Responses of aquatic algae and cyanobacteria to solar UV-B

Continuous depletion of the stratospheric ozone layer has resulted in an increase in solar ultraviolet-B (UV-B; 280–315 nm) radiation reaching the Earth's surface. The consequences for aquatic phototrophic organisms of this small change in the solar spectrum are currently uncertain. UV radiation has been shown to adversely affect a number of photochemical and photobiological processes in a wide variety of aquatic organisms, such as cyanobacteria, phytoplankton and macroalgae. However, a number of photosynthetic organisms counteract the damaging effects of UV-B by synthesizing UV protective compounds such as mycosporine-like amino acids (MAAs) and the cyanobacterial sheath pigment, scytonemin. The aim of this contribution is to discuss the responses of algae and cyanobacteria to solar UV-B radiation and the role of photoprotective compounds in mitigating UV-B damage.     

Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites?

Mycosporines and mycosporine-like amino acids (MAAs) are low-molecular-weight water-soluble molecules absorbing UV radiation in the wavelength range 310-365 nm. They are accumulated by a wide range of microorganisms, prokaryotic (cyanobacteria) as well as eukaryotic (microalgae, yeasts, and fungi), and a variety of marine macroalgae, corals, and other marine life forms. The role that MAAs play as sunscreen compounds to protect against damage by harmful levels of UV radiation is well established. However, evidence is accumulating that MAAs may have additional functions: they may serve as antioxidant molecules scavenging toxic oxygen radicals, they can be accumulated as compatible solutes following salt stress, their formation is induced by desiccation or by thermal stress in certain organisms, they have been suggested to function as an accessory light-harvesting pigment in photosynthesis or as an intracellular nitrogen reservoir, and they are involved in fungal reproduction. Here, the evidence for these additional roles of MAAs as 'multipurpose' secondary metabolites is reviewed, with special emphasis on their functions in the microbial world.     

ULTRAVIOLET SUNSCREENS IN GYMNODINIUM SANGUINEUM (DINOPHYCEAE): MYCOSPORINE-LIKE AMINO ACIDS PROTECT AGAINST INHIBITION OF PHOTOSYNTHESIS

Marine phytoplankton are sensitive to inhibition of photosynthesis by solar ultraviolet (UV) radiation, although sensitivity varies, depending on the growth environment. A mechanism suggested to increase resistance to UV inhibition is the accumulation of UV-absorbing compounds, such as the mycosporine-like amino acids (MAAs) found in many marine organisms. However, the effectiveness of these compounds as direct optical screens in microorganisms has remained unclear. The red-tide dinoflagellate Gymnodinium sanguineum Hirasaka accumulates about 14-fold more MAAs (per unit of chlorophyll) in high (76 W·m⁻²) than in low (15 W·m⁻²) growth irradiance. Biological weighting functions were estimated for UV inhibition of photosynthesis and showed that the high-light-grown cultures have lower sensitivity to UV radiation at wavelengths strongly absorbed by the MAAs. The time course of photosynthesis during exposure to UV radiation was measured using pulsed amplitude modulated (PAM) fluorometry and displayed a steady-state level after 15 min of exposure, indicating active repair of damage to the photosynthetic apparatus. Repair was blocked in the presence of the antibiotic streptomycin, yet high-light G. sanguineum remained less sensitive to UV radiation than did low-light cultures. These experiments show that MAAs act as spectrally specific UV sunscreens in phytoplankton.     

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.     

Sources of mycosporine-like amino acids in planktonic Chlorella-bearing ciliates (Ciliophora)

1. Mycosporine‐like amino acids (MAAs) are a family of secondary metabolites known to protect organisms exposed to solar UV radiation. We tested their distribution among several planktonic ciliates bearing Chlorella isolated from an oligo‐mesotrophic lake in Tyrol, Austria. In order to test the origin of these compounds, the MAAs were assessed by high performance liquid chromatography in both the ciliates and their symbiotic algae. 2. Considering all Chlorella‐bearing ciliates, we found: (i) seven different MAAs (mycosporine‐glycine, palythine, asterina‐330, shinorine, porphyra‐334, usujirene, palythene); (ii) one to several MAAs per species and (iii) qualitative and quantitative seasonal changes in the MAAs (e.g. in Pelagodileptus trachelioides). In all species tested, concentrations of MAAs were always <1% of ciliate dry weight. 3. Several MAAs were also identified in the Chlorella isolated from the ciliates, thus providing initial evidence for their symbiotic origin. In Uroleptus sp., however, we found evidence for a dietary source of MAAs. 4. Our results suggest that accumulation of MAAs in Chlorella‐bearing ciliates represents an additional benefit of this symbiosis and an adaptation for survival in sunlit, UV‐exposed waters.     

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.     

Are Freshwater Mixotrophic Ciliates Less Sensitive to Solar Ultraviolet Radiation than Heterotrophic Ones?1

We tested whether mixotrophic ciliates are more resistant to solar ultraviolet radiation (UVR) than heterotrophic ones because symbiotic algae can provide self-shading by cell matter absorption and eventually by direct UV screening from mycosporine-like amino acids (MAAs). Sensitivity of a natural assemblage to solar radiation was tested in experiments in the original lake and in a more UV transparent alpine lake after transplantation of the ciliates. In both lakes, the assemblage was exposed either to full sunlight, to photosynthetically active radiation only, or kept in the dark. In each lake, exposure was for 5 h at the surface and at the depth corresponding to the 10% attenuation depth at 320 nm. Overall, when the assemblage was exposed to surface UVR, only one out of four dominant mixotrophic ciliates, Vorticella chlorellata, was more resistant than heterotrophic species. The higher UV resistance in V. chlorellata was related to the presence of MAAs and the high percentage of ciliate volume occupied by algal symbionts. Our results indicate that effects of UVR were species-specific and depended on efficient screening of these wavelengths, but also on the depth preference of the ciliates and thus, on their previous exposure history to UVR.     

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 from marine organisms

The substantial loss in the stratospheric ozone layer and consequent increase in solar ultraviolet radiation on the earth’s surface have augmented the interest in searching for natural photoprotective compounds in organisms of marine as well as freshwater ecosystems. A number of photoprotective compounds such as mycosporine-like amino acids (MAAs), scytonemin, carotenoids and several other UV-absorbing substances of unknown chemical structure have been identified from different organisms. MAAs form the most common class of UV-absorbing compounds known to occur widely in various marine organisms; however, several compounds having UV-screening properties still need to be identified. The synthesis of scytonemin, a predominant UV-A-photoprotective pigment, is exclusively reported in cyanobacteria. Carotenoids are important components of the photosynthetic apparatus that serve both light-harvesting and photoprotective functions, either by direct quenching of the singlet oxygen or other toxic reactive oxygen species or by dissipating the excess energy in the photosynthetic apparatus. The production of photoprotective compounds is affected by several environmental factors such as different wavelengths of UVR, desiccation, nutrients, salt concentration, light as well as dark period, and still there is controversy about the biosynthesis of various photoprotective compounds. Recent studies have focused on marine organisms as a source of natural bioactive molecules having a photoprotective role, their biosynthesis and commercial application. However, there is a need for extensive work to explore the photoprotective role of various UV-absorbing compounds from marine habitats so that a range of biotechnological and pharmaceutical applications can be found.     

Effects of global change factors on fatty acids and mycosporine‐like amino acid production in Chroothece richteriana (Rhodophyta)

Under natural conditions, Chroothece richteriana synthesizes a fairly high proportion of fatty acids. However, nothing is known about how environmental changes affect their production, or about the production of protective compounds, when colonies develop under full sunshine with high levels of UV radiation. In this study, wild colonies of C. richteriana were subjected to increasing temperature, conductivity, ammonium concentrations and photosynthetically active radiation (PAR), and UV radiations to assess the potential changes in lipid composition and mycosporine‐like amino acids (MAAs) concentration. The PERMANOVA analysis detected no differences for the whole fatty acid profile among treatments, but the percentages of α‐linolenic acid and total polyunsaturated fatty acids increased at the lowest assayed temperature. The percentages of linoleic and α‐linolenic acids increased with lowering temperature. γ‐linolenic and arachidonic acids decreased with increasing conductivity, and a high arachidonic acid concentration was related with increased conductivity. The samples exposed to UVB radiation showed higher percentages of eicosapentaenoic acid and total monounsaturated fatty acids, at the expense of saturated fatty acids. MAAs accumulation increased but not significantly at the lowest conductivity, and also with the highest PAR and UVR exposure, while ammonium and temperature had no effect. The observed changes are probably related with adaptations of both membrane fluidity to low temperature, and metabolism to protect cells against UV radiation damage. The results suggest the potential to change lipid composition and MAAs concentration in response to environmental stressful conditions due to climate change, and highlight the interest of the species in future research about the biotechnological production of both compound types.     

The effect of ultraviolet radiation on photosynthesis and ultraviolet-absorbing substances in the endemic Arctic macroalga Devaleraea ramentacea (Rhodophyta)

In field studies conducted at the Kongsfjord (Spitsbergen), the effect of filtered natural radiation conditions (solar without ulraviolet [UV]-A+UV-B, solar without UV-B, solar) on photosynthesis and the metabolism of UV-absorbing mycosporine-like amino acids (MAAs) in the marine red alga Devaleraea ramentacea have been studied. While solar treatment without UV-A+UV-B did not affect photosynthesis during the course of a day, solar without UV-B and the full solar spectrum led to a strong inhibition. However, after offset of the various radiation conditions, all algae fully recovered. Isolates collected from different depths were exposed in the laboratory to artificial fluence rates of photosynthetic active radiation (PAR), PAR+UV-A, and PAR+UV-A+UV-B. The photosynthetic capacity was affected in accordance with the original sampling depth, i.e. shallow-water isolates were more resistant than algae from deeper waters, indicating that D. ramentacea is able to acclimate to changes in irradiance. Seven different UV-absorbing MAAs were detected in this alga, namely mycosporine-glycine, shinorine, porphyra-334, palythine, asterina-330, palythinol, and palythene. The total amount of MAAs continuously decreased with increasing collecting depth when sampled in mid June, and algae taken in late August from the same depths contained on average 30–45% higher MAA concentrations, indicating a seasonal effect as well. The presence of increasing MAA contents with decreasing depth correlated with a more insensitive photosynthetic capacity under both UV-A and UV-B treatments. Populations of D. ramentacea collected from 1 m depth, with one fully exposed to solar radiation and the other growing protected as understorey vegetation underneath the kelp Laminaria saccharina, exhibited quantitatively different MAA compositions in the apices. The exposed seaweeds contained 2.5-fold higher MAA values compared with the more shaded algae. Moreover, the exposed isolates showed a strong tissue gradient in MAAs, pigments, and proteins. The green apices contained 5-fold higher MAA contents than the red bases. Transplantation of D. ramentacea from 2 m depth to the surface induced the formation and accumulation of MAAs after 1 week exposure to the full solar spectrum. Control samples which were treated with the solar spectrum without UV-A+B or with solar without UV-B showed unchanged MAA contents, indicating a strong UV-B effect on MAA metabolism. All data well supported the suggested physiological function of MAAs as natural UV sunscreens in macroalgae.     

Short-term variations of mycosporine-like amino acids in the carrageenan-producing red macroalga Mazzaella laminarioides (Gigartinales,Rhodophyta) are related to nitrate availability

Journal of Applied Phycology - The effect of solar UV radiation exposure and NO3– supply on mycosporine-like amino acids (MAAs) accumulation in the carrageenan-producing red macroalga...     

Natural ultraviolet radiation and photosynthetically active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta)

The UV-absorbing mycosporine-like amino acids (MAAs) are hypothesized to protect organisms against harmful UV radiation (UVR). Since the physiology and metabolism of these compounds are unknown, the induction and kinetics of MAA biosynthesis by various natural radiation conditions were investigated in the marine red alga Chondrus crispus collected from Helgoland, Germany. Three photosynthetically active radiation (PAR, 400–700 nm) treatments without UVR and three UV-A/B (290–400 nm) treatments without PAR were given. Chondrus crispus collected from 4–6 m depth contained only traces of the MAA palythine. After 24 h exposure to 100% ambient PAR, traces of three additional MAAs, shinorine, palythinol and palythene, were detected, and their concentrations increased strongly during a one-week exposure to all PAR treatments. The concentration of all MAAs varied directly with PAR dose, with palythine and shinorine being four- to sevenfold higher than palythinol and palythene. Likewise, naturally high doses of both UV-A and UV-B resulted in a strong accumulation of all MAAs, in particular shinorine. While shinorine accumulation was much more stimulated by UVR, the content of all other MAAs was more affected by high PAR, indicating an MAA-specific induction triggered by UVR or PAR. Received: 24 September 1997 / Accepted: 17 December 1997     

Chemical Composition during Maturing and Spawning of the Sponge Dysidea herbacea (Porifera: Demospongiae)

Mycosporine-like amino acids (MAAs) have been implicated in many biochemical processes in marine organisms, but the major emphasis has been directed to their role as UV protectant compounds. The quantitation of MAAs, mycosporine-glu-gly, mycosporine-gly, usujirene and palythene in the sponge Dysidea herbacea [34] suggests that whereas some mycosporine amino acids may serve in this capacity, others are intrinsically involved in the reproductive process. The role of other compounds, such as homarine, gadusol and arachidonic acid, in reproduction of this sponge is also discussed.     

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.     

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.

     

Mycosporine-Like Amino Acids Extracted from Scallop (<Emphasis Type="Italic">Patinopecten yessoensis</Emphasis>) Ovaries: UV Protection and Growth Stimulation Activities on Human Cells

Scallops (Patinopecten yessoensis) are extensively cultured and landed in Japan. During the processing of scallops, large amounts of internal organs and shells are discharged as industrial wastes. To reduce the burden on the environment, effective utilization and disposal methods of the wastes are required. Therefore, we have screened for useful materials in scallop internal organs, and found ultraviolet (UV) absorbing compounds from scallop ovaries. Based on UV absorption, electrospray ionization-mass spectrometry (ESI-MS), ESI-MS/MS, and nuclear magnetic resonance (NMR) spectra, three UV absorbing compounds were identified as mycosporine-like amino acids (MAAs): shinorine, porphyra-334 (P-334), and mycosporine-glycine. To investigate whether MAAs can act as a UV protector for human cells, we examined the protective effects of the three MAAs on human fibroblast cells from UV irradiation. All of the three examined MAAs protected the cells from UV-induced cell death. In particular, mycosporine-glycine had the strongest effect. Further, we found a promotion effect of MAAs on the proliferation of human skin fibroblast cells. From these results, it was found that the three MAAs isolated from scallop ovaries have a protective effect on human cells against UV light. MAAs have potential applications in cosmetics and toiletries as a UV protectors and activators of cell proliferation.     

Mycosporine-like amino acids (MAAs): chemical structure, biosynthesis and significance as UV-absorbing/screening compounds

Continuous depletion of the stratospheric ozone layer has resulted in an increase in ultraviolet-B (UV-B; 280-315 nm) radiation on the earth's surface which inhibits photochemical and photobiological processes. However, certain photosynthetic organisms have evolved mechanisms to counteract the toxicity of ultraviolet or high photosynthetically active radiation by synthesizing the UV-absorbing/screening compounds, such as mycosporine-like amino acids (MAAs) and scytonemin besides the repair of UV-induced damage of DNA and accumulation of carotenoids and detoxifying enzymes or radical quenchers and antioxidants. Chemical structure of various MAAs, their possible biochemical routes of synthesis and role as photoprotective compounds in various organisms are discussed.     

The significance of the study about the biological effects of solar ultraviolet radiation using the Exposed Facility on the International Space Station.

It is believed that ultraviolet (UV) radiation from the sun participated in events related to the chemical evolution and birth of life on the primitive Earth. Although UV radiation would be also a driving force for the biological evolution of life on Earth, life space of the primitive living organisms would be limited in the UV-shielded place such as in the water at an early stage of the evolution of life. After the formation of stratospheric ozone layer through the production of oxygen by photoautotroph, living organisms were able to expand their domain from water to land. As a result, now, many kinds of living organisms containing human beings are flourishing on the ground. In the near future, increased transmission of harmful solar UV radiation may reach the Earth's surface due to stratospheric ozone layer depletion. In order to learn more about the biological effects of solar UV radiation with or without interruption by the ozone layer, the utilization of an Exposed Facility on the International Space Station is required. Experiments proposed for this facility would provide a tool for the scientific investigation of processes involved in the birth and evolution of life on Earth, and could also demonstrate the importance of protecting the Earth's future environment from future ozone layer depletion.