Distribution of mycosporine-like amino acids and photoprotective carotenoids among freshwater phytoplankton assemblages

Phytoplankton have evolved different strategies to minimize the potential damage caused by solar ultraviolet radiation (UVR), including the synthesis of UV-absorbing compounds that act as sunscreens and carotenoids that provide protection against photooxidative stress. The concen- tration and qualitative composition of mycosporine-like amino acids (MAAs) and photoprotective carotenoids (PPCs) were investigated in natural phytoplankton assemblages of 26 lakes located below and above the treeline in the Alps and the Pyrenees. Among these lakes, exposure to UV varied because of differences in the incident spectral dose, water column transparency, stratification, and maximum depth. Seven MAAs were identified, but the most abundant were shinorine (λmax = 334 nm) and palythine (λmax = 320 nm). The highest concentrations of MAAs (up to 9.6 µg (µg chl a) -1 ) and PPCs (up to 0.6 µg (µg chl a) -1 ) were found in the clearest and shallowest lakes, while phyto- plankton from lakes with low UV transparency generally presented low values. However, phyto- plankton of some clear lakes located at high altitude did not have high concentrations of these com- pounds. Consequently, underwater downwelling UVR, UV water transparency, or lake altitude explained only a low percentage (< 26%) of the variability among lakes in MAA and PPC concentra- tion. Within the water column, the concentration of MAAs decreased in most cases with depth, sug- gesting their photoprotective role. Our results indicate that MAAs and PPCs are widespread among lake phytoplankton assemblages and suggest that other environmental factors besides UV exposure are important in regulating their synthesis.

[1]  M. Vernet,et al.  Spectral properties and photosynthetic action in red-tide populations of Prorocentrum micans and Gonyaulax polyedra , 1989 .

[2]  W. Dunlap,et al.  Occurrence of UVA- and UVB-absorbing compounds in 152 species (206 strains) of marine microalgae , 1999 .

[3]  Suzanne Roy,et al.  The effects of UV radiation in the marine environment: Strategies for the minimisation of UV-induced damage , 2000 .

[4]  R. Akselman,et al.  An unusual bloom of Gyrodinium cf. aureolum in the Argentine sea: community structure and conditioning factors , 1992 .

[5]  W. Dunlap,et al.  Photoacclimation of antarctic marine diatoms to solar ultraviolet radiation , 1996 .

[6]  W. Dunlap,et al.  Small-molecule antioxidants in marine organisms: Antioxidant activity of mycosporine-glycine , 1995 .

[7]  J. Catalán,et al.  Attenuation of ultraviolet radiation in mountain lakes: Factors controlling the among‐ and within‐lake variability , 2000 .

[8]  C. Llewellyn,et al.  The rapid determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase high-performance liquid chromatography , 1983 .

[9]  R. Sommaruga,et al.  Dissolved Organic Carbon Concentration and Phytoplankton Biomass in High-mountain Lakes of the Austrian Alps: Potential Effect of Climatic Warming on UV Underwater Attenuation , 1999 .

[10]  R. Bidigare,et al.  EVIDENCE A PHOTOPROTECTIVE FOR SECONDARY CAROTENOIDS OF SNOW ALGAE 1 , 1993 .

[11]  C. Buckley,et al.  A study of the effects of near UV radiation on the pigmentation of the blue-green alga Gloeocapsa alpicola , 1976, Archives of Microbiology.

[12]  L. Nedbal,et al.  The occurrence of UV-B absorbing mycosporine-like amino acids in freshwater and terrestrial microalgae (Chlorophyta) , 1999 .

[13]  A. Ben‐Amotz,et al.  Mode of Action of the Massively Accumulated beta-Carotene of Dunaliella bardawil in Protecting the Alga against Damage by Excess Irradiation. , 1989, Plant physiology.

[14]  M. Lesser,et al.  Effects of ultraviolet radiation on primary productivity in a high altitude tropical lake , 1998, Hydrobiologia.

[15]  D. Karentz Chemical Defenses of Marine Organisms Against Solar Radiation Exposure: UV-Absorbing Mycosporine-Like Amino Acids and Scytonemin , 2001 .

[16]  E. Helbling,et al.  Acclimatization of Antarctic natural phytoplankton assemblages when exposed to solar ultraviolet radiation , 1995 .

[17]  G. Daleo,et al.  Occurrence of mycosporine-like amino acids in the red-tide dinoflagellate Alexandrium excavatum: UV-photoprotective compounds? , 1990 .

[18]  A. Banaszak,et al.  Biochemical photoadaptation in vision: U.V.-absorbing pigments in fish eye tissues , 1989 .

[19]  F. Garcia-Pichel,et al.  UV-absorbing mycosporine-like compounds in planktonic and benthic organisms from a high-mountain lake , 1999 .

[20]  A. Sigleo,et al.  Photoinduction of UV-absorbing compounds in six species of marine phytoplankton , 1998 .

[21]  D. Karentz,et al.  Mycosporine-like amino acids: possible UV protection in eggs of the sea hare Aplysia dactylomela , 1998 .

[22]  K. Whitehead,et al.  Influence of mycosporine‐like amino acids (MAAs) on UV absorption by particulate and dissolved organic matter in La Jolla Bay , 2000 .

[23]  J. Gattuso,et al.  Ultraviolet‐B radiation stimulates shikimate pathway‐dependent accumulation of mycosporine‐like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates , 1999 .

[24]  H. Paerl,et al.  Carotenoid enhancement and its role in maintaining blue-green algal (Microcystis aeruginosa) surface blooms1 , 1983 .

[25]  D. Bramich,et al.  Effects of UV-B irradiation on growth and survival of Antarctic marine diatoms , 1994 .

[26]  C. Wiencke,et al.  Simulation of the effects of naturally enhanced UV-radiation on photosynthesis of Antarctic phytoplankton , 2000 .

[27]  D. Karentz,et al.  Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: Potential protection from ultraviolet exposure , 1991 .

[28]  Sandmann,et al.  Protection of photosynthesis against ultraviolet-B radiation by carotenoids in transformants of the cyanobacterium synechococcus PCC7942 , 1999, Plant physiology.

[29]  F. Garcia-Pichel A model for internal self‐shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens , 1994 .

[30]  D. H. Robinson,et al.  Photoinduction of UV-absorbing compounds in Antarctic diatoms and Phaeocystis antarctica , 1997 .

[31]  H. Marchant,et al.  UV-B protecting compounds in the marine algaPhaeocystis pouchetii from Antarctica , 1991 .

[32]  A. Banaszak,et al.  Increased sensitivity to ultraviolet radiation in nitrogen‐limited dinoflagellates: Photoprotection and repair , 2002 .

[33]  G. F. Humphrey,et al.  New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton , 1975 .

[34]  R. Castenholz,et al.  CHARACTERIZATION AND BIOLOGICAL IMPLICATIONS OF SCYTONEMIN, A CYANOBACTERIAL SHEATH PIGMENT 1 , 1991 .

[35]  S. Taguchi,et al.  Effect of UV-B radiation on the fatty acid composition of the marine phytoplankter Tetraselmis sp.: Relationahip to cellular pigments , 1994 .

[36]  A. Banaszak,et al.  ULTRAVIOLET SUNSCREENS IN GYMNODINIUM SANGUINEUM (DINOPHYCEAE): MYCOSPORINE‐LIKE AMINO ACIDS PROTECT AGAINST INHIBITION OF PHOTOSYNTHESIS , 1998 .

[37]  M. Blumthaler,et al.  Altitude effect of solar UV radiation dependent on albedo, turbidity, and solar elevation , 1993 .

[38]  I. Laurion,et al.  Large variability in the concentration of mycosporine‐like amino acids among zooplankton from lakes located across an altitude gradient , 2001 .