Photoprotection by carotenoids

Carotenoid pigments have been found to have a protective function against photosensitization in green plants. This protective ability has been exploited in the administration of high doses of beta-carotene to patients with erythropoietic protoporphyria to ameliorate the photosensitivity associated with this disease. The carotenoids seem to exert their light-protective function by quenching excited species such as singlet oxygen and free radicals.     

Carotenoid oxygenases: cleave it or leave it

Carotenoid cleavage products (apocarotenoids) are widespread in living organisms and exert key biological functions. In animals, retinoids function as vitamins, visual pigments and signalling molecules. In plants, apocarotenoids play roles as hormones, pigments, flavours, aromas and defence compounds. The first step in their biosynthesis is the oxidative cleavage of a carotenoid catalysed by a non-heme iron oxygenase. A novel family of enzymes, which can cleave different carotenoids at different positions, has been characterized.     

Dietary carotenoids predict plumage coloration in wild house finches

Carotenoid pigments are a widespread source of ornamental coloration in vertebrates and expression of carotenoid-based colour displays has been shown to serve as an important criterion in female mate choice in birds and fishes. Unlike other integumentary pigments, carotenoids cannot be synthesized; they must be ingested. Carotenoid-based coloration is condition-dependent and has been shown to be affected by both parasites and nutritional condition. A controversial hypothesis is that the expression of carotenoid-based coloration in wild vertebrates is also affected by the amount and types of carotenoid pigments that are ingested. We tested this carotenoid-limitation hypothesis by sampling the gut contents of moulting house finches and comparing the concentration of carotenoid pigments in their gut contents with the colour of growing feathers. We found a positive association: males that ingested food with a higher concentration of carotenoid pigments grew brighter ornamental plumage. We also compared the concentration of carotenoids in the gut contents of males from two subspecies of house finches with small and large patches of carotenoid-based coloration. Consistent with the hypothesis that carotenoid access drives the evolution of carotenoid-based colour displays, males from the population with limited ornamentation had much lower concentrations of carotenoids in their gut contents than males from the population with extensive ornamentation. These observations support the idea that carotenoid intake plays a part in determining the plumage brightness of male house finches.     

Carotenoid pigments and the selectivity of psittacofulvin-based coloration systems in parrots

Carotenoid pigments are commonly used as colorants of feathers and bare parts by birds. However, parrots (Aves: Psittaciformes) use a novel class of plumage pigments (called psittacofulvins) that, like carotenoids, are lipid-soluble and red, orange, or yellow in color. To begin to understand how and why parrots use these pigments and not carotenoids in their feathers, we must first describe the distribution of these two types of pigments in the diet, tissues, and fluids of these birds. Here, we studied the carotenoid content of blood in five species of parrots with red in their plumage to see if they show the physiological ability to accumulate carotenoids in the body. Although Scarlet (Ara macao) and Greenwing Macaws (Ara chloroptera) and Eclectus (Eclectus roratus), African Gray (Psittacus erithacus) and Blue-fronted Amazon (Amazona aestiva) Parrots all use psittacofulvins to color their feathers red, we found that they also circulated high concentrations of both dietary (lutein, zeaxanthin, beta-cryptoxanthin) and metabolically derived (anhydrolutein, dehydrolutein) carotenoids through blood at the time of feather growth, at levels comparable to those found in many other carotenoid-colored birds. These results suggest that parrots have the potential to use carotenoids for plumage pigmentation, but preferentially avoid depositing them in feathers, which is likely under the control of the maturing feather follicle. As there is no evidence of psittacofulvins in parrot blood at the tune of feather growth, we presume that these pigments are locally synthesized by growing feathers within the follicular tissue.     

Carotenogenesis associated with arthrosporulation of Trichophyton mentagrophytes.

Carotenoid pigments were demonstrated in arthrospores of the dermatophyte Trichophyton mentagrophytes but were absent from hyphae and microconidia of this fungus. Incubation at higher temperatures (39 degrees C) allowed arthrosporulation to occur, but essentially no carotenoid was detected in such arthrospores. The carotenoid formation in arthrosporulating T. mentagrophytes did not appear to be either induced or stimulated by light illumination. Mature arthrospores contained the carotenoids phytoene, phytofluene, zeta-carotene, neurosporene, lycopene, and gamma-carotene and a few minor unidentified carotenoids. These carotenoids were localized within intracellular granules consisting of osmiophilic matrices and complex membranous elements. This is the first demonstration of carotenoid pigments in dermatophytic fungi.     

Carotenoids and throat pouch coloration in the great frigatebird (Fregata minor)

Carotenoid pigments are a common source of red, orange, and yellow coloration in vertebrates. Animals cannot manufacture carotenoids and therefore must obtain them in their diet to produce carotenoid-based coloration. Male great frigatebirds (Fregata minor) display a bright red inflated gular pouch as part of their elaborate courtship display. The basis of this coloration until now has not been investigated. Using high-performance liquid chromatography (HPLC), we investigated the types and concentrations of carotenoids that great frigatebirds circulate in their plasma and whether male gular pouch coloration was carotenoid-based. Great frigatebird plasma collected during the breeding season contained three carotenoid pigments in dilute concentrations-tunaxanthin, zeaxanthin, and astaxanthin-with astaxanthin accounting for nearly 85% of the carotenoids present. Astaxanthin was the only carotenoid present in gular pouch tissue, but the concentration is the highest reported for any carotenoid-pigmented avian tissue. Throat pouch reflectance curves were measured with a UV-VIS spectrophotometer, revealing a complex pattern of one UV peak (approx. 360 nm), two absorption valleys (approx. 542 and 577 nm), followed by a plateau at approx 630 nm. The reflectance curve suggests a role for additional pigments, in particular hemoglobin, in the production of color in this ornament.     

Laying‐sequence variation in yolk carotenoids and egg characteristics in the red‐winged blackbird Agelaius phoeniceus

In many bird species with asynchronous hatching, smaller, later‐hatched nestlings are out‐competed for food by their larger, earlier‐hatched siblings and therefore suffer increased mortality via starvation. It is thought that female birds can either maintain or reduce the survival disadvantage of later‐hatched nestlings by differentially allocating maternal resources across the eggs of a clutch. Carotenoid pigments are an example of resources that female birds allocate differentially when producing a clutch, but laying sequence patterns for these pigments remain poorly studied in North American songbirds. We examined intraclutch variation in yolk carotenoids and egg metrics in 27 full clutches of red‐winged blackbird Agelaius phoeniceus eggs collected from eight wetlands in central Alberta, Canada. We predicted that carotenoids would decrease across the laying sequence, as in this species, later‐hatched, marginal nestlings suffer greater mortality than earlier‐hatched, core nestlings. We found nine carotenoid pigments in red‐winged blackbird egg yolks, including two that have never been described from avian yolks: α‐doradexanthin and adonirubin. As predicted, concentrations and amounts of most carotenoids decreased across the laying sequence, suggesting that female red‐winged blackbirds depleted their carotenoid resources as they laid more eggs. However, egg mass and yolk mass both increased across the laying sequence, suggesting that female red‐winged blackbirds may use other maternal resources to compensate for the size and survival disadvantage experienced by later‐hatched, marginal nestlings.     

Qualitative and quantitative variations in carotenoid pigments in the ovary and hepatopancreas of Penaeus schmitti during ovarian maturation

Carotenoid pigments of Penaeus schmitti were investigated and identified in the ovaries and hepatopancreas. Their individual variations were measured in these two organs. The relative concentrations of zeaxanthin in hepatopancreas and astaxanthin in ovaries increased during the sexual development. The role of zeaxanthin monoester in carotenoids transfer from hepatopancreas to ovaries during this sexual development is discussed.     

Metabolism of carotenoid pigments in birds

Carotenoid pigments are an important component in the plumage of birds. The metabolic precursors are dietary in origin but many species have the capacity to chemically modify and selectively deposit the pigments. The ensuing plumage patterns are important in communication and identification. The bright yellows, oranges, and reds are due mostly to xanthophylls; keto and hydroxy carotenes. Some are deposited unmodified (e.g., lutein) whereas others are modified chemically (canthaxanthin, astaxanthin). Early workers concentrated on demonstrating that feather carotenoids were derived from the diet and deposited selectively. Progress in defining and solving biological problems depended on advances in chemical and analytical techniques. Subsequent investigation showed that various plumage colormorphs, seasonal plumage changes or colors in common mutant, were due to relatively simple chemical changes in carotenoids but had profound biological consequences. Equally important was the realization that many of these processes were under genetic control. Validation came from feeding studies of flamingos and finches. Recent studies have employed the plumage carotenoids to test hypotheses of genetic divergence, to relate plumage color to environmental process, and to demonstrate the influence of synthetic changes on color. Understanding the processes has advanced with the introduction of high-resolution separation techniques and the ability to determine both conformation and absolute configuration. The next steps will be in the direction of understanding the enzymatic modification, transport, and tissue selectivity of feather carotenoids.     

Antioxidant functions of carotenoids

Carotenoid pigments, including hydrocarbons such as β-carotene or xanthophylls such as lutein and zeaxanthin, are very widely distributed in nature, where they play an important role in protecting cells and organisms against the harmful effects of light, air, and sensitizer pigments. This process has been demonstrated in bacteria, algae, plants, animals, and even in humans in the light-sensitive disease, erythropoietic protoporphyria. The primary mechanism of action of this phenomenon appears to be the ability of carotenoids to quench excited sensitizer molecules as well as quench ¹O₂.

In addition to this protection, and potentially of even greater biological importance, is the fact that carotenoids can also serve as antioxidants under conditions other than photosensitization. This review presents the data available indicating the extent of this important function. Antioxidant action can be documented in both enzymic and nonenzymic systems, and has been reported in subcellular, cellular, and animal studies. In fact, the many reports indicating that carotenoids may possess some anticarcinogenic properties may well be related to their ability to interact with and quench various radical species that can be generated within cells.     

Carotenoid pigments and trophic behaviour of deep-sea shrimps (Crustacea, decapoda, alvinocarididae) from a hydrothermal area of the mid-atlantic ridge

Pigments and trophic behaviour of three species of Alvinocarididae from a Mid-Atlantic hydrothermal site were analysed. Carotenoid pigments are responsible for the more or less marked colouration of these animals. The carotenoid content of whole animals and different tissues were evaluated. Rimicaris exoculata exhibits an increased carotenoid level at the juvenile stage, while Chorocaris chacei and Alvinocaris markensis contain only few traces of pigment. Free and esterified astaxanthin, reported for most pelagic crustaceans, are present in these deep-sea shrimps. The origin of carotenoids of crustaceans living in the aphotic zone is discussed.     

Identification of carotenoid cleavage dioxygenases from Nostoc sp. PCC 7120 with different cleavage activities

Carotenoid cleavage dioxygenases (CCDs) are a class of enzymes that oxidatively cleave carotenoids into apocarotenoids. Dioxygenases have been identified in plants and animals and produce a wide variety of cleavage products. Despite what is known about apocarotenoids in higher organisms, very little is known about apocarotenoids and CCDs in microorganisms. This study surveyed cleavage activities of ten putative carotenoid cleavage dioxygenases from five different cyanobacteria in recombinant Escherichia coli cells producing different carotenoid substrates. Three CCD homologs identified in Nostoc sp. PCC 7120 were purified, and their cleavage activities were investigated. Two of the three enzymes showed cleavage of beta,beta-carotene at the 9,10 and 15,15' positions, respectively. The third enzyme did not cleave full-length carotenoids but cleaved the apocarotenoid beta-apo-8'-carotenal at the 9,10 position. 9,10-Apocarotenoid cleavage specificity has previously not been described. The diversity of carotenoid cleavage activities identified in one cyanobacteria suggests that CCDs not only facilitate the degradation of photosynthetic pigments but generate apocarotenals with yet to be determined biological roles in microorganisms.     

Identification of carotenoids in Erwinia herbicola and in a transformed Escherichia coli strain

The yellow pigments of Erwinia herbicola Eho 10 and of a transformed Escherichia coli LE392 pPL376 have been identified as carotenoids. HPLC separation, spectra and in some cases mass spectroscopy demonstrated the presence of phytoene (15-cis isomer), beta-carotene (all-trans, 9-cis and 15-cis), beta-cryptoxanthin ( = 3-hydroxy beta-carotene), zeaxanthin (3,3'-dihydroxy beta-carotene) and corresponding carotene glycosides. In addition, lycopene and gamma-carotene accumulated in the presence of the inhibitor 2-(4-chlorophenylthio)-triethylamine.HCl. Carotenoid content in the transformed E. coli was two-fold higher than in E. herbicola. The pattern of the carotenoids was similar in the two organisms. Inactivation of the katF gene in E. coli resulted in an 85% lowering of carotenoid formation, as did the addition of 0.5% glucose to the medium. Suppression of carotenoid formation by inactivation of the katF gene lowered, but did not abolish, the protection offered by carotenoids against inactivation by alpha-terthienyl plus near-ultraviolet light (320-400 nm).     

Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata).

Carotenoid-based sexual coloration is the classic example of an honest signal of mate quality. Animals cannot synthesize carotenoid pigments and ultimately depend on dietary sources. Thus, in carotenoid-poor environments, carotenoid coloration may be a direct indicator of foraging ability and an indirect indicator of health and vigour. Carotenoid coloration may also be affected, more directly, by parasites in some species. Carotenoids are not, however, the only conspicuous pigments available to animals. Pteridine pigments, with similar spectral properties, are displayed in the exoskeletons and wings of insects, the irides of birds and the skins of fishes, lizards and amphibians. Unlike carotenoids, pteridines are synthesized de novo by animals. We report that the orange spots that male guppies (Poecilia reticulata) display to females contain red pteridine pigments (drosopterins) in addition to carotenoids. We also examined the relationship between drosopterin production by males and carotenoid availability in the field. The results contrasted sharply with the hypothesis that males use drosopterins to compensate for carotenoid scarcity: males used more, not less, drosopterins in streams with higher carotenoid availability. The positive association between drosopterin use and carotenoid availability could reflect the costs of drosopterin synthesis or it could be a consequence of females preferring a particular pigment ratio or hue. Male guppies appear to use drosopterin pigments in a manner that dilutes, but does not eliminate, the indicator value of carotenoid coloration.     

Carotenoid pigments: their possible role in protecting against photooxidation in eyes and photoreceptor cells

The effect of light on animal tissues is ambivalent. Light is necessary for many functions, e.g. for vision and, as in the flagellate halobacterium, to gain energy. But light is potentially dangerous: it is capable of destroying cells or their components by photooxidation, especially in the presence of sensitizing pigments such as haems and cytochromes, which are ubiquitous in aerobic cells. Several different examples are discussed to show how a compromise is achieved in animal tissues that for functional reasons receive high exposure to light. Carotenoid pigments, present in many eyes and photoreceptors, seem especially suited to protect against the deleterious effects of light because they absorb the dangerous short wavelength part of the light spectrum. In plant tissue, carotenoids are also well known to be capable of 'quenching' photoexcited states of sensitizing pigments and of oxygen, a function that they might have also in animal tissue. A consequence of the considerations is that whenever animal tissues are exposed to higher than usual light levels and/or oxygen pressures cellular damage might occur. Examples are discussed; strategies to circumvent the deleterious effects by photooxidation follow directly from the arguments.     

Differences in carotenoid composition among hymenobacter and related strains support a tree-like model of carotenoid evolution

Carotenoids are structurally diverse pigments of biotechnological interest as natural colorants and in the prevention of human disease. The carotenoids present in 19 strains taxonomically related to the poorly described, nonphotosynthetic bacterial genus Hymenobacter, including 10 novel isolates cultivated from Victoria Upper Glacier, Antarctica, were characterized using high-performance liquid chromatography (HPLC). Nine chemically distinct carotenoids, present in various combinations irresolvable by conventional crude spectrophotometric analyses, were purified by preparative HPLC and characterized using UV-visible light absorption spectroscopy and high-resolution mass spectrometry. All major Hymenobacter carotenoids appear to be derived from a common backbone of 2'-hydroxyflexixanthin and include previously unreported presumptive hexosyl, pentosyl, and methyl derivatives. Their distribution does not, however, correlate perfectly with 16S rRNA gene phylogeny. Carotenoid composition, therefore, may be strain specific and does not follow a strictly homogeneous pattern of vertical evolutionary descent.     

Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration

Carotenoid pigments can directly enhance the immune responsesof vertebrates, and they are used by many animals to createornamental color displays. It has been hypothesized that thesetwo functions of carotenoid pigments are linked: animals musttrade off use of carotenoid pigments for immune function versusornamental display. We tested two key predictions of this hypothesiswith captive American goldfinches, Carduelis tristis, a specieswith extensive carotenoid-based plumage coloration. First, wetested whether the immune systems of male goldfinches are carotenoidlimited during molt by supplying treatment groups with low,approximately normal, or high dietary access to lutein and zeaxanthin.Dietary treatment had a significant effect on plumage and billcolor but not on immunocompetence. We compared the cell-mediatedand humoral immune responses and the course of disease afterinfection for males in the different treatments. We observedno significant effect of the carotenoid content of diet on immuneresponse or disease resistance. Second, we tested whether therewas a positive relationship between immune function and expressionof ornamental coloration by comparing both the pre- and posttreatmentplumage coloration of males to their immune responses. We failedto find the predicted trade-off between ornament display andimmune function. These findings do not support the hypothesisthat songbirds with extensive carotenoid-based plumage displaystrade off the use of carotenoids for ornamentation versus immunefunction.     

Carotenoid pigments in rust fungi: Extraction,separation, quantification and characterisation

Diseases caused by rust fungi represent critical constraints to global plant production. A characteristic feature of rust pathogens is the striking pigments they produce in one or more spore forms, which give them a rusty appearance. Here, we review the literature published to date on the extraction, separation, quantification and characterisation of carotenoid pigments in rust fungi. These pigments are thought to protect rust fungi against UV radiation and oxidative stress, and possibly act as virulence factors. The yellow-orange colour of some rust species is due to carotenoid pigments. Four carotenoids have been found in rust fungi: phytoene, lycopene, γ-carotene and β-carotene, but their relative contributions to biological functions are largely unknown. Different pre-processes and storage of spore materials, as well as different extraction processes, have been applied in a wide range of investigations on rust spore pigments. We find that the value of the current literature on rust carotenoids for taxonomic diagnostics in understanding the evolution of pigment biosynthesis and in assessing their role in pathogenesis is limited. Re-investigation of rust carotenoid composition using modern analytical technologies is therefore critical to further these fields of research. Our review includes detailed guidance on choice of techniques for rust carotenoid experimental analyses.     

Die Hemmung der lichtinduzierten Chlorophyll-, Carotinoid- und Anthocyansynthese durch Äthanol

The Inhibition of the Light Induced Chlorophyll, Carotenoid and Anthocyan Synthesis by Ethanol. It is shown that already low concentrations of ethanol inhibit the light induced formation of pigments (chlorophylls, carotenoids, anthocyanins) in Raphanus-seedlings. The degree of inhibition depends on the ethanol concentration and rises with increasing incubation period. The inhibition of pigment synthesis is reversible, and immediately ceases when ethanol is removed. The formation of chlorophylls and anthocyanin is more repressed than that of carotenoids, and the formation of β-carotene to a higher extent than that of xanthophylls. It is concluded that ethanol inhibits pigment formation by inhibition of protein synthesis. These results indicate that ethanol and other lower alcohols cannot be used for the solubilizing of organic compounds when these are applied to plant tissues.     

Carotenoids bolster immunity during moult in a wild songbird with sexually selected plumage coloration

Carotenoid‐based colours in animals are valuable models for testing theories of sexual selection and life‐history trade‐offs because the pigments used in coloration are chemically tractable in the diet and in the body, where they serve multiple purposes (e.g. health enhancement, photoprotection). An important assumption underlying the hypothesized signalling value of carotenoid coloration is that there is a trade‐off in carotenoid pigment allocation, such that not all individuals can meet the physiological/morphological demands for carotenoids (i.e. carotenoids are limited) and that only those who have abundant supplies or fewer demands become the most colourful. Studies of carotenoid trade‐offs in colourful animals have been limited largely to domesticated species, which may have undergone artificial selection that changed the historical/natural immunomodulatory roles of carotenoids, to young animals lacking carotenoid‐based signals or to species displaying carotenoid‐based skin and bare parts. We studied the health benefits of carotenoids during moult in house finches (Carpodacus mexicanus), which display sexually selected, carotenoid‐based plumage coloration. We manipulated dietary carotenoid availability during both winter (nonmoult) and autumn (moult) in captive males and females and found that carotenoid‐supplemented birds mounted stronger immune responses (to phytohemagglutinin injection and to a bacterial inoculation in blood) than control birds only during moult. This study provides experimental, seasonal support for a fundamental tenet of Lozano's ‘carotenoid trade‐off’ hypothesis and adds to a growing list of animal species that benefit immunologically from ingesting higher dietary carotenoid levels. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 560–572.