177. Conchiolin-Constituent Amino Acids and Shell Structures o f Bivalved Shells
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1 800 [Vol. 42, 177. Conchiolin-Constituent Amino Acids and Shell Structures o f Bivalved Shells By Masahiko AKIYAMA Geological and Mineralogical Institute, Tokyo University of Education (Comm. by Hisakatsu YABE, M.J.A., Sept. 12, 1966) Introduction, The shells of calcium carbonate are decalcified in hydrochloric acid or tetrasodium ethylene-diamine tetraacetate solution, leaving the organic materials like agar-agar, which are well known as conchiolin. Because of being insoluble in both the dilute acid or alkaline solutions and any organic solvent it is classified as screloprotein, but can be distinguished. from collagen or keratin consisting of the bone- and tooth-organic matters in amino acid composition. Yasuda and Nakajimal' accomplished paper chromatographic analyses of the amino acids included in several molluscan shells belonging to three different orders and stated that the shells of each order had the characteristic amino acid compositions, respectively. The studies of the conchiolin of Pinctada martensii2' '3' reveal that the amino acid composition in the inner layer of mother of pearl (nacreous) is different from that in the outer layer of prismatic structure. Of late, Hotta4' figured the amino acid composition of conchiolins included in the three bivalved genera, Glycymeris, Patinopecten, and Pinctada, and pointed out the possibility that each species belonging to the same family has a similar amino acid composition of conchiolin and species to the different family different composition. The microscopic studies of shell structure have been carried out by many authors, such as Schmidt, Bz(ggild, Hass, Schenck, and Kado,5' Recently, Kobayashis' has distinguished seven fundamental shellstructural units in pelecypod shells; that is, prismatic, nacreous, foliated, crossed lamellar, complex, homogeneous, and composite prismatic structures, and he has also made clear that all of the shells belonging to pelecypods consist of the outer and inner layers built up by any of the structural units mentioned above and that all apecies of the same family are constructed by the same structural units, those of the different family being by the different ones. Those facts lead us to the presumption that the species peculiarity in amino acid composition of conchiolin depends upon the differences of shell-structural units. The present paper reveals the property of amino acid composi-
2 No. 7] Conchiolin-Constituent Amino Acids and Shell Structures 801 tion of each shell-structural unit distinguished by Kobayashi, of which data are the most fundamental for the research of the conchiolin remnants in fossil bivalved shells. Materials and methods. All shell samples were carefully cleaned to remove any possible surface contamination. The samples were mechanically separated from the fifteen recent pelecypod shells, each one being homogeneous in shell-structural patterns. The amino acids included in the samples of 200 mg were analysed with two dimentional paper chromatography,7' 8' which does not differentiate methionine and phenylalanine from valine and leucines, the f ormers being added to the latters as valine- or leucine-equivalents. Results. As shown in Table I, both the prismatic and nacreous Table I. Total amount of amino acids (Values are given as micrograms of amino from the living bivalved shells acids per 100 milligrams of shell) layers have the highest amino acid content, the crossed lamellar layers the smallest, those of the other four layers being intermediate in amount. In the next, the amino acid composition in each shell-structural layer were investigated. Percentages of each amino acid to total ones of each shell-structural layer are shown in Fig. 1. Prismatic layer. This layer is characterized by the largest
3 802 M. AKIYAMA [Vol. 42, Fig. 1. Comparison of amino acid composition of conchiolin proteins in each shell-structural pattern of bivalved shells (Values are given as weight per cent of amino acids found). 1-A. Prismatic layer. Five line graphs of each amino acid on the abscissa show weight per cent of the amino acid to total ones of Pinctada martensii, Pinna attenuata, Atrina pectinata japonica, Anomia lischkei, and Ostrea gigas from left to right. 1-B. Nacreous layer. Mytilus crassitesta, Pinctada martensii, Pinna attenuata, and Anodonta woodiana from left to right. 1-C. Foliated layer. Chlamys nipponensis, Patinopecten yessoensis, Anomia lischkei, Ostrea denselamellosa and 0, gigas from left to right. 1-D. Crossed lamellar layer. Anadara broughtoni, Corbicula leana, and Mactra venerif ormis from left to right. 1-E. Complex layer. Mactra veneriformis. 1-F. Composite prismatic layer. Meretrix lusoria and Venerupis japonicas from left to right. 1-G. Homogeneous layer. Meretrix lusoria of the left and Venerupis japonicus of the right two.
4 No. 7] Conchiolin-Constituent Amino Acids and Shell Structures 803 amount of glycine of all amino acids, taking 18 to 20 percents in all of the analysed species except for an unusual value of 26 percents in Anomia lischkei. The higher contents of amino acids next to glycine are in leucines, serine, and histidine, taking the values between 10 to 15 percents. Anomia lischkei shows remarkably lesser amount of valine than the other species. Nacreous layer. This layer has the largest amount of alanine of all amino acids, taking 24 percents in all analysed species and contains 17 to 19 percent glycine in almost all species. There is an exception that Pinctada martensii has lesser amount of alanine than glycine. All of the layers as far as the analysed species take a constant value of 13 to 14 percents in valine, showing no difference among the species. Aspartic acid is of low content in all species, taking two percents. Therefore, it is probably concluded that this layer is characterized in having much alanine in the amino acid composition. Foliated layer. This layer has the largest amount of glycine of all amino acids, ranging from 21 to 32 percents. Serine takes a value of 11 to 22 percents, being next to glycine. Leucine content of this layer is lesser than that of the prismatic and nacreous layers, and about five percents of alanine are included in these layers of all species except for Ostrea denselamellosa. Crossed lamellar, composite prismatic, and homogeneous layers. There are no differences in amino acid composition in these three kinds of structural units. Glycine ranges from 10 to 17 percents and lesser amount of alanine is common to all of these structural units of all species except for Mactra veneri f ormis. An unusual amount of proline is there in the crossed lamellar layer of Corbicnla leana. Complex layer. It is regrettable that there is only one analytical datum on the complex layer of Mactra venerif ormis, which is characterized in amino acid composition by the larger amount of leucines (29%) and the lesser amount of glycine (15%). The definite property of this shell-structural unit on amino acid composition should be def erect until several samples belonging to this layer are analysed. Discussion. From the amino acid composition in shells, the shell-structural units are divided into the five groups; that is, prismatic, nacreous, foliated, complex, and crossed lamellar, composite prismatic, and homogeneous layers. It is, therefore, concluded that the property of conchiolin in amino acid composition should not be discussed in defiance of shell-structural patterns. Yasuda and Naka jima1' have found out that the paper chromatographic analysis
5 804 M. AKIYAMA [Vol. 42, of conchiolin included in several shells belonging to Archaeogastropoda, Disodonta, and Heterodonta indicates a constant ratio of alanine to glycine in the order level in taxonomy. Of late, Hare and Abelson9~ have suggested that the primitive shells such as Petrotrochus and Astraea belonging to Archaeogastropoda, Acila and Mytilus to Pelecypoda, and Nautilus to Cephalopoda, have higher content of proteins, in which much alanine and glycine are included. They have also stated that all shells analysed take the different amino acid constituent patterns in the family level, while the constant patterns in the genus level, figuring the amino acid constitutions of the several shells belonging to the three families, P teridae, Pectinidae, and Veneridae. Kobayashi's study6' indicates that all of the shells belonging to P teridae are consisting of prismatic and nacreous layers, all of the shells to Pectinidae are only of foliated layers, and almost of the shells to Veneridae are of composite prismatic and homogeneous layers. The above mentioned facts lead us to the conclusion that the analytical data of Hare and Abelson are being subjected to the shell-structural patterns and the cruxes of their paper may be there in defiance of these patterns. Hare' ' separated the shell of Mytilus californianus into three different structural parts; outer prismatic, nacreous, and inner prismatic layers, and carried out an amino acid analysis of the three layers, respectively, indicating no distinguishing differences between the prismatic and the nacreous layer. On the other hand, the definite differences are there in the content of alanine between the above mentioned two layers in so far as the writer's data shown herein. It is, therefore, necessary to re-examine whether or not the shell of Mytilus call f ornianus consists of the prismatic and nacreous layers in the true sense. After all, it is obvious that the properties of the conchiolin on the amino acid composition should be treated of with regard to the shell-structural patterns, prior to discussing the species peculiarity. Acknowledgement. I am grateful to Drs. Masae Omori, Shoji Ijiri, and Takayo Fujiwara for their kind guidances and encouragements throughout the present work, and also to Dr. Hisakatsu Yabe, M.J.A., for communicating the paper to the Academy. Acknowledgements are due to Dr. Iwao Kobayashi for his suggestions and offering some of the specimens analysed, and to the members of `Fossil Club' and to the staffs of the Geological and Mineralogical Institute, Tokyo University of Education for their valuable critisisms to my work.
6 No. 7] Conchiolin-Constituent Amino Acids and Shell Structures 805 References 1) M. Yasuda and Y. Nakajima: Kassui Rombunshu, 2, 1-4 (1953). 2) S. Tanaka, H. Hatano, and 0. Itasaka: Bull. Chem. Soc. Japan, 33, (4), (1960). 3) S. Tanaka, H. Hatano, and S. Ganno: Rep. Nippon Inst. Sci. Res. Pearl, 74, 1-9 (1963). 4) S. Hotta: Jour. Geol. Soc. Japan, 71, (842), (1965). 5) Y. Kado: Jour. Sci., Hiroshima Univ., 1, (14), (1953). 6) I. Kobayashi: Earth Science, 73, 1-12 (1964). 7) M. Yasuda: Bull. Fac. Fish., Nagasaki Univ., 6, 1-17 (1958). 8) M. Akiyama: Jour. Geol. Soc. Japan, 70, (828), (1964). 9) P. E. Hare and P. H. Abelson: Ann. Rep., Geophys. Lab., Carnegie Inst., Washington, , (1964). 10) P. E. Hare: Science, 139, (3551), (1963). Postscript. When the manuscript had been made up, Hare and Abelson published an interesting paper entitled the "Amino Acid Composition of Some Calcified Proteins", Ann. Rep., Geophy. Lab., Carnegie Inst., Washington, (1965), in which they discussed the comparative biochemistry of conchiolin proteins especially in pelecypod and gastropod shells and revealed the amino acid composition of conchiolin proteins of the nacreous, prismatic, and crossed lamellar layers.
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