A new lysozyme from the eastern oyster, Crassostrea virginica, and a possible evolutionary pathway for i-type lysozymes in bivalves from host defense to digestion

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Xue, Qinggang ^a   Hellberg, Michael E ^b   Schey, Kevin L ^c,d   Itoh, Naoki ^a,e   Eytan, Ron I ^b   Cooper, Richard K ^a   La Peyre, Jerome F ^a  

^a LOUISIANA STATE UNIVERSITY AGRICULTURAL CENTER   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d VANDERBILT UNIVERSITY   (United States)

^e TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BIVALVE; CHEMICAL DEFENSE; CHEMICAL PROPERTY; DIGESTION; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GROWTH REGULATOR; IMMUNITY; INHIBITOR; PHYLOGENETICS; PHYSIOLOGICAL RESPONSE; POLYMERASE CHAIN REACTION; PROTEIN;

BACTERIA (MICROORGANISMS); BIVALVIA; CRASSOSTREA VIRGINICA; INVERTEBRATA; MAMMALIA; MOLLUSCA; OSTREIDAE; VERTEBRATA;

COMPLEMENTARY DNA; LYSOZYME;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; GENETIC SELECTION; GENETICS; ISOLATION AND PURIFICATION; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOLECULAR WEIGHT; OYSTER; PHYLOGENY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; CRASSOSTREA; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MURAMIDASE; PHYLOGENY; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 77954552336     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-213     Document Type: Article

References (98)

1. From the discovery of lysozyme to the characterization of several lysozyme families. P Jollès, Lysozymes: model enzymes in biochemistry and biology Basel: Birkhauser Verlag, Jollès P, 1996 3 5
2. The properties of lysozyme and its action on microorganisms. MRJ Salton, Bacteriol Rev 1957 21 82 99 13436356
3. Lysozyme: a chapter of molecular biology. P Jollès, Angew Chem Int Ed Engl 1969 8 227 239 10.1002/anie.196902271 4977569
4. Mechanism of lysozyme. DM Chipman N Sharon, Science 1969 165 454 465 10.1126/science.165.3892.454 4893486
5. Plant lysozymes. JJ Beintema AC Terwisscha van Scheltinga, Lysozymes: model enzymes in biochemistry and biology Basel: Birkhauser Verlag, Jollès P, 1996 75 86
6. Phage lysozymes. J Fastrez, Lysozymes: model enzymes in biochemistry and biology Basel: Birkhauser Verlag, Jollès P, 1996 35 64
7. Bacterial lysozymes. JV Holtje, Lysozymes: model enzymes in biochemistry and biology Basel: Birkhauser Verlag, Jollès P, 1996 65 74
8. Insect lysozymes. D Hultmark, Lysozymes: model enzymes in biochemistry and biology Basel: Birkhauser Verlag, Jollès P, 1996 87 102
9. The ruminant digestive model using bacteria already employed early in evolution by symbiotic mollusks. J Jollès A Fiala-Médioni P Jollès, J Mol Evol 1996 43 525 527 10.1007/BF02337523
10. Adaptive evolution of lysozyme: Changes in amino acid sequence, regulation of expression and gene number. EM Prager, Lysozymes: model enzymes in biochemistry and biology Basel: Birkhauser Verlag, Jollès P, 1996 323 345
11. Common precursor of lysozyme of hen egg-white and bacteriophage T4. BW Matthews MG Grütter WF Anderson SJ Remington, Nature 1981 290 334 335 10.1038/290334a0 7207627
12. Goose lysozyme structure: an evolutionary link between hen and bacteriophage lysozymes? MG Grütter LH Weaver BW Matthews, Nature 1983 303 828 831 10.1038/303828a0 6866082
13. Comparison of goose-type, chicken-type, and phage-type lysozymes illustrates the changes that occur in both amino acid sequence and three-dimensional structure during evolution. LH Weaver MG Grütter SJ Remington TM Gray NW Issacs BW Matthews, J Mol Evol 1985 21 97 111 10.1007/BF02100084
14. Crystal structure of Tapes japonica lysozyme with substrate analogue: structural basis of the catalytic mechanism and manifestation of its chitinase activity accompanied by quaternary structural change. T Goto Y Abe Y Kakuta K Takeshita T Imoto T Ueda, J Biol Chem 2007 282 27459 27467 10.1074/jbc. M704555200 17631496
15. What's new in lysozyme research? P Jollès J Jollès, Mol Cell Biochem 1984 63 165 189 10.1007/BF00285225 6387440
16. Antimicrobial properties of lysozyme in relation to foodborne vegetative bacteria. B Masschalck CW Michiels, Crit Rev Microbiol 2003 29 191 214 10.1080/713610448 14582617
17. Mechanism of the antineoplastic action of lysozyme: evidence for host mediated effects. G Sava V Ceschia S Pacor, Anticancer Res 1989 9 1175 1180 2817798
18. Lysozyme stimulates lymphocyte response to ConA and IL-2 and potentiates 5-fluorouracil action on advanced carcinomas. G Sava S Pacor G Dasic A Bergamo, Anticancer Res 1995 15 1883 1888 8572573
19. Clustering of peptidoglycan recognition protein-SA is required for sensing lysine-type peptidoglycan in insects. JW Park CH Kim JH Kim BR Je KB Roh SJ Kim HH Lee JH Ryu JH Lim BH Oh WJ Lee NC Ha BL Lee, Proc Natl Acad Sci USA 2007 104 6602 6607 10.1073/pnas.0610924104 17409189
20. Lysozyme and RNases as anti-HIV components in beta-core preparations of human chorionic gonadotropin. S Lee-Huang PL Huang Y Sun PL Huang HF Kung DL Blithe HC Chen, Proc Natl Acad Sci USA 1999 96 2678 2681 10.1073/pnas.96.6.2678 10077570
21. Structural and functional modeling of human lysozyme reveals a unique nonapeptide, HL9, with anti-HIV activity. S Lee-Huang V Maiorov PL Huang A Ng HC Lee YT Chang N Kallenbach PL Huang HC Chen, Biochemistry 2005 44 4648 4655 10.1021/bi0477081 15779891
22. The non-enzymatic microbicidal activity of lysozymes. K During P Porsch A Mahn O Brinkmann W Gieffers, FEBS Lett 1999 449 93 100 10.1016/S0014-5793(99) 00405-6 10338111
23. A helix-loop-helix peptide at the upper lip of the active site cleft of lysozyme confers potent antimicrobial activity with membrane permeabilization action. HR Ibrahim U Thomas A Pelligrini, J Biol Chem 2001 276 43767 43774 10.1074/jbc.M106317200 11560930
24. Mouse lysozyme M is important in pulmonary host defense against Klebsiella pneumoniae infection. P Markart TR Korfhagen TE Weaver HT Akinbi, Am J Respir Crit Care Med 2004 169 454 458 10.1164/rccm.200305-669OC 14617511
25. Recombinant destabilase-lysozyme: synthesis de novo in E. coli and action mechanism of the enzyme expressed in Spodoptera frugiperda. LL Zavalova IP Baskova EV Barsova EV Snezhkov SB Akopov SA Lopatin, Biochemistry (Mosc) 2004 69 776 781 10.1023/B:BIRY.0000040203.37624.ef 15310278
26. The interactions of antimicrobial peptides derived from lysozyme with model membrane systems. HN Hunter W Jing DJ Schibli T Trinh IY Park SC Kim HJ Vogel, Biochim Biophys Acta 2005 1668 175 891 10.1016/j.bbamem.2004.12.004 15737328
27. Unravelling the structure of the pneumococcal autolytic lysozyme. B Monterroso C Lápez-Zumel JL García JL Siz P García NE Campillo M Menéndez, Biochem J 2005 391 41 49 10.1042/BJ20050612 15943581
28. The peptidoglycan-degrading property of lysozyme is not required for bactericidal activity in vivo. JA Nash TN Ballard TE Weaver HT Akinbi, J Immunol 2006 177 519 526 16785549
29. Evolutionary derepression of lysozyme. DE Dobson E Dayan AC Wilson, Federation Proceedings 1979 38 674 674
30. Stomach lysozymes of ruminants. I. Distribution and catalytic properties. DE Dobson EM Prager AC Wilson, J Biol Chem 1984 259 11607 11616 6432801
31. Adaptive evolution in the stomach lysozymes of foregut fermenters. JW Stewart CB Schilling AC Wilson, Nature 1987 330 401 404 10.1038/330401a0 3120013
32. Stomach lysozymes of the three-toed sloth (Bradypus variegatus), an arboreal folivore from the Neotropics. MA Pacheco JL Concepcion JDR Rangel MC Ruiz F Michelangeli MG Dominguez-Bello, Comp Biochem Physiol A Mol Integr Physiol 2007 147 808 819 10.1016/j.cbpa.2006.07.010 16959513
33. Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin. JR Kornegay JW Schilling AC Wilson, Mol Biol Evol 1994 11 921 928 7815930
34. A bacteria-digesting midgut-lysozyme from Musca domestica (Diptera) larvae: purification, properties and secretory mechanism. FJA Lemos AF Ribeiro WR Terra, Insect Biochem Mol Biol 1993 23 533 541 10.1016/0965-1748(93)90062-W
35. Insect lysozyme from house fly (Musca domestica) larvae: possible digestive function based on sequence and enzymatic properties. Y Ito M Nakamura T Hotani T Imoto, J Biochem 1995 118 546 551 8690715
36. Lysozyme in the salivary glands of the malaria vector Anopheles darlingi. CK Moreira-Ferro S Daffre AA James O Marinotti, Insect Mol Biol 1998 7 257 264 10.1111/j.1365-2583.1998.00067.x 9662475
37. Purification and characterization of the lysozyme from the gut of the soft tick Ornithodoros moubata. P Kopcek R Vogt L Jindrk C Weise I Safarík, Insect Biochem Mol Biol 1999 29 989 997 10.1016/S0965-1748(99) 00075-2 10560138
38. Molecular cloning of lysozyme-encoding cDNAs expressed in the salivary gland of a wood-feeding termite, Reticulitermes speratus. A Fujita T Minamoto I Shimizu T Abe, Insect Biochem Mol Biol 2002 32 1615 1624 10.1016/S0965-1748(02) 00100-5 12429113
39. Sequence characterization and expression patterns of defensin and lysozyme encoding genes from the gut of the reduviid bug Triatoma brasiliensis. CA Arajo PJ Waniek P Stock C Mayer AM Jansen GA Schaub, Insect Biochem Mol Biol 2006 36 547 560 10.1016/j.ibmb.2006.04.003 16835020
40. Digestive function of lysozyme in synanthropic acaridid mites enables utilization of bacteria as a food source. T Erban J Hubert, Exp Appl Acarol 2008 44 199 212 10.1007/s10493-008-9138-x 18357505
41. Identification and characterization of two novel lysozymes from Rhodnius prolixus, a vector of Chagas disease. RJ Ursic-Bedoya H Nazzari D Cooper O Triana M Wolff C Lowenberger, J Insect Physiol 2008 54 593 603 10.1016/j.jinsphys.2007.12.009 18258253
42. Molecular evolution of ruminant lysozyme. DM Irwin, Lysozymes: model enzymes in biochemistry and biology Basel: Birkhauser Verlag, Jollès P, 1996 347 361
43. Stomach lysozyme gene of the langur monkey - tests for convergence and positive selection. KW Swanson DM Irwin AC Wilson, J Mol Evol 1991 33 418 425 10.1007/BF02103133 1960739
44. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Z Yang, Mol Biol Evol 1998 15 568 573 9580986
45. The lysozyme from Asteria rubens. J Jollès P Jollès, Eur J Biochem 1975 54 19 23 10.1111/j.1432-1033.1975.tb04108.x 1149747
46. The lysozyme of the starfish Asteria rubens. A paradigmatic type i lysozyme. S Bachali X Bailly J Jollès P Jollès JS Deutsch, Eur J Biochem 2004 271 237 242 10.1046/j.1432-1033.2003.03915.x 14717691
47. Degradation of bacteria by Mytilus edulis. TH Birkbeck JG McHenery, Mar Biol 1982 72 7 15 10.1007/BF00393942
48. Lysozyme of the mussel, Mytilus edulis (L.). JG McHenery TH Birkbeck, Mar Biol Lett 1979 1 111 119
49. Lysozyme activity in shellfishes. A Mochizuki M Matsumira, Bull Jpn Soc Sci Fish 1983 49 131 135
50. Distribution of lyzozyme-like activity in 30 bivalve species. JG McHenery JA Allen TH Birkbeck, Comp Biochem Physiol B Biochem Mol Biol 1986 85 581 584 10.1016/0305-0491(86)90051-9
51. Occurrence and characterization of lysozyme in the marine bivalves. K Takahashi K Mori T Nomura, Bull Jpn Soc Sci Fish 1986 52 863 868
52. Amino acid sequences of lysozymes newly purified from invertebrates imply wide distribution of a novel class in the lysozyme family. Y Ito A Yoshikawa T Hotani S Fukuda K Sugimura T Imoto, Eur J Biochem 1999 259 456 461 10.1046/j.1432-1327.1999.00064.x 9914527
53. Protein purification and gene isolation of chlamysin, a cold active lysozyme-like enzyme with antibacterial activity. IW Nilsen K Overbo E Sandsdalen E Sandaker K Sletten M Bjornar, FEBS Lett 1999 464 153 158 10.1016/S0014-5793(99)01693-2 10618496
54. Purification and characterization of lysozyme from brackishwater clam Corbicula japonica. K Miyauchi M Matsumiya A Mochizuki, Nippon Suisan Gakkaishi 2000 66 275 281
55. Multiple invertebrate lysozymes in blue mussel (Mytilus edulis). QM Olsen IW Nilsen K Sletten B Myrnes, Comp Biochem Physiol B Biochem Mol Biol 2003 136 107 115 10.1016/S1096-4959(03)00174-X 12941644
56. Purification and characterization of lysozyme from plasma of the eastern oyster (Crassostrea virginica). QG Xue KL Schey AK Volety FL Chu JF La Peyre, Comp Biochem Physiol B Biochem Mol Biol 2004 139 11 25 10.1016/j.cbpc.2004.05. 011 15364284
57. A new lysozyme from the eastern oyster (Crassostrea virginica) indicates adaptive evolution of i-type lysozymes. QG Xue N Itoh KL Schey YL Li RK Cooper JF La Peyre, Cell Mol Life Sci 2007 64 82 95 10.1007/s00018-006-6386-y 17160350
58. cDNA cloning and tissue expression of plasma lysozyme in the eastern oyster, Crassostrea virginica. N Itoh QG Xue Y Li RK Cooper JF La Peyre, Fish Shellfish Immunol 2007 23 957 968 10.1016/j.fsi.2007.03.006 17703954
59. Evidence for dimerization of lysozyme in alkaline solution. AJ Sophianopoulos KE Vanholde, J Biol Chem 1961 236 C82 PC83 13915232
60. Physical studies of muramidase (lysozyme) 2: pH-dependent dimerization. AJ Sophianopoulos KE Vanholde, J Biol Chem 1964 239 2516 2524 14235529
61. Self-association of muramidase (lysozyme) in solution at 25 degrees, pH 7.0, and I-0.20. RC Deonier JW Williams, Biochemistry 1970 9 4260 4207 10.1021/bi00824a004 5528746
62. Conformation of lysozyme in aqueous solution: effect of ionic strength and protein concentration. OG Hampe, Eur J Biochem 1972 31 32 37 10.1111/j.1432-1033.1972.tb02496.x 4640465
63. Bivalvia - a look at the branches. R Bieler PM Mikkelsen, Zool J Linn Soc 2006 148 223 235 10.1111/j.1096-3642.2006.00255.x (Pubitemid 44748107)
64. A small chimerically bifunctional monomeric protein: Tapes japonica lysozyme. K Takeshita Y Hashimoto T Ueda T Imoto, Cell Mol Life Sci 2003 60 1944 1951 10.1007/s00018-003-3082-z 14523554
65. Presence and characterization of multiple mantle lysozymes in the Pacific oyster, Crassostrea gigas. N Itoh Y Okada KG Takahashi M Osada, Fish Shellfish Immunol 2010 20211734
66. Distribution of multiple peptidoglycan recognition proteins in the tissues of Pacific oyster, Crassostrea gigas. N Itoh KG Takahashi, Comp Biochem Physiol B Biochem Mol Biol 2008 150 409 417 10.1016/j.cbpb.2008.04.011 18538602
67. Rapid evolution of immune proteins in social insects. L Viljakainen JD Evans M Hasselmann O Rueppell S Tingek P Pamilo, Mol Biol Evol 2009 26 1791 1801 10.1093/molbev/msp086 19387012
68. Evolution of function in protein superfamilies, from a structural perspective. AE Todd CA Orengo JM Thornton, J Mol Biol 2001 307 1113 1143 10.1006/jmbi.2001.4513 11286560
69. The gene of chlamysin, a marine invertebrate-type lysozyme, is organized similar to vertebrate but different from invertebrate chicken-type lysozyme genes. IW Nilsen B Myrnes, Gene 2001 269 27 32 10.1016/S0378-1119(01)00457-7 11376934
70. Phylogenetic analysis of invertebrate lysozymes and the evolution of lysozyme function. S Bachali M Jager A Hassanin F Schoentgen P Jollès A Fiala-Medioni JS Deutsch, J Mol Evol 2002 54 652 664 10.1007/s00239-001-0061-6 11965437
71. The primary structures and properties of non-stomach lysozymes of sheep and cow, and implication for functional divergence of lysozyme. Y Ito H Yamada M Nakamura A Yoshikawa T Ueda T Imoto, Eur J Biochem 1993 213 649 658 10.1111/j.1432-1033.1993.tb17805.x 8477739
72. Evolution of cow nonstomach lysozyme genes. DM Irwin, Genome 2004 47 1082 1090 10.1139/g04-075 15644966
73. Episodic evolution in the stomach lysozymes of ruminants. J Jollès P Jollès BH Bowman EM Prager CB Stewart AC Wilson, J Mol Evol 1989 28 528 535 10.1007/BF02602933 2504928
74. Episodic adaptive evolution of primate lysozymes. W Messier CB Stewart, Nature 1997 385 151 154 10.1038/385151a0 8990116
75. Bivalve systematics during the 20th Century. JA Schneider, J Paleontol 2001 75 1119 1127 10.1666/0022-3360(2001)075<1119:BSDTC<2.0.CO;2
76. Diversification and adaptive sequence evolution of Caenorhabditis lysozymes (Nematoda: Rhabditidae). H Schulenburg C Boehnisch, BMC Evol Biol 2008 8 114 10.1186/1471-2148-8-114 18423043
77. The probability of duplicate gene preservation by subfunctionalization. M Lynch A Force, Genetics 2000 154 459 10629003
78. Control of Listeria monocytogenes and Salmonella anatum on the surface of smoked salmon coated with calcium alginate coating containing oyster lysozyme and nisin. S Datta ME Janes QG Xue J Losso JF La Peyre, J Food Sci 2008 73 67 M71 10.1111/j.1750-3841.2007.00633.x 18298738
79. Improved prediction of signal peptides: SignalP 3.0. JD Bendtsen H Nielsen G von Heijne S Brunak, J Mol Biol 2004 340 783 795 10.1016/j.jmb.2004. 05.028 15223320
80. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller, Nucleic Acids Res 1997 25 3389 3402 10.1093/nar/25.17.3389 9254694
81. Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. AA Schäffer L Aravind TL Madden S Shavirin JL Spouge YI Wolf EV Koonin SF Altschul, Nucleic Acids Res 2001 29 2994 3005 10.1093/nar/29.14.2994 11452024
82. Protein identification and analysis tools on the ExPASy Server. E Gasteiger C Hoogland A Gattiker S Duvaud MR Wilkins RD Appel A Bairoch, The proteomics protocols handbook Totowa, NJ: Humana Press, Walker JM, 2005 571 607
83. CLUTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. JD Thompson DG Higgins TJ Gibson, Nucleic Acids Res 1994 22 4673 4680 10.1093/nar/22.22.4673 7984417
84. Alignment uncertainty and genomic analysis. KM Wong MA Suchard JP Huelsenbeck, Science 2008 319 473 47 10.1126/science.1151532 18218900
85. BAli-Phy: simultaneous Bayesian inference of alignment and phylogeny. MA Suchard BD Redelings, Bioinformatics 2006 22 2047 2048 10.1093/bioinformatics/ btl175 16679334
86. Tracer v1.4. A Rambaut AJ Drummond, 2007 http://beast.bio.ed.ac.uk/Tracer
87. The origin of new genes: glimpses from the young and the old. M Long E Betrn K Thornton W Wang, Nat Rev Genetics 2005 4 865 875 10.1038/nrg1204
88. ProtTest: selection of best-fit models of protein evolution. F Abascal R Zardoya D Posada, Bioinformatics 2005 21 2104 2105 10.1093/bioinformatics/bti263 15647292
89. MrBayes 3: Bayesian phylogenetic inference under mixed models. F Ronquist JP Huelsenbeck, Bioinformatics 2003 19 1572 1574 10.1093/bioinformatics/btg180 12912839
90. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. DJ Zwickl, Ph.D. dissertation The University of Texas at Austin 2006 http://garli. googlecode.com
91. Holder. J Sukumaran T Mark, DendroPy Phylogenetic Computing Library Version 3.0.0 2009 http://packages.python.org/DendroPy
92. Statistical methods for detecting molecular adaptation. Z Yang JP Bielawski, Trends Ecol Evol 2000 15 496 503 10.1016/S0169-5347(00)01994-7 11114436
93. Codon-substitution models for detecting adaptation at individuals sites along specific lineages. Z Yang R Nielsen, Mol Biol Evol 2002 19 908 917 12032247
94. PAML 4: phylogenetic analysis by maximum likelihood. Z Yang, Mol Biol Evol 2007 24 1586 1591 10.1093/molbev/msm088 17483113
95. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. M Anisimova JP Bielawski Z Yang, Mol Biol Evol 2001 18 1585 1592 11470850
96. Cloning of cDNAs and hybridization analysis of lysozymes from two oyster species, Crassostrea gigas and Ostrea edulis. T Matsumoto AM Nakamura KG Takahashi, Comp Biochem Physiol B Biochem Mol Biol 2006 145 325 330 10.1016/j.cbpb.2006.08.003 16996284
97. cDNA cloning and in situ hybridization of a novel lysozyme in the Pacific oyster, Crassostrea gigas. N Itoh KG Takahashi, Comp Biochem Physiol B Biochem Mol Biol 2007 148 160 166 10.1016/j.cbpb.2007.05.005 17584512
98. Genes from the medicinal leech (Hirudo medicinalis) coding for unusual enzymes that specifically cleave endo-epsilon (gamma-Glu)-Lys isopeptide bonds and help to dissolve blood clots. L Zavalova S Lukyanov I Baskova E Snezhkov S Akopov S Berezhnoy E Bogdanova E Barsova ED Sverdlov, Mol Gen Genet 1996 253 20 25 10.1007/s004380050291 9003282