Journal of Molecular Evolution

, Volume 42, Issue 5, pp 543–551 | Cite as

Cloning and sequencing analysis of three amylase cDNAs in the shrimpPenaeus vannamei (Crustacea decapoda): evolutionary aspects

  • Alain Van Wormhoudt
  • Daniel Sellos
Articles

Abstract

InPenaeus vannamei, α-amylase is the most important glucosidase and is present as at least two major isoenzymes which have been purified. In order to obtain information on their structure, a hepatopancreas cDNA library constructed in phage lambda-Zap II (Strategene) was screened using a synthetic oligonucleotide based on the amino acid sequence of a V8 staphylococcal protease peptide ofP. vannamei α-amylase. Three clones were selected: AMY SK 37 (EMBL sequence accession number: X 77318) is the most complete of the analyzed clones and was completely sequenced. It contains the complete cDNA sequence coding for one of the major isoenzymes of shrimp amylase. The deduced amino acid sequence shows the existence of a 511-residue-long pre-enzyme containing a highly hydrophobic signal peptide of 16 amino acids. Northern hybridization of total RNA with the amylase cDNA confirms the size of the messenger at around 1,600 bases. AMY SK 28, which contains the complete mature sequence of amylase, belonged to the same family characterized by a common 3′ terminus and presented four amino acid changes. Some other variants of this family were also partially sequenced. AMY SK 20 was found to encode a minor variant of the protein with a different 3′ terminus and 57 amino acid changes.

Phylogenetic analysis established with the conserved amino acid regions of the (β/α) eight-barrel domain and with the total sequence ofP. vannamei showed close evolutionary relationships with mammals (59–63% identity) and with insect α-amylase (52–62% identity). The use of conserved sequences increased the level of similarity but it did not alter the ordering of the groupings. Location of the secondary structure elements confirmed the high level of sequence similarity of shrimp α-amylase with pig α-amylase.

Key words

α-Amylase isoenzymes cDNA nucleotide sequence Invertebrate Crustacea 

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References

  1. Abele LO, Felgenhauer BE (1986) Phylogenetic and phenetic relationships among the lower Decapods. J Crust Biol 6:385–400Google Scholar
  2. Abele LG (1991) Comparison of morphological and molecular phylogeny of the Decapoda. Memoirs of the Queensland Museum 31: 101–108Google Scholar
  3. Boer PM, Hickey DA (1986) The α-amylase gene inDrosophila melanogaster: nucleotide sequence, gene structure and expression. Nucleic Acid Res 14:8399–8411PubMedGoogle Scholar
  4. Burkenroad MD (1963) The evolution of the Eucarida (Crustacea, Eumalacostaca) in relation to fossil record. Tulane Studies Geol 2:3–16Google Scholar
  5. Cisne JL (1974) Trilobites and the origin of arthropods. Science 186: 13–18Google Scholar
  6. Chirgwin JJ, Przbyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologicaly active ribonucleic acid from sources enriched in ribonucleases. Biochemistry 18:5294–5299CrossRefPubMedGoogle Scholar
  7. Davis BT (1964) Disc electrophoresis. II—Method and application to human serum proteins. Ann NY Acad Sci 321:404–428Google Scholar
  8. Dessen P, Fondrat C, Valencien C, Mugnier C (1990) BISANCE: French service for access to biomolecular sequence databases. Comp Appl Biosci 6:355–356PubMedGoogle Scholar
  9. Felgenhauer BE, Abele GL (1983) Phylogenetic relationships among shrimp-like Decapods. In: Schram FR (ed) Crustaceans issue 1: Crustacean phylogeny. AA Balkema, Rotterdam, Netherlands pp 291–311Google Scholar
  10. Glaessner MF (1969) Decapoda. In: Moore RC (ed) Treatise on invertebrate Paleontology. part R, Arthropoda 4, 11 R399–R533. Geological Society of America, Boulder, Colorado and the University of Kansas Press, LawrenceGoogle Scholar
  11. Grossman GL, James AA (1993) The salivary gland of the vector mosquitoAedes aegypti expresses a novel member of the amylase gene family. Insect Mol Biol 1:223–232PubMedGoogle Scholar
  12. Hagenbuchle O, Bovery R, Young RA (1980) Tissue specific expression of mouse α-amylase genes: nucleotide sequence of isoenzyme mRNAs from pancreatic and salivary glands. Cell 21:179–187PubMedGoogle Scholar
  13. Hein J (1990) Unified approach to aligment and phylogenies. In: Doolittle RF (ed) Methods in Enzymology Acad Press NY, 183: 626–644Google Scholar
  14. Hickey DA, Benkel BF, Boer PH, Genest Y, Abukashwa S, Ben David G (1987) Enzyme encoding genes as molecular clocks: the molecular evolution of animal alpha-amylases. J Mol Evol 26:252–256CrossRefPubMedGoogle Scholar
  15. Huang N, Stebbins GL, Rodriguez RL (1992) Classification and evolution of α-amylases in plants. Proc Natl Acad Sci USA 89:7526–7530PubMedGoogle Scholar
  16. Ikeo K, Takahashi K, Gojoborit J (1995) Different evolution histories of Kringle and protease domains in serine proteases: a typical example of domain evolution. J Mol Evol 40:331–334CrossRefPubMedGoogle Scholar
  17. Janecek S (1992) New conserved amino acid region of α-amylase in the third loop of their (β/α)8-barrel domain. Biochem J 288:1069–1075PubMedGoogle Scholar
  18. Janecek S (1994a) Sequence similarities and evolutionary relationships of microbial, plant and α-amylases. Eur J Biochem 224:519–524CrossRefGoogle Scholar
  19. Janecek S (1994b) Parallel β/α-barrels of α-amylase, cyclodextrin, glycosyltransferase and oligo-1-6 glucosidase versus the barrel of β-amylase: evolutionary distance is a reflection of unrelated sequence. Febs Lett 353:119–123CrossRefGoogle Scholar
  20. Jespersen H, McGregor E, Henrissat B, Sierks MR, Svensson B (1993) Starch and glycogen-debranching and branching enzymes: prediction of structural features of the (β/α)8-barrel domain and evolutionary relationships to other amylolytic enzymes. J Prof Chem 12:791–805Google Scholar
  21. Keller P, Kaufman DL, Allan BJ, Williams BL (1971) Isoenzymes of human parotid α-amylases. Biochemistry 10:4867–4874PubMedGoogle Scholar
  22. Kim W, Abele LG (1990) Molecular phylogeny of selected decapod crustaceans based on 18S rRNA nucleotide sequences. J Crust Biol 10:1–13Google Scholar
  23. Kyte J, Doolytle RF (1982) A single method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132CrossRefPubMedGoogle Scholar
  24. Le Moullac G (1995) Adaptation des enzymes digestives à l'alimentation chez la crevettePenaeus vannamei (Crustacea Decapoda). Thèse EPHE, 120 pGoogle Scholar
  25. Levy JN, Gemmil RM, Doane WW (1985) Molecular cloning of alpha-amylase fromDrosophila melanogaster. II Clone organisation and verification. Genetics 11:313–324Google Scholar
  26. McDonald RJ, GreRar MM, Swain WF, Pietet RL, Thomas G, Rutter WJ (1980) Structure of a family of rat amylase genes. Nature 287: 117–122Google Scholar
  27. McGregor EA (1993) Relationships between structure and activity in the α-amylase family of starch metabolising enzymes. Starch 45: 232–237Google Scholar
  28. McKay RM, Baird S, Dove MJ, Errat JA, Gines M, Moranelli F, Nasim A, Willick GE, Yaguchi M (1985) Glucanase gene diversity in prokaryotic and eukaryotic organisms. Biosystems 18:279–292Google Scholar
  29. Nakajima R, Imanaka T, Aiba S (1986) Comparison of amino acid sequences of eleven α-amylases. Appl Microbiol Biotech 23:353–360CrossRefGoogle Scholar
  30. Nakamura Y, Ogama M, Nishida T, Emi M, Kosaki G, Himeno S, Matsubara K (1984) Sequence of cDNAs for human salivary and pancreatic α-amylases. Gene 28:263–270CrossRefPubMedGoogle Scholar
  31. Ovendeen JR, Brasher DJ, White RWG (1992) Mitochondrial analysis of the red rock lobsterJasus edwardsii supports an apparent absence of population subdivision throughout Australasia. Mar Biol 112:319–326Google Scholar
  32. Palumbi SR, Benzie J (1991) Large mitochondrial DNA differences between morphologically similar Penaeid shrimps. Mol Mar Biol Biotech 1:27–34Google Scholar
  33. Pasero L, Mazzei-Pierron Y, Abadie B, Chicheportiche Y, Marchis-Mouren G (1986) Complete amino-acid sequence and location of the five disulfide bridges in porcine b pancreatic α-amylases. Biochim Biophys Acta 869:147–157PubMedGoogle Scholar
  34. Pictet R, McDonald RJ, Swain WF, Grebar MM, Hobart PM, Crawform R, Shen LD, Bell G, Rutter WJ (1981) Differentiation of the pancreas: an analysis of the structure of the amylase and insulin genes. Fortsh Zool B 26:227–245Google Scholar
  35. Raimbaud E, Buleon A, Perez S, Henrissat B (1989) Hydrophobic cluster analysis of the primary sequences of α-amylases. Int J Biol Macromol 2:217–225Google Scholar
  36. Schram FR (1982) The fossil record and evolution of crustacea. In: Abele LG (ed) The biology of crustacea. Acad Press NY, London, 1:241–304Google Scholar
  37. Sellos D, Van-Wormhoudt A (1992) Molecular cloning of a c-DNA that encodes a serine protease with chymotryptic and collagenolytic activities in the hepatopancreas of the shrimpPenaeus vannamei (Crustacea, Decapoda). FEBS Lett 309:219–224CrossRefPubMedGoogle Scholar
  38. Van Wormhoudt A (1980) Régulation d'activité de l'α-amylase à différentes températures d'adaptation et en fonction de l'ablation des pédoncules oculaires et du stade de mue chezPalaemon serratus. Biochem System Ecol 8:193–203Google Scholar
  39. Van Wormhoudt A (1983) Variations immunoquantitatives de l' α-amylase au cours du cycle d'intermue à différences saisons chezPalaemon serratus (Crustacea Decapoda). Mar Biol 74:127–132CrossRefGoogle Scholar
  40. Van Wormhoudt A, Favrel P (1988) Electrophoretic characterization ofPalaemon elegans (Crustacea Decapoda) α-amylase system: study of amylase polymorphism during the intermolt cycle. Comp Biochem Physiol 89B:201–207Google Scholar
  41. Van Wormhoudt A, Bourreau G, Le Moullac G (1995) Amylase polymorphism in Crustacea Decapoda: electrophoretic and immunological studies. Biochem System Ecol 23:139–149Google Scholar
  42. Van Wormhoudt A, Le Moullac G, Klein B, Sellos D (1996) Adjustment of the expression of digestive enzymes to casein level in food inPenaeus vannamei. Br J Nutr 55 (in press)Google Scholar

Copyright information

© Springer-Verlag New York Inc 1996

Authors and Affiliations

  • Alain Van Wormhoudt
    • 1
  • Daniel Sellos
    • 1
  1. 1.Laboratoire de Biologie Marine du Collège de FranceConcarneauFrance

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