 species of freshwater copepods from 20 lakes of varying ultraviolet radiation (UVR) transparency in North America, New Zealand and Argentina. Co‐occurring cladocerans were also analysed (seven species from 12 lakes). Many of the calanoid copepod populations were red with carotenoid pigmentation, allowing comparison of MAA and carotenoid accumulation as photoprotective strategies. 2. In two Pennsylvania (U.S.A.) lakes, MAA and carotenoid contents were followed during the early spring to mid‐summer period of lake warming. A pronounced seasonal pattern of higher carotenoid/low MAA content in spring, shifting to low carotenoid/higher MAA content in summer, was observed in calanoids from the more UV transparent lake. 3. All copepod samples contained MAAs. Visibly red calanoids, especially southern Hemisphere Boeckella, often had moderate to high concentrations (2.5–11 μg MAA mg^?1 dw), but low concentrations (0.04–1 μg MAA mg^?1 dw) in some N. American red calanoids show that high carotenoid pigmentation (e.g. 5–10 μg carotenoid mg^?1 dw) does not necessarily imply high MAA content. 4. No cladoceran sample had more than trace amounts of MAAs (<0.05 μg mg^?1 dw). Therefore, MAA accumulation does not seem to be a photoprotective strategy utilized by Daphnia (five species from nine lakes) or other cladocerans. 5. Seven identifiable MAAs were widely distributed among both calanoids and cyclopoids. Shinorine was ubiquitous and was usually the most abundant MAA in N. American samples. In contrast, porphyra‐334 was the predominant MAA in the southern Hemisphere Boeckella. 6. Copepods from higher UVR lakes tended to have a higher MAA content, but this relationship was statistically weak overall and taxon‐specific when found.     

Ultraviolet and osmotic stresses induce and regulate the synthesis of mycosporines in the cyanobacterium Chlorogloeopsis PCC 6912

The cyanobacterium Chlorogloeopsis PCC 6912 was found to synthesize and accumulate two putative UV sunscreen compounds of the mycosporine (mycosporine-like amino acid; MAA) type: mycosporine-glycine and shinorine. These MAAs were not constitutively present in the cells; their synthesis could be induced specifically either by exposure to UVB radiation (280–320 nm) or by osmotic stress, but not by other stress factors such as heat or cold shock, nutrient limitation, or photooxidative stress. A significant synergistic enhancement of MAA synthesis was observed when both stress factors were applied in combination. Although osmotic stress could induce MAA synthesis, comparison of the intracellular contents of MAAs with those of sugar osmolytes (glucose and trehalose) indicated that MAAs play no significant role in attaining osmotic homeostasis. UVB strongly enhanced the accumulation of shinorine, whereas osmotic stress had a more pronounced effect on mycosporine-glycine. This differential effect on the steady-state contents of each MAA could be explained either by differential regulation of biosynthesis or by differential loss rates of MAAs (leakage) under each condition. A preferential leakage of mycosporine-glycine from the cells after a hypoosmotic shock was detected. The results are interpreted in terms of an adaptive necessity for a combined regulatory control responding to both UV and external osmotic conditions in organisms that accumulate water-soluble sunscreens intracellularly. Received: 26 March 1999 / Accepted: 13 July 1999     

UV‐Acclimation of Cultured Phytoplankton Exposed to Natural and Enhanced UVB Radiation and Methodological Aspects of MAA Quantification

Bloom‐forming dinoflagellates often synthesize high concentrations of mycosporine‐like amino acids (MAAs) as a protection from high PAR and UV radiation, which may afford them a competitive advantage over other species. Photoprotection and long‐term acclimation to natural and enhanced UVB radiation were examined during 4 weeks in three dinoflagellates and one diatom. Semi‐continuous, nutrient‐replete cultures were maintained outdoors under natural light, with or without additional UVB (from lamps). The photosynthetic performance (XE‐PAM fluorometry) and the concentration and composition of MAAs and photoprotective carotenoids (PPCs; comprising xanthophylls) were followed weekly. A great variety of MAAs was found in the dinoflagellates (up to 10, identified by cochromatography and LC–MS). Large differences between sp. (and between two strains of the same sp.) were observed. In most cases, the composition and concentration of MAAs and PPCs increased under enhanced UVB. Growth rate and photosynthetic performance were sometime lower under enhanced UVB, while in other cases photoacclimation seemed to occur. The least affected sp. was Alexandrium tamarense who responded most rapidly to enhanced UVB. The algae also responded to changes in natural incident radiation. Some methodological aspects of MAA quantification were also investigated (with four species of dinoflagellates). Our results indicate how freezing (liquid‐N) likely breaks the cells, mobilizing the water‐soluble MAAs in the filter moist (otherwise highly packaged in fresh cells), while the organelles containing the pigments remain relatively intact. The implications of standard sample handling on the evaluation of MAA concentration in algae and on the estimation of the absorption of suspended material in water from in vivo spectroscopy (filter pad technique) will also be discussed.     

Antarctic krill (Euphausia superba) acquire a UV-absorbing mycosporine-like amino acid from dietary algae

We hypothesised that Antarctic krill acquire UV-absorbing mycosporine-like amino acids (MAAs) from dietary algae, which produce MAAs in response to ultraviolet (UV) irradiation. To test this hypothesis, we grew cultures of Phaeocystis antarctica that had been grown under either photosynthetically active radiation (PAR, 400-750 nm) plus UV irradiation (UVR, 280-400 nm), or else PAR-only. Algae grown under PAR-only produced high concentrations of porphyra-334, whereas additional UVR caused formation of high concentrations of mycosporine-glycine:valine and lower concentrations of porphyra-334. Krill were fed with either of these two cultures on eight occasions over 63 days. A third group was starved for the duration of the experiment. Animals were analysed after 36 and 63 days for MAA content. Remaining animals from all treatments were starved for a further 35 days and analysed to examine MAA retention characteristics. Our findings are that krill acquired different MAAs from dietary algae depending on the light conditions under which the algae were grown. Specifically, krill fed algae grown under PAR-only had higher concentrations of porphyra-334 than starved krill. Conversely, krill fed algae grown under PAR with additional UVR had high body concentrations of mycosporine-glycine:valine. MAA concentrations in starved krill remained static throughout the experiment. However, long term starvation (35 days) caused levels of certain acquired MAAs to decline. From this we can infer that MAA concentrations in krill are dependent on the MAA content of phytoplankton, and therefore the algae's response to UV exposure. This has implications for transfer of MAAs through marine trophic webs.     

MYCOSPORINE‐LIKE AMINO ACIDS AND PHYLOGENIES IN GREEN ALGAE: PRASIOLA AND ITS RELATIVES FROM THE TREBOUXIOPHYCEAE (CHLOROPHYTA)1

A UV‐absorbing mycosporine‐like amino acid (324 nm‐MAA), so far only known from the green macroalgal genus Prasiola (Trebouxiophyceae), was also identified in other morphologically diverse green algae closely related to Prasiola spp. in 18S rDNA phylogenies. Using HPLC, a second UV‐absorbing compound was found only in Myrmecia incisa Reisigal among all studied strains. This substance showed an absorption maximum at 322 nm and hence was designated as putative 322 nm‐MAA. Preliminary UV‐exposure experiments indicated that all species containing one or the other MAA showed a strong accumulation of the respective compound, thus supporting their function as putative UV sunscreen. Both UV‐absorbing substances were only identified in the studied members of the Trebouxiophyceae but were absent in members of the Ulvophyceae and Chlorophyceae. When mapped on an 18S rDNA phylogeny, the distribution of 324 nm‐MAA was found to be scattered within the Trebouxiophyceae but was consistent with a distribution that follows phylogenetic patterns rather than ecological adaptations. The 324 nm‐MAA was also detected in two phylogenetically related species from freshwater as well as from subaerial habitats, Watanabea reniformis Hanagata et al. and isolate UR7/5, which were phylogenetically independent of Prasiola and its closer allies. MAAs were absent in another Trebouxiophyceae clade comprising lichen photobionts (Coccomyxa pringsheimii Jaag) as well as freshwater picoplanktonic algae (Choricystis minor (Skuja) Fott). The data presented suggest a chemotaxonomic value of the 324 nm‐MAA in green algal taxonomy. To address the paraphyly of the genus Myrmecia Printz as presently circumscribed, we propose the new combination Lobosphaera incisa.     

Effects of salinity and ultraviolet radiation on the concentration of mycosporine-like amino acids in various isolates of the benthic cyanobacterium Microcoleus chthonoplastes

The effects of salinity and ultraviolet B (UV‐B) treatment on the intracellular mycosporine‐like amino acid (MAA) concentration in three isolates of the benthic cyanobacterium Microcoleus chthonoplastes from the Baltic Sea (WIS), Spain (EBD) and Australia (TOW) were compared. All strains contained shinorine and, in addition, both EBD and TOW exhibited the unknown MAA‐332, and WIS exhibited the unknown MAA‐346. Salinity treatment led to MAA accumulation in TOW and WIS, but not in EBD. Whereas UV‐B exposure was accompanied by a strong increase in MAA in EBD and TOW, WIS did not survive the treatment. All data indicate isolate‐specific MAA accumulation patterns under different environmental conditions and can be explained by ecotypic differentiation. A double function of MAAs as organic osmolytes and photoprotect‐ants seems possible.     

The relative contributions of diet and associated microbiota to the accumulation of UV‐absorbing mycosporine‐like amino acids in the freshwater copepod Boeckella antiqua

1. Mycosporine‐like amino acids (MAAs) are ubiquitous compounds in aquatic organisms that are usually considered sunscreens that protect them from harmful ultraviolet radiation. Given that virtually all animals lack the metabolic pathways to synthesise MAAs de novo, they must acquire them either from their diet or from microorganisms living in close association. In freshwater copepods, accumulation of MAAs is stimulated by exposure to ultraviolet and/or visible radiation. 2. A 2 × 2 factorial experiment was performed to assess the contributions of dietary and microbial sources of MAAs in the freshwater copepod Boeckella antiqua. The treatments consisted of two different diets: an MAA‐free diet, including only Chlamydomonas reinhardtii, and an MAA‐rich diet, including both C. reinhardtii and Peridinium inconspicuum, crossed with two antibiotic treatments, with and without chloramphenicol. Treatment with chloramphenicol was intended to inhibit the development of bacteria associated with the copepods. 3. MAA concentration in B. antiqua was affected by the experimental conditions: (i) exposure to artificial PAR + UVR stimulated the accumulation of several MAAs (up to 62% increase in total MAA concentration with respect to the initial concentration); (ii) the presence of chloramphenicol in the culture media reduced the MAA concentration in copepods fed an MAA‐free diet; (iii) in the absence of chloramphenicol, copepods fed the MAA‐rich diet had significantly higher total MAA concentration than those fed the MAA‐deficient diet; but (iv) dietary supplementation with an MAA‐rich algae in the presence of chloramphenicol failed to significantly increase total MAA concentration. 4. Analysis of profiles from denaturing gradient gel electrophoresis (DGGE) showed that the prokaryotic community associated with the copepods was affected by chloramphenicol. Dendograms constructed from digitalised DGGE images consistently grouped the antibiotics treatments separately from the initial samples and the treatments without antibiotics. Two band positions were exclusive to treatments without antibiotics. 5. We conclude that when offered an MAA‐rich diet, B. antiqua may accumulate a proportion of MAAs from diet. However, we suspect that in the absence of an MAA‐rich dietary source (as in its natural habitat), virtually all MAAs present in B. antiqua are produced by copepod‐associated prokaryotes.     

BLUE LIGHT AND UV-A RADIATION CONTROL THE SYNTHESIS OF MYCOSPORINE-LIKE AMINO ACIDS IN CHONDRUS CRISPUS (FLORIDEOPHYCEAE)

The induction of UV-absorbing compounds known as mycosporine-like amino acids (MAAs) by red, green, blue, and white light (43% ambient radiation greater than 390 nm) was examined in sublittoral Chondrus crispus Stackh. Fresh collections or long-term cultures of sublittoral thalli, collected from Helgoland, North Sea, Germany, and containing no measurable amounts of MAAs, were exposed to filtered natural radiation for up to 40 days. The MAA palythine (λ_max 320 nm) was synthesized in thalli in blue light to the same extent observed in control samples in white light. In contrast, thalli in green or red light contained only trace amounts of MAAs. After the growth and synthesis period, the photosynthetic performance of thalli in each treatment, measured as pulse amplitude modulated chlorophyll fluorescence, was assessed after a defined UV dose in the laboratory. Thalli with MAAs were more resistant to UV than those without, and exposure to UV-A+B was more damaging than UV-A in that optimal (F_v/F_m) and effective (φ_II) quantum yields were lower and a greater proportion of the primary electron acceptor of PSII, Q, became reduced at saturating irradiance. However, blue light-grown thalli were generally more sensitive than white light control samples to UV-A despite having similar amounts of MAAs. The most sensitive thalli were those grown in red light, which had significantly greater reductions in F_v/F_m and φ_II and greater Q reduction. Growth under UV radiation alone had been shown previously to lead to the synthesis of the MAA shinorine (λ_max 334 nm) rather than palythine. In further experiments, we found that preexposure to blue light followed by growth in natural UV-A led to a 7-fold increase in the synthesis of shinorine, compared with growth in UV-A or UV-A+B without blue light pretreatment. We hypothesize that there are two photoreceptors for MAA synthesis in C. crispus, one for blue light and one for UV-A, which can act synergistically. This system would predispose C. crispus to efficiently synthesize UV protective compounds when radiation levels are rising, for example, on a seasonal basis. However, because the UV-B increase associated with artificial ozone reduction will not be accompanied by an increase in blue light, this triggering mechanism will have little additional adaptive value in the face of global change unless a global UV-B increase positively affects water column clarity.     

Distribution of Mycosporine-Like Amino Acids Along a Surface Water Meridional Transect of the Atlantic

The composition and abundance of mycosporine-like amino acids (MAAs) were investigated in the surface waters along a 13,000-km meridional transect (52° N to 45° S) in the Atlantic Ocean (Atlantic Meridional Transect programme: Cruise AMT 18: 4/10/2008-10/11/2008). MAAs were ubiquitous along the transect, although the composition of the MAAs was variable. Highest concentrations were in the far south (below 40° S; MAA >1 μg L(-1)) and in north subtropical equatorial region (NER: 0-25° N; MAA up to 0.8 μg L(-1)). Highest MAA relative to chlorophyll-a occurred in the NER (MAA/chl-a ratio between 2 and 5). MAA/chl-a significantly correlated with the preceding month's mean daily UV dose and with UV-B/UV-A. In the far south, high MAA concentrations coincided with high phytoplankton biomass, high nutrients and a deep mixed layer associated with the austral spring. Here, the phytoplankton community was dominated by micro- and nano-eukaryotes. At the NER, the high MAA/chl-a coincided with low nutrient concentrations, a shallow mixed layer depth (20-70 m) and to a lesser extent to a shallow nitracline (40-90 m). Here, the phytoplankton consisted primarily of picophytoplankton (0-0.2 μm), dominated by the pico-cyanobacteria Synechococcus sp. and Prochlorococcus sp. and by the nitrogen fixing filamentous cyanobacterium Trichodesmium. The low nitrate concentrations (<0.1 μmol L(-1)) at the NER suggest that nitrogen fixation was required for MAA production. Specific MAAs could not easily be assigned to particular groups of phytoplankton and we could not rule out the possibility that MAAs were associated with symbiotic cyanobacteria contained within heterotrophic dinoflagellates or diatoms.