CAROTENOID METABOLISM

Decapod crustaceans are well known for accumulating carotenoid pigments in the ovary and eggs in the form of chromoproteins (Zagalsky et al., 1967; Wallace et al., 1967). Carotenoids form two classes by their chemical structure: (1) carotenes that are constituted by carbon and hydrogen; (2) oxycarotenoids or xanthophylls that have carbon, hydrogen, and additionally, oxygen (Isler, 1971).

Astaxanthin is the most commonly identified carotenoid pigment found in conjugation with the lipovitellin, giving it a golden yellow color to the eggs of crabs. Unlike the other carotenoid-protein complexes, in which the carotenoid components are directly linked to protein chains through amino groups, in the eggs of decapod crustaceans, they are dissolved nonstoichiometrically in the lipid prosthetic groups of the lipovitellin (Zagalsky et al., 1967). Additionally, carotenoids can be esterified to the fatty acids of the lipovitellin molecules. The pigments of the eggs are derived from the hemolymph as conjugates of vitellogenin, which is then sequestered into the growing oocytes for final deposition. Changes in the color of the egg mass of decapod crustaceans are an easy index of carotenoid metabolism, as occurring during embryogenesis.

Kour and Subramoniam (1992) investigated the qualitative and quantitative changes in the carotenoids during embryogenesis of a sand crab E. asiatica. Table 10.4 shows the variation in the occurrence of different carotenoids in

TABLE 10.4 Carotenoid Content in Different Egg Developmental Stages of Emerita asiatica (yg/g Wet Weight)

Carotenoid

Species

Stages

I

III

V

VII

VIII

IX

X

a-carotene

0.853 ± 0.056

0.921 ± 0.189

1.490 ± 0.026

0.833 ± 0.013

0.960 ± 0.012

0.031 ± 0.002

-

P-carotene

15.560 ± 0.122

16.072 ± 0.141

15.445 ± 0.087

14.320 ± 0.097

12.220 ± 0.034

7.220 ± 0.034

3.700 ± 0.069

Lutein

2.080 ± 0.067

-

-

-

-

-

-

Echinenone

0.846 ± 0.031

1.960 ± 0.036

3.540 ± 0.036

-

-

-

-

Isozeaxanthin

4.373 ± 0.068

1.500 ± 0.019

3.540 ± 0.039

3.380 ± 0.048

0.031 ± 0.010

-

-

Zeaxanthin

4.034 ± 0.045

-

4.510 ± 0.058

4.093 ± 0.248

-

5.971 ± 0.372

-

Canthaxanthin

-

-

-

2.972 ± 0.323

5.806 ± 0.528

4.613 ± 0.264

2.606 ± 0.264

a-doradexanthin

-

-

-

-

-

-

0.666 ± 0.117

Isocryptoxanthin

6.712 ± 0.198

5.100 ± 0.197

3.910 ± 0.153

3.630 ± 0.161

2.540 ± 0.236

2.136 ± 0.142

2.104 ± 0.173

Free astaxanthin

0.600 ± 0.022

0.216 ± 0.016

0.686 ± 0.034

0.608 ± 0.016

1.192 ± 0.055

2.440 ± 0.100

0.848 ± 0.044

Esterified

astaxanthin

-

-

-

-

-

-

4.280 ± 0.018

Data from Kour, D.V.R., Subramoniam, T., 1992. Carotenoid metabolism during embryonic development of a marine crab, Emerita asiatica (Milne-Edwards). Invertebr. Reprod. Dev. 21 (2), 99-106.

different stages of embryo development. By far, the most abundant form of carotenoid deposited in the developing eggs is в-carotene, with its concentration varying between 15.4 pg/g wet weight and 16.1 pg/g wet weights in the early stages of embryogenesis. After maintaining almost the same level up to stage V, в-carotene concentration declined gradually to reach a low level of 3.7 pg/g wet weight in the newly hatched larvae. a-Carotene also showed a declining trend during embryogenesis. Obviously, these two parent carotenoids of dietary origin undergo bioconversion into more oxidized forms such as hydroxyl and ketocarotenoids. Other pigments such as echinenone and isozeaxanthin occurred mainly in the early stages, whereas zeaxanthin was found in stages I, V, VII, and IX. Canthaxanthin made its appearance only from stage VII onward. While free astaxanthin was observed in all stages, esterified astaxanthin was visualized only in the hatching stage. In spite of these metabolic conversions taking place during embryogenesis, the total carotenoids remained almost same. Based on the initial occurrence of a- and в-carotene, lutein, and astaxanthin, as well as the identification of several intermediate compounds during the course of embryo- genesis, the following pathways have been proposed for carotenoid metabolism in crustacean eggs (Fig. 10.4). Apparently, astaxanthin is the final product of в-carotene metabolism in the crustacean embryos. The highest amount of astax- anthin present in embryogenesis is due to the conversion of dietary pigments such as a- and в carotene. Lutein also contributed to the formation of astaxanthin through several intermediary compounds such as a- and в-doradexanthin. Compounds such as zeaxanthin, echinenone, canthaxanthin, isocryptoxanthin, and isozeaxanthin appear during the formation of astaxanthin from в-carotene. Esterification of astaxanthin toward the last stage of embryonic development is associated with the origin of chromatophores and the possible biosynthesis of visual pigments.

In a freshwater crayfish, Astacus leptodactylus, Berticat et al. (2000) studied the carotenoid content in the embryos and followed the metabolic conversions of free astaxanthin and lutein, the latter being predominant in freshwater species. In this crayfish, astaxanthin is noncovalently bound to protein in the vitel- lus, and is freed during yolk utilization. The steady decline of lutein toward the hatching stage is also related to their metabolic conversion into astaxanthin. After giving rise to many intermediate compounds, astaxanthin is esterified at the closing stage of hatching. The appearance of blue and red chromatophores in the later stages of embryonic development is related to the esterified astaxanthin. The appearance of several other compounds such as zeaxanthin, canthax- anthin, echinenone, в-doradexanthin, and a-carotene was detected by HPLC separation. The high amount of astaxanthin in the embryos of A. leptodactylus as well as other decapod crustaceans studied is related to metabolic adaptation of the embryos, developing under endotrophic conditions.

The carotenoids in the freshly laid eggs of the freshwater prawn Mac- robrachium olfersii consist of a-carotene (0.8-6.4 pg/g fresh egg weight), в-carotene (0.13-13.0 pg/g fresh egg weight), and astaxanthin (23.2-38.8 pg/g fresh egg weight), together with a mixture of four unidentified yellow pigments

FIGURE 10.4

(Ribeiro et al., 2001). During stages I, II, and III of embryogenesis, the relative concentrations of a- and p-carotene as well as astaxanthin increased significantly, but their concentration decreased significantly at the latter stages (IV and V).

Zadorozhny et al. (2008) analyzed the qualitative and quantitative changes in the composition of carotenoids at various stages of embryo development in the crab species Chionoecetes opilio, Paralithodes camtschaticus, and P. platypus. Major carotenoids are astaxanthin and p-carotene. The carotenoid content in the early development stages (orange colored) in C. opilio was found to be 22.7 ng, and in P camtschaticus and P platypus (the violet egg) it amounted to 49.2 and 23.3 ng, respectively. At the later development stage (the brown egg), the carotenoid content was decreased to 13.1 ng in C. opilio and to 20.1 ng in P camtschaticus.

Change in carotenoid titers during embryogenesis is a useful metabolic parameter to monitor the development of embryo. Whether total carotenoids increase, decrease, or remain unchanged may reflect underlying biochemical and physiological events and should help to disclose the role of the carotenoids in crustacean embryonic development. The esterified astaxanthin in the juvenile stages of A. leptodactylus could impart protective coloration that could make them less vulnerable to predators (Berticat et al., 2000). In addition, astaxanthin could play a structural role in the stabilization of protein structure and protection from oxidative damage by free radical species (Vershinin and Lukyanova, 1993).

Embryonic metabolism of carotenoid pigments continues into larval stages in decapod crustaceans. Toward the end of embryogenesis, astaxanthin is partly esterified into new compounds and the rest stored as pigmentary source for their larval metabolism. In the shrimp, Penaeus japonicus, the hatched out nonfeeding larva relies on astaxanthin precursors for further metabolism (Petit et al., 1991). However, the pigmentary composition changes in the next zoea and mysis stages, when it starts feeding on microalgae and then Artemia nauplius larva. In A. salina, cis-canthaxanthin was found exclusively in the ovaries, and eggs (Nelis et al., 1988). cis-Canthaxanthin disappeared progressively during the nauplius stage and was isomerized to the all trans-canthaxanthin. When fed to the mysis stage of P. japonicus, canthaxanthin is not converted into astaxan- thin but distributed to all larval tissues in a storage form. In the postlarval stage, these precursor pigments undergo oxidation and esterification. In the P20 stage, most of the astaxanthin is esterified to mono- and diesters, whereas canthaxan- thin is retained as it is.

 
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