STRACT 7. Six crotenoid pigments, -carotene, isozeaxanthin (?), lutein. zeaxanthin, an astaxanthin ester, and astaxanthin were isolated from the bodies and stalk fluid of Pollicipes polymerus, althoughi the proportions differ in each case. 2. Similar extracts of the different developmental stages of ovigerous lamellae showed the presence of the same six carotenoids with the exception of isozeaxanthin. 3. A decline of the amount of astaxanthin ester and lutein and the apparent simultaneous increase of astaxanthin with maturation of the nauplii was observed. 4. Astaxanthin was found to be bound to a lipo-protein in the stalk fluid and ovigerous lamellae but not in the bodies. 5. The presence of protein bound astaxanthin in the lamellae appears to decline with maturation. 0. The involvement of the astaxanthin lipo-protein complex which is stored in the stalk fluid is discussed. 78 INTRODUCTION Much of the investigation concerning the pigmentation of the Crustacea has been centered on the decapods although some recert investigations have been made on species of both copepods (Herring, 1967) and isopods (Lee, 1966a & b). In the majority of these studies astaxanthin (4-4'-di-keto, 3-3'-di-hydroxy/-carotene) has been found to be very abundant and more or less characteristic of the class. Furthermore, the presence of astaxanthin in the form of protein complexes has been shown to be frequently linked to rø¬ productive and developmental processes (Cheesman, et al, 1966). Some research on the pigmentation of stalked barnacles (Class Cirripedia) has been carried out by Ball (1911) and Fox and Crozier (1967). Ball's study revealed that the blue pigment in the ovaries and developing embryos of Lepas fascicularis is a carotenoprotein with astaxanthin attached to euglobuin. Fox and Crozier discovered that a similar blue color found in the body of L. fascicularis is likewise the result of an astaxanthin protein complex. These two complexes are typical carotenoproteins, both showing absorption maxima as a broad band at about 600mu. [Cheesman, et al, 1966). Furthermore, in Ball's study the developing nauplii were found to change color from blue to pink, reprèsenting the liberation of astaxanthin from the protein complex. Green (1965) has suggested that this breakdown of the carotenoprotein during development, a process commonly seen to occur in crustaceans, may coincide with the peak of proteinase activity and thus represent a mechanism during development by which protein stores can be re¬ leased to the embryos at specific stages of development. The present investigation of Pollicipes polymerus was prompted by the similarity of this barnacle's bright orange stalk fluid to 78 -2- ovarian tissue suggesting the presence of a carotenoprotein which might be involved in the devolopment of the nauplii, perhaps in a manner similar to that described above. The ovigerous lamellae, moreover, were observed to change color during development from a bright orange, similar to that of the stalk fluid, to yellow and then brown, further suggesting such a relationship. The present study is an an invetigation of the carotenoids and carotenoproteins present in both adult and immature barnacles. their stalk fluid, and various stages of the ovigerous lamellae. MATERTALS AND METHODS Animals Barnacles were collected both at The Hopkins Marine Station. Pacific Grove, California and approximately one quarter mile south of the mouth of Malpaso Creek near Yankee Point along California Highway Wl. They were either brought back to the laboratory and stored in a deep freezer at -7°0 until needed or the ovigerous la¬ mellae were dissected in the field and frozen as soon as'possible. The stalk fluid was collected by cutting whole clumps of barnacles from the rocks and allowing the stalks to drain. The material was then centrifuged before being used. xtraction of Carotenoids The carotenoids were extracted from the bodies, ovigerous lamellae, and stalk fluid with acetone. Petroleum ether (b.p. 20-10°0) was added and the carotenoids transferred to the petroleum ether phase by the addition of water. The petroleum ether solu- tion was repeatedly washed with water until free of acetone, dried with anhydrous sodium sulfate and concentrated under a stream of nitrogen. The carotenoids were initially seperated chromatographically on collunns of aluminum oxide (Woelm neutral - activity grade 1 for chromatography, Eschwege, Deutschland). The aluminum ogide was activated by exposure to 11000 for one hour in an oven prior to packing the columns. The columns, which were of two sizes. measured approrimately l om x 15 cm and 1.5 om x 17 cm, respectively. Figments were placed on the columns in petroleum ether and developed with acetone-petroleum ether mixtures of different proportions. The resulting bands were eluted and transfered again to petroleum ether. Further purification was carried out on columms containing 75 a mixture of magnesium oxide and "celite" (1:1 w/w). These columns were likewise developed with acetone-petroleum ether mixtures. Pigment Identification In all cases it was necessary to confirm results by comparing samples of known carotenoids (kindly supplied by Professor B.C.L. Weedon, University of London) with the extracted pigments by means of thin layer chromatography. Shandon equipment was used through- out and the plates were spread with aluminum oxide (Aluminiumoxid G-nach Stahl, E. Merck AG., Darmstadt, Deutschland) to a depth of 200mu. The plates were developed in one of four acetone-petroleum ether mixtures: 5% for carcenes, and 253, 302, and 50% for the di¬ keto and di-hydroxy derivatives. It shoud be noted that the recorded Re values can be considered as valid for individual plates only, since identical conditions from plate to plate were not possible even under the most careful conditions. Saponification was carried out by dissolving the pigments in a 12% solution of KOH in methanol, followed by incubation in the dark at room temperature overnight. After saponification the pigments were re-extracted with petroleum ether. The chromatographic and partition characteristics were recorded and the absorption maxima of the extracted pigments determined in petroleum ether, diethyl ether and carbon disulfide. A Beckman DK2A Ratio Recording Spectophotometer was utilized for all such recordings. Quantitative determinations were based on the extinction at the wavelength of maximum absorbance in solutions of a given volume. The relative amount of each pigment is given as a percentage of the total. It should be noted that these values are only approxi- 76 -5- mations as no allowances were made for differences in molar extinction. Protein Complex Protein complexes were extracted from the body, stalk fluid. and ovigerous lamellae with O.2M phosphate buffer pH7 (KH.PO. 4 NaghPo). The extracted protein complex was then precipitated with saturated ammonium sulfate, centrifuged, redissolved in dis- illed water, and placed on columns of DEAE-cellulose (Whatman DE 50). The proteins were then eluted by stepwise increase in the ionic concentration of the perfusing buffer. The DEAE-cellulose was prepared by first washing with normal NaoH, then distilled water, normal Hol and finally again with distilled water. Columns were prepared by packing a slurry of the purified exchange medium in distilled water. The columns measured approximately 1.5 x 20 cm and were thoroughly washed with 0.2M phosphate buffer, pH/, followed by distilled water before the protein solutions were added. Lipid Identification Tentative identification of the class of lipids present in the stalk fluid was carried out according to the method of Bloor (cf. Mangold, 1962). 10 parts of stalk fluid was extracted with 20 parts of ethanol-diethyl ether (3 to 1) for 24 hours, concentrated under nitrogen and plated on thin layer plates of Silica Gel G (E. Merck AG, Darmstadt, Deutschland) spread to a depth of 200u. The plates were developed with a mixture of petroleum ether, diethyl ether, acetic acid (90:10:1 v/v). The lipids were detected with a 0.05% solution of Rhodamine B in 96% ethanol under U.V. light as dark violet spots on a pink background. o RESUI Bodies of Mature Adults The bodies were dissected from the calcarious plates and ex¬ tracted and the pigments separated as outlined above. A total of six carotenoid pigments were isolated (Fig 1). These were O-caro- tene, isozeaxanthin, lutein, zeaxanthin, an, astaxanthin ester. and astaxanthin. The specific characteristics of these pigments are given below (Table 1). Fraction 7,/-carotene. Fraction 1 elutes from alumina with 1-23 acetone in petroleum ether as a yellow band. It is epiphasic when partitioned between both 90% and 95% methanol and petroleum ether. The absorption spectrum in petroleum ether (119-176mu) is in close agreement with those reported for /-carotene. (Goodwin, 1951) Fraction ! is inseparable from known samples of/-carotene when co-chromatographed on thin layer plates of alumina. On such chromatographs (using 5% acetone in petroleum ether as the solvent nixture) both show Re values of 0.98. Fraction 2, Isozeaxanthin (l-l'-dihydroxy-B-carotene) ? ? Fraction 2 eluted from alumina as a yellow band with 30% acetone in petroleum ether, slightly ahead of Fraction 3. However, it was seperable from Fraction 3 on columns of MgO-celite and on such columns could be eluted with 15% acetone-petroleum ether. It was mostly hypophasic to 90% methanol and completely hypophasic to 958 methanol both before and after saponification. When this fraction was plated gainst a known standard of isozeaxanthin in a 258 acetone-petro- leum ether mixture, the isozeaxanthin (R.-O.82) plated slightly ahead of Fraction 2 (R.-O.79). However, large amounts of lipid present in the sample made identification by thin layer chromato- graphy difficult. The sample exhibited absorption peaks at.llõmu 78 -7- and 472mu in petroleum ether which is close to those recorded for isozeaxanthin (Goodwin, 1954). Iodine catalyzed isomeri¬ zation was carried out according to the method of Zechmeister (cf. Davies, 1965) Under these conditions isozeaxanthin formed a series of five isomers while excess lipid interfered with the results obtained with a similar treatment of the sample solution. The identification of isozeaxanthin, therefore, must remain con- jecture at this time since lackof material prevented further investigation. Fraction 3, Astaxanthin ester. This fraction elutes with isozeaxan- thin from alumina with 30% acetone in petroleum ether as a purple band. It is separable from isozeaxanthin, however, on columns of Ngo-celite by elution with 100% acetone. The ester reveals a single absorption maximum at Lóõmü in petroleum ether. The fraction is 65% hypophasic before saponification and completely hypophasic afterwards. The saponified pigment is inseparable from astaxanthin (Re-O.18) in a solvent mixture of 30% acetone in petroleum ether when co-chromatographed. Fraction 1-Lutein. This pigment together with Fraction 5 eluted slowly from alumina with 70% acetone-petroleum ether as a bright yellow band. However, it was separable from Fraction 5 on Mgo¬ celite and could be eluted from the latter with 153 acetone in petroleum ether. This fraction was hypophasic to 90% and 958 methanol both before and after saponification. The absorption maxima in petroleum ether were ll5mu and 173mu. When co-chro- matographed with a known sample of lutein in 25% acetone-pet- roleum ether as a solvent mixture, the fractions were inseperable (Rg-O.16) 75 -8- Fraction 5 - Zeaxanthin. This pigment elutes with lutein from col- umns of alumina with 70% acetone in petroleum ether. However, when rechromatographed on Mgô-celite it is clearly separable as an orange-yellow band above lutein and can be eluted with 60% acetone¬ petroleum ether. Its absorption maxima in petroleum ether are 5Omu and 176mu. It is completely hypophasic to both 903 and 958 methanol. The pigmenttis inseparable from authentic zeaxanthin but separable from lutein and isozeaxanthin when co-chromatographed in a 25% acetone-petroleum ether solvent mixture. Fraction 6 - Astaxanthin. This fraction elutes from columns of alumina as a purple streak with a 20% mixture of glacial acetic acid in methanol. The pigment was completely hypophasic in both 908 and 958 methanol both before and after saponification. It was insepgrable when co-chromatographed with known astacene. Like- wise, it gave a single absorption maximum in petroleum ether at 170mu which was identical to the spectrum of known aståcene. It should be noted that up to 30 of the pigment was estimated to be lost on the column. Bodies of Immature barnacles Hilgard (1960) in her study of reproduction in the barnacle P. polymerus reported that individuals with a breadth of less than 17.2 mmwere never found to produce ovigerous lamellae. Barnacles smaller than this were collected and the pigments extracted and seperated. When compared to extracts of mature animals, no dif¬ ference could be found in the kinds of carotenoids isolated. Stalk Fluid The dark orange fluid which bathes the ovarian tissue in the stalk was collected and the carotenoids extracted and separated 3 -9- chromatographically. The same six fractions were again present although in different proportions. Ovigerous Lamellae The ovigerous lamellae were collected and divided into three groups representing progressively advanced stages of development. These could be easily denoted by their overt color: bright orange, yellow, or brown. Bright orange lamellae were found to correspond to Barnes' (1965) stages A, B, and C. The yellow lamellae paralleled his D and E stages while the brown lamellae were the same as his stages G and H. Carotenoids were extracted from the three groups and chro¬ matographed as outlined earlier. The pigments isolated were -caro- tene, lutein, zeaxanthin, an astaxanthin ester, and astaxanthin. No astaxanthin was found, possibly due to the small amount of mater- ial available. Quantative Determinations Table 2 lists the relative amounts of the individual carotenoids obtained from the bodies of mature and immature barnacles, stalk fluid, and the three stage of ovigerous lamellae studied. These are represented as a percentage of the total carotenoid content. All the carotenoids originally isolated are present in approx- imately equal amounts in both mature and immature animals. The carotenoids of the stalk fluid are similar to those of the body ex- tracts with the exception of almost negligable amounts of the ester and about 203 more astaxanthin. The early lamellae extracts were similar to those of the mature bodies except for a slightly higher amount of -carotene and the absence of isozeaxanthin. When compared to the earlier lamellar stages the middle and late lamellae exhibit a 10% increase in astaxanthin and a corresponding decrease of about 16%-20% in lutein and the ester. Protein Comple Phosphate buffer extracts of the orange stalk fluid yield an orange water soluble pigment with a single absorption maximum in the visible range at about 170mu (Fig 2). This orange pigment was precipitated with saturated ammonium sulfate and after centrifuga- tion the resulting pellet was redissolved in distilled water and run through a DEAE-cellulose column as outlined earlier. The solution eluted from the column with distilled water but left behind some orange material believed to be lipid in character, which could not be eluted even with the addition of methanol. The material which had eluted still retained some of its original orange color, but upon standing overnight turned yellow. An acetone extract was made which freed the carotenoid with the con- sequent formation of a white flocculent protein precipitate. The carotenoid was transferred to petroleum ether in which it exhibited a single absorption peak at 170 mu. When plated against a known mixture of the carotenoids found in the bodies of adult barnacles (solvent mixture of 25% acetone-petroleum ether), astaxanthin was found to be the only pigment present. The presence of the same astaxanthin protein complex was ver¬ ified in all three stages of ovigerous lamellae by its unique spectral characteristics and by thin layer chromatography. Although no quantitative determinations were carried out the abun- dance of this protein complex appeared to decrease as the lamellae matured. No carotenoprotein was found in the bodies of adults. Lipid Determina! tion When a portion of the phosphate buffer extract of the stalk fluid was mixed with diethyl ether, a yellow pellet formed at the C 0 -11- interface. This and the unusual behavior of this extract suggested the presence of a lipo-protein complex. An initial determination of the class of lipids present in this fluid was carried out as itlined earlier (cf. Mangold, 1962). The thin layer chromatograph of the lipid extract suggested the presence of a single lipid group. saturated hydrocarbons. DISC TON Body This study has shown the presence of six carotenoids in the bodies of mature P. polymerus. Astaxanthin and a single astaxan- thin ester represent about 55% of the total carotenoid component of this species. The only other pigment in substantial quantity is lutein which represents about 31% of the total. This is in general agreement with other studies of crustacean pigments in which astaxanthin and lutein have both been found to be character- istic, the former often amounting to well over one-half the total. For example, in a recent study of the decapod Carcinus maenas Gilchrist and Lee (1967) found that in the epidermis astaxanthin accounted for 56% and lutein represented 212 of the total carotenoid present. It is interesting to compare the results of this study to those obtained by Fox and Crozier (1967) from their work on the body pigmentation of another stalked barnacle, L. fascicularis. They found that carotenes accounted for 24.18 of the total carotenoid while the remaining 75% was astaxanthin. This astaxanthin was, however, in the form of a blue carotenoprotein whereas no carotenoid is protein bound in the bodies of Pollicipes. When the immature bodies of Pollicipes were extracted, no dif- ference in the kind or relative abundance of carotenoids was found. This data suggests that Pollicipes does not metabolize its large amount of astaxanthin from carotene precursors since the presence of possible intermediates was never established as it has been in the case of other crustacea (cf. Lee 1966a; Gilchrist & Lee 1967). Perhaps, though, metabolism in Pollicipes could take place very -13- rapidly in one of the larval stages or at some other specific time so that its occurance would not have been detected in this study. Fluid The characteristics of the stalk fluid and its contained protein-complex in particular are extremely unusual. When freshly collected the fluid is a dark orange with absorption character- istics similar to those expected for the unbound carotenoid, but upon standing overnight it turns yellow with a concomitant loss of absorption in much of the visible range (Fig 2). The same carotenoids present in the body are also found here except that the astaxanthin is bound in some way to what appears to be a lipo- protein. Although all six carotenoids were precipitated from the fluid by the addition of ammonium sulfate only astaxanthin was eluted from a DEAE-cellulose column suggesting that it alone is truly bound to protein. Numerous theories concerning the possible roles of caroteno- protein in invertebrates have been suggested (Cheesman, et al, 1966). Among these are, stabilization of the protein configuration, pro- tective coloration against solar radiation, and protective color- ation as a method of concealment. Protein stabilization seems unlikely in polymerus because the fluid appears to be highly un- stable. Since the fluid is completely bounded by a thick black epidermis, it could not possibly provide protection either against solar radiation or predation. Lipo-protein complexes which have been noted in the blood of many invertebrates may be involved in the transport of carotenoids. since linkage to a protein makes fat soluble carotenoids water soluble (Cheesman, et al 1966). A carotenoid attached to a lipo-protein -14- could possibly mediate the transport of large water soluble molecules across lipid bound membranes. Such properties could be important at the onset of reproduction when the bransfer of critical supplies for egg production is essential. That a sim- ilar astaxanthin lipo-protein was found in the developing lamellae suggests that the protein bound astaxanthin in the stalk fluid is used in some manner by the nauplii during maturation. Polymerus' stalk fluid thus appears to act as a store of this as- taxanthin lipo-protein complex for use during reproduction. A change in the relative amounts of carotenoid pigments during development was observed. The percentages of %-carotene and zea- xanthin seemed to remain roughly the same throughout development. No isozeax ithin was detected. Both lutein and the astaxanthin ester, however, showed a relative decrease in abundance in the late stages of development. It is not known, though, whether this de¬ cline and the increase in free astaxanthin which was also observed are actually related. Thus, although the percentage of non-ester- ilied astaxanthin in the late stages is almost identical with the percentage of astaxanthin bound to the lipo-protein in the stalk fluid, it is uncertain whether or not this represents the direct removal of protein-bound astaxanthin. The possibility of the up- take of astaxanthin derived from the carotenoid lipo-protein complex of the stalk fluid exists, but the most likely source of this free astaxanthin is the breakdown of the lipo-protein complex found in the early stages or de-esterification. That carotenoproteins are broken during some stage of devel- opment is a well known fact. Lwoff (1927) observed the breakage -15- of a blue carotonoprotein in the eggs of the copepod Idya furcata and the resulting transfer of the freed carotenoid to the nauplier eye. Green (1965) also observed a similar process in Cladocera where the carotenoprotein becomes restricted to the embryonic fat cells as soon as they are formed, and once the link with the pro¬ tein is broken the free carotenoid passes into fat droplets. Green speculates that this linkage of protein and carotenoid and its consequent stabilizing effect removes the protein from the possibility of attack by certain enzymes. Furthermore, he suggests that the breakdown of a carotenoprotein may coincide with the peak of proteinase activity. Ball (1941) found that the blue astaxanthin protein complex in Lepas broke at a definite point in the development of the nauplii. A similar series of events apparently occurs in Pollicipes. The percentage of lipo-protein bound astaxanthin likewise appears to decline sharply with advancing development, although not all of the complex is broken when the late stages are reached. The protein complex in polymerus is, furthermore, so unstable that to postulate any stabilization of the protein configuration due to the presence of astaxanthin seems highly improbable. Rather, the enhancement of the movement of water soluble molecules across lipid-bound membranes, the transport of fat soluble carotenoids in an aqueous medium or the stabilization of lipid membrane seem to be the most probable functions of this carotenoid lipo-protein complex. P. polymerus, thus, parallels other invertebrates by the abun- dance of astaxanthin found throughout its body. This astaxanthin, moreover, appears to be taken directly from plant food sources C -16 rather than metabolized from carotene precursors. In the stalk fluid and ovigerous lamellae the astaxanthin is bound to a highly instable lipo-protein which possibly results in some form of en- hanced nutrient transport during development of the ovigerous lamellae. IGURE Carotenoids from mature bodies as they appear on alumina when developed with petroleum ether - acetone mixtures. e percentage of acetone needed to elute each of the pigments is included. Fareron No. C C . . PAMENT ASTAXANTHN ZEAXANTHIN LOTEIN ASTA ZANTMN F51R LSOEFANANTNIN 7) G-eROTENE * ELUTE 2 eton INCOH of nree 70% ACETENE f perevt 30J NCETONE Retrove C 90 TABLE 1 Absorption maxima in petroleum ether, diethyl ether, and carbon disulfide of each of the carotenoids isolated from the mature bodies of P. polymerus. Absorption maxima (mu) Fraction Pigmer Pet. Ether Diethyl Ether Carbon Disulfide 180-510 B-carotene Ll9-176 150-176 177-506 Isozeaxanthin (?) lh6-172 119-177 Astaxanthin 500 Ester 167 168 Lutein 169-501 112-170 Ll5-171 119-176 175-506 Zeaxanthin 150-176 Astaxanthin 172 500 172 p TADLE 2 The relative percentages of the pigments isolated from the mature body, ature body, stalk fluid, early ovigerous lamellae, intermediate lamellae, and late lamellae. mature immature stalk early middle late body pigmer body lamellae lamellae lamellae Ö-carotene 119 68 112 88 10% Isozeaxanthin(?) 19 Astaxanthin Ester 268 258 39 288 208 8% Lutein 3118 32% 20% 338 368 Zeaxanthin 59 112 39 23 38 Astaxanthin 298 319 579 60% 238 339 O IURE 2 Absorption spectrum of (A) the orange stalk fluid of P. polymerus and (B) the redissolved p recipi ated protein complex from this fluid in 0.2M phosphate buffer, pH7. C od 21 ACKNOLELGEME This research was supported in part by a Gail H. Calmerton Scholarship for undergraduates from Stanford University. 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