481 Chemical Defenses of Marine Organisms Against Solar Radiation Exposure: UV-Absorbing Mycosporine-Like Amino Acids and Scytonemin Deneb Karentz CONTENTS I. Introduction 482 A. Ultraviolet Radiation and the Solar Spectrum 482 B. Ultraviolet Radiation in Marine Environments 483 C. Biological Consequences of Ultraviolet Exposure 484 1. Absorption of UV by Organic Molecules 484 2. Photo-Oxidative Stress 484 D. Biological Defenses Against Ultraviolet Radiation 484 1. Avoidance 484 2. Sunscreening 485 3. Antioxidants 486 II. UV-Absorbing Compounds in Marine Organisms 486 A. Mycosporine-Like Amino Acids (MAAs) 486 1. MAA Structure 486 2. MAA Synthesis 487 3. Phylogenetic Patterns of MAA Occurrence 491 4. Geographic Distribution of MAAs 493 5. MAAs in Freshwater Taxa 498 6. Concentration of MAAs in Cells and Tissues 499 7. Distribution of MAAs Relative to Radiation Exposure (Depth and Season) 500 8. Regulation of MAA Concentrations 501 9. Effectiveness of MAAs for UV Protection 505 10. Other Functions of MAAs in Marine Organisms 506 B. Scytonemin 508 1. Scytonemin Structure and Localization 508 2. Scytonemin Distribution 508 3. Regulation of Scytonemin Concentration 508 4. Effectiveness of Scytonemin for Ultraviolet Protection 509 15 9064_ch15/fm Page 481 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC 482 Marine Chemical Ecology III. Evolutionary Aspects of Ultraviolet Protection 510 Acknowledgments 511 References 511 I. INTRODUCTION Ultraviolet radiation (UV, 100 to 400 nm) comprises the shortest wavelengths of the solar spectrum that reach the Earth’s surface (~290 to 400 nm). Although UV spans a very small range within the solar spectral band, it can elicit a wide variety of biological responses and it is impossible for most organisms to avoid UV exposure. UVB wavelengths (280 to 320 nm) are injurious to cells (e.g., cause direct molecular damage to DNA and proteins), while longer UVA wavelengths (320 to 400 nm) can be both harmful (e.g., initiate photo-oxidative damage) and beneficial (e.g., required for vitamin D synthesis and DNA repair). 1–3 It is generally accepted that incident UV wavelengths and intensities were much more haz- ardous under ancient Earth atmospheres than they are today. 4,5 As a result, nearly all organisms have some capability for protection against UV exposure and for repair of UV-induced damage; many of these biological defenses are common across very diverse taxa. 2,6,7 Secondary metabolites that absorb UV radiation and provide protection from UV damage occur in most phylogenetic groups. 8 For example, melanins in bacteria, fungi, and animals and flavanoids in plants significantly reduce the potential damage caused by direct exposure to UV. 9–11 In aquatic organisms, mycospo- rine-like amino acids (MAAs) and scytonemin are assumed to serve a complementary or analogous sunscreen function. 6,12–15 A. U LTRAVIOLET R ADIATION AND THE S OLAR S PECTRUM Within the electromagnetic spectrum, UV is the wavelength band between X-rays (1 to 100 nm) and visible light (400 to 700 nm). UV wavelengths are further subdivided into four categories based on physical properties and the biological consequences of exposure. 3 • Vacuum UV (100 to 200 nm): Air and water absorb this portion of the UV spectrum; therefore, these wavelengths do not penetrate past the upper reaches of the Earth’s atmosphere. • UVC (far UV, 200 to 280 nm): UVC wavelengths are the most damaging to organisms because they are most efficiently absorbed by nucleic acids and proteins. Fortunately, as sunlight is attenuated through the atmosphere, the entire UVC component is absorbed and these wavelengths do not penetrate past the stratosphere. Although UVC was prob- ably a biologically important component of incident solar radiation during earlier geo- logic eras when life on Earth first originated and began to evolve (without benefit of an ozone layer), UVC is not ecologically relevant in present day environments. However, much of what is known about UV photobiology is the result of research investigating the response of cells to UVC exposure from artificial sources (e.g., germicidal lamps emitting 254 nm radiation). • UVB (middle UV, 280 to 320 nm): UVB is extremely harmful to organisms and the primary cause of erythema (sunburning of human skin). A large proportion of the UVB below 300 nm is absorbed by stratospheric ozone, but the small amount that does reach the Earth’s surface is sufficient to cause significant damage and can be lethal. The primary consequence of ozone depletion is an increase in the bandwidth and intensity of shorter wavelengths of incident UVB. 9064_ch15/fm Page 482 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC Chemical Defenses of Marine Organisms Against Solar Radiation Exposure 483 • UVA (near UV, 320 to 400 nm): These longest wavelengths of UV can be both harmful and beneficial. UVA is implicated in many photosensitive reactions and can compound the damage caused by UVB. Despite the negative impact of UVA on cells, these wave- lengths trigger an array of fundamental responses in organisms through the action of cryptochromes. 16 UVA wavelengths are not significantly affected by stratospheric ozone. B. U LTRAVIOLET R ADIATION IN M ARINE E NVIRONMENTS After atmospheric attenuation of UV, marine organisms have an additional environmental UV filter of the overlying water column. Although intertidal species have the greatest risk of exposure and experience the highest doses of UV, planktonic and subtidal benthic organisms are also subject to harmful levels of UV in surface waters and at shallow depths. Pure water is transparent to UV wavelengths, but dissolved substances and particulate matter present in natural waters cause significant absorption, reflection, and diffusion of UV within the water column. This results in variable absorption of wavelengths from the incident UV spectrum and wide variation in attenu- ation coefficients between different water masses (Figure 15.1). 17–20 Even in the clearest waters, UVB is usually attenuated within the upper 10 m of the water column, although UVB wavelengths have been detected up to 60 m in the very transparent waters of the Southern Ocean during springtime ozone depletion. 18,20–23 UVA wavelengths generally penetrate to depths of approximately 50 m or more. Characterization of the underwater UV regime is not extensive, although documentation of UV penetration to ecologically significant depths has been known since at least the 1950s. 24 The importance of daily and seasonal variations in UV or the role of vertical mixing in the temporal variability of exposure have not yet been comprehensively studied or evaluated but are the focus of current research efforts. FIGURE 15.1 A. In-water attenuation of four indicated UV wavelengths in coastal Antarctic waters on 16 Oct. 1996 measured with a PUV-500 spectroradiometer (Biospherical Instruments, San Diego, CA). B. Spectral depth range of attenuation to 10% of incident UV levels in various water masses. Number labels on lines refer to reference citations. Modified from Booth, C.R. and Morrow, J.E., Impacts of solar UVR on aquatic microorganisms: the penetration of UV into natural waters, Photochem. Photobiol. , 65:254–257, 1997, Figure 3. With permission from the Amercian Society for Photobiology, Augusta, GA. 308 nm 320 nm 340 nm 380 nm 20 20 20 20 17 17 19 18 UVAUVB wavelength (nm) 280 320 360 400 0.01 0.1 1 10 0.1 1 10 100 0 5 10 15 20 25 30 depth (m) depth (m) UV ( W cm -2 ) A B 9064_ch15/fm Page 483 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC 484 Marine Chemical Ecology C. B IOLOGICAL C ONSEQUENCES OF U LTRAVIOLET E XPOSURE 1. Absorption of UV by Organic Molecules UV (especially UVB) is absorbed by two major groups of organic molecules — nucleic acids and proteins. Absorption of UV photons causes these molecules to undergo conformational changes that subsequently interfere with or destroy their ability to participate in vital metabolic functions. The formation of UV photoproducts in DNA can significantly compromise the accuracy of transcription and replication; therefore, UV damage to DNA molecules by UV exposure can result in debilitating, mutagenic, and lethal effects. 3 Damage to proteins is also problematic as these molecules function as enzymes, hormones, and structural components of cells. Generally, protein damage is not con- sidered as important as damage to DNA. 25 Protein molecules are present in numerous copies and are readily degraded and resynthesized; however, prevention of UV-induced damage to defray the energetic costs of repair and replacement of molecules is certainly advantageous. 2. Photo-Oxidative Stress In addition to the direct absorption as a biological hazard, UV can have additional indirect effects on organisms. 26,27 A number of UV photochemical reactions occur in solutions, both within cells and in the external aquatic environment. In the presence of UV, water itself is hydrolyzed, producing hydroxyl ions. Related reactions involving dissolved substances and mediated by UV lead to the formation of peroxides, super oxide, and other radicals. These reactive products are toxic by causing oxidative damage to biological molecules. 28–31 D. B IOLOGICAL D EFENSES AGAINST U LTRAVIOLET R ADIATION In response to the ubiquitous presence of UV, most organisms have developed a variety of defenses to tolerate exposure. 2 These include adaptations to minimize UV exposure and to repair UV-induced damage when protective measures are not adequate. 2,6 Characteristics that are useful for evading UV damage include avoidance, screening of UV, and antioxidant activity. 6 The focus of this chapter is on specific chemical defenses used by marine organisms to reduce the amount of UV radiation that reaches vital molecular targets, but a very brief overview of other UV defense strategies is presented below. 1. Avoidance Physically moving away from UV radiation is one of the most effective means of minimizing exposure. This can be accomplished in a number of ways and does not necessarily require moving great distances. However, it does require that an organism have the ability to detect the presence of UV wavelengths (directly or indirectly) and that the organism is capable of movement. UV can alter the behavior (motility and photo-orientation) of unicellular organisms and metazoans. 32–34 Generally, organisms tend to avoid high light intensities, and many of the photoreceptors respon- sible for light responses detect UVA and visible, not the more harmful, UVB radiation. 16 In terrestrial plants, there are many examples of blue light receptors and numerous genes that are regulated by blue light exposure. 35 In some cases (e.g., chalcone synthesis), the roles of various wavelengths from the UV and visible spectra can be clearly distinguished on both a genetic and biochemical basis. While receptors for visible light are very common in marine species, less is known about the detection of UV. In aquatic invertebrates, UV photoreception is primarily in the UVA wavelengths, although variable UVB phototropic responses have been observed. 36–38 Visual UV photosensitivity is a specific characteristic in some animal species, including arthropods, reptiles, fish, birds, and 9064_ch15/fm Page 484 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC Chemical Defenses of Marine Organisms Against Solar Radiation Exposure 485 mammals. 39–41 It is presumed that the potential for ocular damage caused by UV is offset by the benefits of UV vision (e.g., increased visual acuity for capture of prey). 41,42 Obligate phototrophs have a dilemma with regard to solar exposure. UVA and/or visible wavelengths (also referred to as photosynthetically available radiation, PAR, 350 to 700 nm 43 ) are required for photosynthesis, but exposure to UV can be harmful. Benthic autotrophs (e.g., algal macrophytes and seagrasses) cannot relocate once spores or seeds have germinated. Phytoplanktonic species have more options for avoiding UV through passive transport by vertical mixing or active vertical migration behavior. Some biological processes are on a diurnal cycle and may be entrained to a circadian rhythm. When events are scheduled at night, this provides an opportunity for UV avoidance. For example, dinoflagellates tend to undergo mitosis and cytokinesis during the dark, thereby avoiding UV exposure during a vulnerable period of the cell cycle. A common temporal avoidance strategy in invertebrates is spawning after sunset. 44 In the ascidian Corella inflata , not only are embryos shielded within the adult body cavity during development, but release and settlement of competent larvae are nocturnal events. 45 Usually, intensities of UV and visible light co-vary so that an avoidance response to one includes avoiding the other. However, under ozone depletion, incident UVB intensities increase while UVA/visible light fields remain unchanged. Therefore, if organisms are relying on visible or UVA wavelengths to provide accurate proportional cues for changes in UVB, ozone depletion can exert an undue and unexpected selective pressure on populations and communities. 2. Sunscreening The outer covering of organisms can provide substantial protection against UV exposure. At the cellular level, cell walls and membranes offer protection by blocking or attenuating incident UV before it reaches organelles and other intracellular components. For example, it is estimated that the outer silicate wall of diatoms can absorb up to 30% of incident UVB radiation, affording a significant primary UV defense for the cell. 46 For metazoans, cuticles, carapaces, shells, scales, feathers, and fur all provide an effective optical barrier between incident UV and internal tissues. These external surfaces can absorb more than 95% of incident UVB, providing an effective radiation shield for internal cells and tissues. 47,48 The environment can also provide passive shading from UV. In benthic cyanobacterial communities, the extracellular presence of ferric chloride in sediments functions as an adequate UV filter for cells. 49 Across diverse taxonomic groups of marine organisms there are several classes of compounds that absorb UV and act as putative sunscreens. These include scytonemin (Figure 15.9), an extra- cellular cyanobacterial sheath pigment, and the mycosporine-like amino acids (MAAs, Figures 15.3–15.6) that are usually located intracellularly in cyanobacteria, algae, invertebrates, and fish. These compounds are the major focus of this chapter and will be discussed in detail below. Many marine species also possess the tyrosinase-mediated pathway to synthesize the UV-absorbing pigment melanin. Melanin occurs in a wide range of taxa including bacteria, fungi, invertebrates, and chordates. While much is known about the role of melanin in the UV protection of mammalian skin, very little research has been conducted to examine the efficiency of melanin as a UV-protective mechanism in aquatic taxa. 9 It is known that melanin levels in juvenile ham- merhead sharks, Sphyrna lewini , are directly correlated to solar UV exposure; in the freshwater crustacean Daphnia pulex , melanin concentrations are genetically determined within populations and are correlated to UV sensitivity. 50,51 The few studies that have been undertaken suggest that melanin has an important role in UV protection in aquatic environments. Several other UV-absorbing compounds have been implicated in the protection of aquatic organisms from UV exposure. These compounds do not seem to be as common as MAAs (Figures 15.3–15.6) or scytonemin (Figure 15.9), possibly because less effort has been made to 9064_ch15/fm Page 485 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC 486 Marine Chemical Ecology study them. One such molecule is biopterin glucoside (BG), a UVA-absorbing compound isolated from cyanobacteria and related to pteridine pigments. 52 The synthesis of BG in Oscillatoria sp. is induced by exposure to UVA wavelengths, and the presence of BG has been shown to confer increased UVA resistance to cells. 53,54 However, in intertidal cyanobacterial mat communities, pterin concentrations remain unchanged across seasons, suggesting a minor role in UV protection. 55 Further studies suggest that pterins may have a regulatory role in UV protection. In Chlorogloeopsis sp., pterins appear to function as UVB receptors and may be involved with signaling the induction of MAA synthesis. 56 Further research on these compounds is required to better understand their contribution to cell survival under solar stress. Other compounds such as phlorotannins, sporopollenin, coumarins, tridentatols, polyphenolics, and several as yet unidentified substances (e.g., P380) have also been implicated as UV protectants that can increase UV tolerance. 57–63 With the rapidly accelerating rate of research in the area of aquatic UV photobiology, it is highly likely that additional new types of UV-screening compounds will continue to be discovered. Many of these secondary metabolites probably have multiple protective functions. For example, tridentatols serve as allelopathic agents, antioxidants, and sunscreens. 57,58,64 3. Antioxidants Cells have substantial chemical defenses against the UV photoproducts produced in seawater and intracellular fluids. Many organisms have antioxidants (e.g., carotenoids, ascorbate, tocopherols, anthocyanins, and tridentatols) that quench photo-oxidative reactions. 64–67 Cells also have enzymes (e.g., catalase and superoxide dismutase) that can counteract the oxidative nature of peroxides and other radicals. 26 Some compounds, such as the UV-absorbing pigment melanin, can act as both optical filter and antioxidant. 68 The MAA mycosporine-glycine (Figure 15.3) functions in a similar dual capacity. 69 The role of UV-mediated reactions in seawater relative to biological effects is an important current area of study. II. UV-ABSORBING COMPOUNDS IN MARINE ORGANISMS A. M YCOSPORINE -L IKE A MINO A CIDS (MAA S ) In the late 1960s, studies of water extracts from marine cyanobacteria and cnidarians detected unknown UV-absorbing compounds that were initially named for their maximum wavelengths of absorbance, e.g., substance-320 (S-320) exhibited maximum absorbance at 320 nm. 70,71 Relatively high concentrations of S-320 and related compounds were observed in a variety of marine organ- isms. It was speculated that these compounds either have a solar protective function or are precursors to common pigments. During the subsequent decade, the widespread and taxonomically diverse distribution of S-320 and similar UV-absorbing compounds in marine organisms was confirmed. 72–78 Additional investigations strengthened the notion that these compounds serve as sunscreens. 73,79–81 With the subsequent elucidation of molecular structures (Figures 15.3–15.6), the S compounds were identified as mycosporine-like amino acids (MAAs). 80,82–87 1. MAA Structure MAAs found in aquatic organisms are closely related to fungal mycosporines that were first isolated from sporulating mycelia. 88–91 12 for a detailed comparison of MAA and mycosporine structure.) MAAs are colorless water-soluble compounds with absorption maxima (309 to 360 nm) within the UVB and UVA (Table 15.1). 92 They are derivatives of aminocyclohex- enone or aminocyclohexenimine rings (Figure 15.2). 93 Nineteen known MAA compounds result from N -substitutions of different amino acid moieties to the cyclohexenone or cyclohexenimine chromophore. There are only two aminocyclohexenone-derived MAAs from marine organisms: 9064_ch15/fm Page 486 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC (See Bandaranayake Chemical Defenses of Marine Organisms Against Solar Radiation Exposure 487 mycosporine-glycine and mycosporine-taurine (Figure 15.3). 12 These are most similar in structure to the fungal mycosporines and the only two known MAAs with maximum absorbance in the UVB. The remaining MAAs are iminomycosporines and absorb maximally at UVA wavelengths. The majority of iminomycosporines contain glycine (12 MAAs, including shinorine, porphyra-334, palythine, asterina-330, and palythinol), and the other five iminomycosporines have serine or threonine substitutions (Figures 15.4 and 15.5). 94,95 Two MAAs isolated from reef-building corals are sulfate esters (palythine:threonine-sulfate and palythine:serine-sulfate). 96 It is most likely that more types of MAAs and related compounds occur in marine organisms. With increasing interest in these molecules and further investigation, identification of additional forms is expected. Related UV-absorbing compounds found in marine organisms are gadusol (1,4,5-trihydroxy- 5-hydroxymethyl-2-methoxycyclohex-1-en-3-one) and deoxy-gadusol (Figure 15.6). 97–99 Gadusol is a colorless oil first observed in the eggs of fish and sea urchins. 97–99 It is a derivative of cyclohexane and is structurally similar to both the fungal mycosporines and MAAs. An isomer of gadusol (spinulosin quinol-hydrate) is synthesized in fungi and arises from an acetate precursor. 97 Other fungal mycosporines are synthesized via products of the shikimate pathway, and it is speculated that the shikimate pathway is also a plausible synthetic route for gadusol. 97 2. MAA Synthesis Metabolic pathways for MAA synthesis, conversion, and degradation have not yet been elucidated. Based on structural affinity with gadusol and fungal mycosporines, MAAs are most likely syn- thesized through the shikimate pathway. 74,97 This is confirmed for the production of MAAs by the zooxanthellae of the coral Stylophora pistillata and is probably true for other organisms as well . 100 The shikimate pathway is present in a variety of taxa including bacteria, fungi, algae, and plants. The products of this pathway are involved in the synthesis of the aromatic amino acids tyrosine, phenylalanine, and tryptophan. There is no complementary or analogous pathway for the synthesis of aromatic compounds in animals. 101 Organisms that do not have the shikimate pathway have an obligate requirement for ingestion of the aromatic amino acids phenylalanine and tryptophan FIGURE 15.2 Aminocyclohexenone and aminocyclohexenimine ring structures. FIGURE 15.3 Molecular structures and wavelengths of maximum absorbance ( λ max ) for two aminomycospo- rines from marine organisms. O NHR OCH 3 OH HO NHR OCH 3 OH HO NH aminocyclohexenone aminocyclohexenimine OCH 3 NH COOH HO HO OCH 3 NH HO HO O O mycosporine-glycine λ max = 310 nm mycosporine-taurine λ max = 309 nm SO 3 H 9064_ch15/fm Page 487 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC 488 Marine Chemical Ecology TABLE 15.1 Chemical and Optical Characteristics of Deoxy-Gadusol, Gadusol, and 19 MAAs that Ha ve Been Identified in Marine Organisms Compound Abbreviation Formula mw λ max ε Species Deoxy-gadusol DG C 8 H 12 O 5 188 268 a 294 b Auxis thazard 76 Gadusol GD C 8 H 12 O 6 204 269 a 296 b 12400 97 21800 76 Gadus morhua 97 Auxis thazard 76 Palythine PI C 10 H 16 N 2 O 5 244 320 36200 204 29400 @ 310 nm 153 Palythoa tuberculosa 204 Chondrus yendoi 84 Mycosporine-glycine MG C 10 H 15 NO 6 245 310 28100 @ 310 nm 153 22400 @ 320 nm 153 Palythoa tuberculosa 83 Palythine-serine PS C 11 H 18 N 2 O 6 274 320 10500 95 Pocillopora eydouxi 95 Usujirene US C 13 H 20 N 2 O 5 284 357 Palmaria palmata 205 Palythene PE C 13 H 20 N 2 O5 284 360 50000 75,85 Palythoa tuberculosa 75,85 Mycosporine-methylamine:serine (N-methylpalythine:serine) MS C 12 H 20 N 2 O 6 288 325 16600 95 Pocillopora eydouxi 95 Asterina-330 AS C 12 H 20 N 2 O 6 288 330 23030 @ 310 nm 160 37260 @ 320 nm 160 Asterina pectinifera 206 Mycosporine-taurine MT C 10 H 17 NSO 7 295 309 c Anthopleura elegantissima 120 Mycosporine-methylamine:threonine (N-methylmycosporine:threonine) MM C 13 H 22 N 2 O 6 302 330 3300 94 2800 @ 320 nm 94 1900 @ 313 nm 94 Pocillopora damicornis 94 Stylophora pistillata 94 Mycosporine-2-glycine M2 C 12 H 18 N 2 O 7 302 331 d Anthopleura elegantissima 102,120 9064_ch15/fm Page 488 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC Chemical Defenses of Marine Organisms Against Solar Radiation Exposure 489 Palythinol PL C 13 H 22 N 2 O 6 302 332 43500 75,85 Palythoa tuberculosa 75,85 Z-palythenic acid PA C 14 H 20 N 2 O 7 328 337 29200 92 Halocynthia roretzi 92 E-palythenic acid C 14 H 20 N 2 O 7 328 337 29200 206 Halocynthia roretzi 206 Shinorine (mytilin A) SH C 13 H 20 N 2 O 8 332 334 44668 87 Chondrus yendoi 87 Mytilus galloprovincialis 74 Mycosporine-glycine:valine MV C 15 H 24 N 2 O 7 344 335 Euphausia superba 107 Porphyra-334 (mytilin B) PR C 14 H 22 N 2 O 8 346 334 42300 86 Porphyra tenera 86 Mytilus galloprovincialis 74 Palythine-serine-sulfate SS C 11 H 18 N 2 O 9 S 354 321 Stylophora pistillata 96 Palythine-threonine-sulfate TS C 12 H 20 N 2 O 9 S 368 321 Stylophora pistillata 96 Mycosporine-glutamic acid:glycine GG C 15 H 22 N 2 O 9 374 330 43900 122 Dysidea herbacea 122 Note: Abbreviations used in subsequent tables are shown (Abb.) along with chemical formulae, molecular weights (mw), w avelengths of maximum absorbance (λ max , in nm), extinction coefficients (ε) at λ max or other indicated wavelengths, and species from which original identi fications were made. (Compounds are listed in order of molecular weight.) a at pH < 2. b at pH > 7. c value for mycosporine-glycine methyl ester (ε = 28000) can be substituted. 120 d value for shinorine (ε = 44668) can be substituted. 120 9064_ch15/fm Page 489 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC 490 Marine Chemical Ecology (phenylalanine can be converted into tyrosine by animal metabolism). The dietary requirement for aromatic amino acids probably precludes de novo synthesis of gadusol or MAAs in inverte- brates and chordates. 101 It has been proposed that ingested MAAs could serve as precursors for conversion to gadusol and can be interconverted into different MAAs by animal metabolism or enteric bacteria. 14,101–103 If MAAs are synthesized via the shikimate pathway, then in the marine environment they would be produced by bacteria and primary producers (algae) and transferred by ingestion/assimilation to consumer organisms. It has been demonstrated that diet can regulate MAA content in invertebrates and fish. 104–106 The first direct evidence of this was obtained from controlled feeding experiments with the temperate sea urchin Strongylocentrotus droebachiensis. 104 Furthermore, the assimilation of MAAs from food sources can be very efficient. In medaka fish, the MAA concentrations in ocular tissues increase by nearly 800% over a 5-month period by providing fish with a MAA- enriched diet. 106 MAA acquisition by ingestion/assimilation and not de novo synthesis in consumer organisms is further supported by observed gradients of MAAs along the digestive tract of sea urchins. In Strongylocentrotus droebachiensis, the posterior portion of the gut has over three times the concentration of MAAs as the anterior portion of the digestive tract, indicating sequential absorp- tion of ingested material. 104 Similar observations have been made in holothuroid species. 102 FIGURE 15.4 Molecular structures and wavelengths of maximum absorbance (λ max ) for 12 glycine-contain- ing iminomycosporines from marine organisms. N OCH 3 NH COOH HO HO HO N OCH 3 NH COOH HO HO COOH H 3 C COOH N OCH 3 NH COOH HO HO COOH N OCH 3 NH COOH HO HO H 3 C COOH H 3 C N OCH 3 NH COOH HO HO COOH HOOC N OCH 3 NH COOH HO HO H 3 C N OCH 3 NH COOH HO HO HO CH 3 N OCH 3 NH COOH HO HO HO N H 3 C OCH 3 NH COOH HO HO COOH N CH 3 OCH 3 NH COOH HO HO COOH NH OCH 3 NH COOH HO HO N H 3 C OCH 3 NH COOH HO HO HO mycosporine- glutamic acid:glycine λ max = 330 nm shinorine λ max = 334 nm porphyra-334 λ max = 334 nm mycosporine-2 glycine λ max = 331 nm mycosprine-glycine:valine λ max = 335 nm asterina-330 λ max = 330 nm usujirene λ max = 357 nm palythinol λ max = 332 nm E -palythenic acid λ max = 337 nm Z -palythenic acid λ max = 337 nm palythine λ max = 320 nm palythene λ max = 360 nm 9064_ch15/fm Page 490 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC [...]... 9064_ch15/fm Page 492 Tuesday, April 24, 2001 5:26 AM 492 Marine Chemical Ecology The majority of marine cyanobacteria, algae, invertebrates, ascidians, and fish probably contain MAAs, as 87% of marine taxa examined have detectable levels (Table 15. 2) Palythine (see Figure 15. 4) is the most common MAA found in marine organisms (61% of all species analyzed), followed by shinorine (57%), mycosporine-glycine... Prochlorophyta152 1 Cyanophyta112,183,207 4 Total 5 Algae Bacillariophyta46, 115, 124–126,171 28 Chlorophyta77,105,107,110,112,171,195 21 Dinophyta31, 115, 119,129,138 ,153 ,171, 9 172,195 Haptophyta171 2 Phaeophyta77,107,110,112,195 28 2 Rhodophyta69,77,86,87,104,105,107, 48 110–112,123,141,142,167,195,205 Total 138 Invertebrates Annelida107 © 2001 by CRC Press LLC 6 Marine Chemical Ecology Raphidophyta 115 9064_ch15/fm... species containing a specific MAA (see Table 15. 1 for key to MAA acronyms), and number and percent of species containing any MAAs (∑) are shown Marine Chemical Ecology © 2001 by CRC Press LLC 9064_ch15/fm Page 496 Tuesday, April 24, 2001 5:26 AM 496 TABLE 15. 3 Regional Distribution of MAAs 9064_ch15/fm Page 497 Tuesday, April 24, 2001 5:26 AM Chemical Defenses of Marine Organisms Against Solar Radiation... phytoplankton.124,126,128 There have been a few tentative identifications of mycosporine-glycine:valine in organisms from © 2001 by CRC Press LLC 9064_ch15/fm Page 498 Tuesday, April 24, 2001 5:26 AM 498 Marine Chemical Ecology TABLE 15. 4 Twenty-Five Maxima Reported for MAA Concentrations in Marine Species Species 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 Diphora strigosa112 Montastrea cavernosa112... Takeda, D., and Matsunaga, T., UV-A-induced expression of GroEL in the UV-A-resistant marine cyanobacterium Oscillatoria sp NKBG 091600, Microbiol., 145, 949, 1999 54 Wachi, Y., Burgess, J G., Iwamoto, K., Yamada, N., Nakamura, N., and Matsunaga, T., Effect of ultraviolet-A (UV-A) light on growth, photosynthetic activity and production of biopterin glucoside by the marine UV-A resistant cyanobacterium Oscillatoria... mycosporine-glycine and palythine, not shinorine, porphyra-334 or palythinol Individual MAAs have waveband-specific responses Observed changes in palythine and palythene, not asterina-330 Observed changes in palythine, not mycosporine-glycine Observed changes in palythene and palythinol, not mycosporine-glycine Observed changes in asterina-330 and shinorine, not palythine © 2001 by CRC Press LLC 9064_ch15/fm... Garcia-Pichel, F., UV-absorbing mycosporine-like compounds in planktonic and benthic organisms from a high-mountain lake, Arch Hydrobiol., 144, 255, 1999 131 Xiong, F., Kopecky, J., and Nedbal, L., The occurrence of UV-B absorbing mycosporine-like amino acids in freshwater and terrestrial microalgae (Chlorophyta), Aquat Bot., 63, 37, 1999 132 Garcia-Pichel, F and Castenholz, R W., Occurrence of UV-absorbing,... Hawaii Institute of Marine Biology, Technical Report 41, Sea Grant Publication UNIHI-SEAGRANT-CR-9 5-0 3, 1995 45 Bingham, B L and Reyns, N., Ultraviolet radiation and distribution of the solitary ascidian Corella inflata (Huntsman), Biol Bull., 196, 94, 1999 46 Davidson, A T., Bramich, D., Marchant, H J., and Mcminn, A., Effects of UV-B irradiation on growth and survival of Antarctic marine diatoms, Mar... detectable levels of MAAs (Table 15. 3) Palythine, shinorine, porphyra-334, mycosporine-glycine, asterina-330, palythinol, palythene, and mycosporine-2-glycine have been found at all latitudes Other MAAs are less frequently reported and have more limited distributions; however, this may be a function of insufficient data and not a true representation of MAA occurrence Tropical marine organisms are not only... Lett., 22, 3001, 1981 © 2001 by CRC Press LLC 9064_ch15/fm Page 515 Tuesday, April 24, 2001 5:26 AM Chemical Defenses of Marine Organisms Against Solar Radiation Exposure 515 93 Grant, P T., Middleton, C., Plack, P A., and Thomson, R H., The isolation of four aminocyclohexenimines (mycosporines) and a structurally related derivative of cyclohexane-1:3-dione (gadusol) from the brine shrimp, Artemia, Comp . expected. Related UV-absorbing compounds found in marine organisms are gadusol (1,4,5-trihydroxy- 5-hydroxymethyl-2-methoxycyclohex-1-en-3-one) and deoxy-gadusol (Figure 15. 6). 97–99 Gadusol is. nm SO 3 H 9064_ch15/fm Page 487 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC 488 Marine Chemical Ecology TABLE 15. 1 Chemical and Optical Characteristics of Deoxy-Gadusol, Gadusol,. 10 0.1 1 10 100 0 5 10 15 20 25 30 depth (m) depth (m) UV ( W cm -2 ) A B 9064_ch15/fm Page 483 Tuesday, April 24, 2001 5:26 AM © 2001 by CRC Press LLC 484 Marine Chemical Ecology C. B IOLOGICAL