Variation in the antiviral and antibacterial activity of abalone Haliotis laevigata, H. rubra and their hybrid in South Australia

Aquaculture

Volumn 315, Issue 3-4, 2011, Pages 242-249

  Dang, Vinh T ^a   Speck, Peter ^a   Doroudi, Mehdi ^b   Smith, Ben ^c   Benkendorff, Kirsten ^d  

^a FLINDERS UNIVERSITY   (Australia)

^b Aquaculture Program   (Australia)

^c Southern Australian Seafoods Pty Ltd   (Australia)

^d SOUTHERN CROSS UNIVERSITY   (Australia)

Author keywords

Abalone ganglioneuritis; Antiviral activity; Haemolymph; Herpes simplex virus type 1; Molluscan immunity; Vibrio harveyi

Indexed keywords

ANTIMICROBIAL ACTIVITY; AQUACULTURE; ASSAY; BACTERIAL DISEASE; COMMERCIAL SPECIES; HYBRID; IDENTIFICATION METHOD; INTRASPECIFIC VARIATION; MORTALITY; POPULATION STRUCTURE; REPRODUCTIVE BEHAVIOR; SNAIL; SPECIES DIVERSITY;

AUSTRALIA; SOUTH AUSTRALIA;

BACTERIA (MICROORGANISMS); GASTROPODA; HALIOTIDAE; HALIOTIS LAEVIGATA; HERPESVIRIDAE; HUMAN HERPESVIRUS 1; VIBRIO HARVEYI;

EID: 79955023803     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2011.03.005     Document Type: Article

References (93)

1. Abdi H. The Bonferonni and Šidák corrections for multiple comparisons. Encyclopedia of Measurement and Statistics 2007, Sage, Thousand Oaks, CA. N.J. Salkind (Ed.).
2. Arzul I., Renault T. Herpesvirus infections in marine bivalves. Virologie 2002, 6:169-174.
3. Arzul I., Renault T., Thebault A., Gerard A. Detection of oyster herpesvirus DNA and proteins in asymptomatic Crassostrea gigas adults. Virus Research 2002, 84:151-160.
4. Austin B., Zhang X.H. Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Letters in Applied Microbiology 2006, 43:119-124.
5. Bachère E., Gueguen Y., Gonzalez M., De Lorgeril J., Garnier J., Romestand B. Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunological Reviews 2004, 198:149-168.
6. Beaumont A.R., Turner G., Wood A.R., Skibinski D.O.F. Hybridisations between Mytilus edulis and Mytilus galloprovincialis and performance of pure species and hybrid veliger larvae at different temperatures. Journal of Experimental Marine Biology and Ecology 2004, 302:177-188.
7. Benkendorff K. Molluscan biological and chemical diversity: secondary metabolites and medicinal resources produced by marine molluscs. Biological Reviews 2010, 85:757-775.
8. Benkendorff K., Bremner J.B., Davis A.R. A putative role for the precursors of Tyrian Purple in the egg masses of the Australian Muricid, Dicathais orbita. Journal of Chemical Ecology 2000, 26:1037-1050.
9. Benkendorff K., Bremner J.B., Davis A.R. Indole derivatives from the egg masses of muricid molluscs. Molecules 2001, 6:70-78.
10. Benkendorff K., Davis A.R., Bremner J.B. Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 molluscs and 4 polychaetes. Journal of Invertebrate Pathology 2001, 78:109-118.
11. Benkendorff K., Davis A.R., Rogers C.N., Bremner J.B. Free fatty acids and sterols in the benthic spawn of aquatic molluscs, and their associated antimicrobial properties. Journal of Experimental Marine Biology and Ecology 2005, 316:29-44.
12. Benzie J.A.H., Kenway M., Ballment E., Frusher S., Trott L. Interspecific hybridization of the tiger prawns Penaeus monodon and Penaeus esculentus. Aquaculture 1995, 133:103-111.
13. Carson J., Higgins M.J., Wilson T.K., Gudkovs N., Bryant T.N. Aquatic animal health subprogram. Vibrios of aquatic animals: development of a national standard diagnostic technology. Final report for project 2001/628 2006, 347. Fisheries Research & Development Corporation, Canberra.
14. Chang P.H., Kuo S.T., Lai S.H., Yang H.S., Ting Y.Y., Hsu C.L., Chen H.C. Herpes-like virus infection causing mortality of cultured abalone Haliotis diversicolor supertexta in Taiwan. Diseases of Aquatic Organisms 2005, 65:23-27.
15. Charlet M., Chernysh S., Philippe H., Hetru C., Hoffmann J., Bulet P. Innate immunity: isolation of several cysteine-rich antimicrobial peptides from the blood of a mollusc, Mytilus edulis. The Journal of Biological Chemistry 1996, 271:21808-21813.
16. Chen J.H., Yang H.Y., Peng S.W., Chen Y.J., Tsai K.Y. Characterisation of abalone (Haliotis diversicolor) hemocytes in vitro. The Biological Bulletin 1996, 31:31-38.
17. Cheng T.C. Bivalves. Invertebrate Blood Cells 1981, 233-299. Academic Press, London. N.A. Ratcliffe, A.F. Rowley (Eds.).
18. Cheng W., Hsiao I.S., Chen J.-C. Effect of ammonia on the immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Fish and Shellfish Immunology 2004, 17:193-202.
19. Cheng W., Hsiao I.S., Chen J.C. Effect of nitrite on immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Diseases of Aquatic Organisms 2004, 60:157-164.
20. Cheng W., Hsiao I.S., Hsu C.H., Chen J.C. Change in water temperature on the immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Fish and Shellfish Immunology 2004, 17:235-243.
21. Cheng W., Juang F.M., Chen J.C. The immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus at different salinity levels. Fish and Shellfish Immunology 2004, 16:295-306.
22. Cheng W., Li C.H., Chen J.C. Effect of dissolved oxygen on the immune response of Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Aquaculture 2004, 232:103-115.
23. Cook P. The current status of abalone farming in South Africa. Journal of Shellfish Research 1998, 17:601-602.
24. Cory A.H., Owen T.C., Barltrop J.A., Cory J.G. Use of an aqueous soluble tetrazolium formazan assay for cell-growth assays in culture. Cancer Communications 1991, 3:207-212.
25. Crane M.S.J., Corbeil S., Colling A., Williams L.M., Wong F., Savin K., Cogan N., Fegan M., Mohammad I., Sunarto A., Handlinger J., Pyecroft S., Douglas M., Murdoch B., Warner S. Development and validation of a real-time (TaqMan) PCR assay for the detection and identification of abalone herpes-like virus (AbHV). 4th FRDC Aquatic Animal Health Subprogram Scientific Conference, Cairns 2009.
26. Dang V.T., Benkendorff K., Speck P. In vitro antiviral activity against herpes simplex virus in abalone Haliotis laevigata. Journal of General Virology 2011, 92:627-637. 10.1099/vir.0.025247-0.
27. Day R., Hooper C., Benkendorff K., Slocombe R., Handlinger J. Investigations on the immunology of stressed abalone. Final report for FRDC project number: 2004/233 2010, Fisheries Research and Development Corporation and The University of Melbourne.
28. De Zoysa M., Kang H.S., Song Y.B., Jee Y., Lee Y.D., Lee J. First report of invertebrate Mx: cloning, characterization and expression analysis of Mx cDNA in disk abalone (Haliotis discus discus). Fish and Shellfish Immunology 2007, 23:86-96.
29. De Zoysa M., Nikapitiya C., Whang I., Lee J.-S., Lee J. Abhisin: a potential antimicrobial peptide derived from histone H2A of disk abalone (Haliotis discus discus). Fish and Shellfish Immunology 2009, 27:639-646.
30. De Zoysa M., Whang I., Lee Y., Lee S., Lee J.-S., Lee J. Defensin from disk abalone Haliotis discus discus: molecular cloning, sequence characterization and immune response against bacterial infection. Fish and Shellfish Immunology 2010, 28:261-266.
31. Defer D., Bourgougnon N., Fleury Y. Detection and partial characterisation of an antimicrobial peptide (littorein) from the marine gastropod Littorina littorea. International Journal of Antimicrobial Agents 2009, 34:188-190.
32. Defer D., Bourgougnon N., Fleury Y. Screening for antibacterial and antiviral activities in three bivalve and two gastropod marine molluscs. Aquaculture 2009, 293:1-7.
33. Duchemin M.B., Fournier M., Auffret M. Seasonal variation of immune parameters in diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg). Aquaculture 2007, 264:73-81.
34. Fegan M., Kvalheim N., Wong F., Mohammad I., Savin K., Lancaster M., Crane M.S.J., Warner M.S. Development of an in situ hybridisation assay for the detection and identification of the abalone herpes-like virus. 4th FRDC Aquatic Animal Health Subprogram Scientific Conference, Cairns 2009.
35. Fleming A.E., Hone P.W. Abalone aquaculture. Aquaculture 1996, 140:1-4.
36. Freeman K. Aquaculture and related biological attributes of abalone species in Australia-a review. Fisheries Research Report 2001, No. 128:48. Fisheries Western Australia.
37. Gestal C., Costa M., Figueras A., Novoa B. Analysis of differentially expressed genes in response to bacterial stimulation in hemocytes of the carpet-shell clam Ruditapes decussatus: identification of new antimicrobial peptides. Gene 2007, 406:134-143.
38. Godoy C., Jerez G. The introduction of abalone in Chile: ten years later. Journal of Shellfish Research 1998, 17:603-605.
39. Gordon H.R., Cook P.A. World abalone supply, markets and pricing: historical, current and future. Journal of Shellfish Research 2001, 20:567-570.
40. Gordon H.R., Cook P.A. World abalone fisheries and aquaculture update: supply and market dynamics 2004, 935-939. National Shellfisheries Association.
41. Gunkel C., Lewbart G.A. Anesthesia and analgesia of invertebrates. Anesthesia and Analgesia in Laboratory Animals 2008, 535-538. Elsevier Science & Technology. R.E. Fish, M.J. Brown, P.J. Danneman, A.Z. Karas (Eds.).
42. Hahn K.O. Handbook of Culture of Abalone and Other Marine Gastropods 1989, CRC Press, Boca Raton, Florida.
43. Handlinger J., Carson J., Donachie L., Gabor L., Taylor D. Bacterial infection in Tasmanian farmed abalone: causes, pathology, farm factors and control options. Proceedings of the 5th Symposium on Diseases in Asian Aquaculture, Australia 2005, 289-300. P. Walker, R. Lester, M.G. Bondad-Reantaso (Eds.).
44. Hochberg Y. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 1988, 75:800-802.
45. Hooper C., Day R., Slocombe R., Handlinger J., Benkendorff K. Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish and Shellfish Immunology 2007, 22:363-379.
46. Hooper C., Hardy-Smith P., Handlinger J. Ganglioneuritis causing high mortalities in farmed Australian abalone (Haliotis laevigata and Haliotis rubra). Australian Veterinary Journal 2007, 85:188-193.
47. Kamenarska Z., Serkedjieva J., Najdenski H., Stefanov K., Tsvetkova I., Dimitrova-Konaklieva S., Popov S. Antibacterial, antiviral, and cytotoxic activities of some red and brown seaweeds from the Black Sea. Botanica Marina 2009, 52:80-86.
48. Lee T.G., Maruyama S. Isolation of HIV-1 protease-inhibiting peptides from thermolysis hydrolysate of osyer proteins. Biochemical and Biophysical Research Communications 1998, 253:604-608.
49. Lee J.B., Hayashi K., Maeda M., Hayashi T. Antiherpetic activities of sulfated polysaccharides from green algae. Planta Medica 2004, 70:813-817.
50. Li C.P. Antimicrobial effect of abalone juice. Proceedings of the Society for Experimental Biology and Medicine 1960, 103:522-524.
51. Li C.P., Prescott B., Jahnes W.G. Antiviral activity of a fraction of abalone juice. Proceedings of the Society for Experimental Biology and Medicine 1962, 109:534-538.
52. Li Y., Qin J.G., Abbott C.A., Li X.X., Benkendorff K. Synergistic impacts of heat shock and spawning on the physiology and immune health of Crassostrea gigas: an explanation for summer mortality in Pacific oysters. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 2007, 293:2353-2362.
53. Li C.H., Zhao J.M., Song L.S. A review of advances in research on marine molluscan antimicrobial peptides and their potential in aquaculture. Molluscan Research 2009, 29:17-26.
54. Li Y., Qin J.G., Li X., Benkendorff K. Monthly variation of condition index, energy reserves and antibacterial activity in Pacific oysters, Crassostrea gigas, in Stansbury (South Australia). Aquaculture 2009, 286:64-71.
55. Li Y., Qin J.G., Li X., Benkendorff K. Spawning-dependent stress response to food deprivation in Pacific oyster Crassostrea gigas. Aquaculture 2009, 286:309-317.
56. Li Y., Qin J.G., Li X., Benkendorff K. Spawning-dependent stress responses in pacific oysters Crassostrea gigas: a simulated bacterial challenge in oysters. Aquaculture 2009, 293:164-171.
57. Li Y., Qin J.G., Li X., Benkendorff K. Assessment of metabolic and immune changes in postspawning Pacific oyster Crassostrea gigas: identification of a critical period of vulnerability after spawning. Aquaculture Research 2010, 41:155-165.
58. Maier M.S., Roccatagliata A.J., Kuriss A., Chludil H., Seldes A.M., Pujol C.A., Damonte E.B. Two new cytotoxic and virucidal trisulfated triterpene glycosides from the antarctic sea cucumber Staurocucumis liouvillei. Journal of Natural Products 2001, 64:732-736.
59. Malham S.K., Lacoste A., Gélébart F., Cueff A., Poulet S.A. Evidence for a direct link between stress and immunity in the mollusc Haliotis tuberculata. Journal of Experimental Zoology Part A: Comparative Experimental Biology 2003, 295A:136-144.
60. Mandal P., Pujol C.A., Carlucci M.J., Chattopadhyay K., Damonte E.B., Ray B. Anti-herpetic activity of a sulfated xylomannan from Scinaia hatei. Phytochemistry 2008, 69:2193-2199.
61. Matozzo V., Marin M. First evidence of gender-related differences in immune parameters of the clam Ruditapes philippinarum (Mollusca, Bivalvia). Marine Biology 2010, 157:1181-1189.
62. Mitta G., Vandenbulcke F., Roch P. Original involvement of antimicrobial peptides in mussel innate immunity. FEBS Letters 2000, 486:185-190.
63. Nicolas J.L., Basuyaux O., Mazurie J., Thebault A. Vibrio carchariae, a pathogen of the abalone Haliotis tuberculata. Diseases of Aquatic Organisms 2002, 50:35-43.
64. Nishimori E., Hasegawa O., Numata T., Wakabayashi H. Vibrio carchariae causes mass mortalities in Japanese abalone, Sulculus diversicolor supratexta. Fish Pathology 1998, 33:495-502.
65. Ohta S., Ono F., Shiomi Y., Nakao T., Aozasa O., Nagate T., Kitamura K., Yamaguchi S., Nishi M., Miyata H. Anti-Herpes Simplex Virus substances produced by the marine green alga, Dunaliella primolecta. Journal of Applied Phycology 1998, 10:349-356.
66. Olicard C., Didier Y., Marty C., Bourgougnon N., Renault T. In vitro research of anti-HSV-1 activity in different extracts from Pacific oysters Crassostrea gigas. Diseases of Aquatic Organisms 2005, 67:141-147.
67. Olicard C., Renault T., Torhy C., Benmansour A., Bourgougnon N. Putative antiviral activity in hemolymph from adult Pacific oysters, Crassostrea gigas. Antiviral Research 2005, 66:147-152.
68. Otero-Gonzalez A.J., Magalhaes B.S., Garcia-Villarino M., Lopez-Abarrategui C., Sousa D.A., Dias S.C., Franco O.L. Antimicrobial peptides from marine invertebrates as a new frontier for microbial infection control. Journal of the Federation of American Societies for Experimental Biology 2010, 24:1320-1334.
69. Ponce N.M.A., Pujol C.A., Damonte E.B., Flores M.L., Stortz C.A. Fucoidans from the brown seaweed Adenocystis utricularis: extraction methods, antiviral activity and structural studies. Carbohydrate Research 2003, 338:153-165.
70. Pouvreau S., Enriquez-Diaz M., Le Souchu P., Connan J.P., Le Roy B., Mingant C., Moal J., Delaporte M., Le Coz J.R., Samain J.F. Reproduction, bioenergetic and summer mortality of Crassostrea gigas: experimental approach. Journal of Shellfish Research 2003, 22:351.
71. Puglisi M., Engel S., Jensen P., Fenical W. Antimicrobial activities of extracts from Indo-Pacific marine plants against marine pathogens and saprophytes. Marine Biology 2007, 150:531-540.
72. Rahman M.A., Uehara T., Lawrence J.M. Growth and heterosis of hybrids of two closely related species of Pacific sea urchins (Genus Echinometra) in Okinawa. Aquaculture 2005, 245:121-133.
73. Reed L.J., Muench H. A simple method of estimating fifty percent endpoints. The American Journal of Hygiene 1938, 27:493-497.
74. Renault T., Lipart C., Arzul I. A herpes-like virus infecting Crassostrea gigas and Ruditapes philippinarum larvae in France. Journal of Fish Diseases 2001, 24:369-376.
75. Roch P., Yang Y., Toubiana M., Aumelas A. NMR structure of mussel mytilin, and antiviral-antibacterial activities of derived synthetic peptides. Developmental and Comparative Immunology 2008, 32:227-238.
76. Russell W.C. A sensitive and precise plaque assay for herpes virus. Nature 1962, 195:1028-1029.
77. Salvador N., Garreta A.G., Lavelli L., Siguán M.A.R. Antimicrobial activity of Iberian macroalgae. Scientia Marina 2007, 71:101-113.
78. Savin K., Cocks B., Wong F., Sawbridge T., Cogan N., Savage D., Warner S. A neurotropic herpesvirus infecting the gastropod, abalone, shares ancestry with oyster herpesvirus and a herpesvirus associated with the amphioxus genome. Virology Journal 2010, 7:308.
79. Smit A.J. Medicinal and pharmaceutical uses of seaweed natural products: a review. Journal of Applied Phycology 2004, 16:245-262.
80. Soletchnik P., Faury N., Goulletquer P. Seasonal changes in carbohydrate metabolism and its relationship with summer mortality of Pacific oyster Crassostrea gigas (Thunberg) in Marennes-Oléron bay (France). Aquaculture 2006, 252:328-338.
81. Speck P.G., Simmons A. Divergent molecular pathways of productive and latent infection with a virulent strain of herpes simplex virus type 1. Journal of Virology 1991, 65:4001-4005.
82. Speck P.G., Simmons A. Synchronous appearance of antigen-positive and latently infected neurons in spinal ganglia of mice infected with a virulent strain of herpes simplex virus. Journal of General Virology 1992, 73:1281-1285.
83. Stirk W., Reinecke D., van Staden J. Seasonal variation in antifungal, antibacterial and acetylcholinesterase activity in seven South African seaweeds. Journal of Applied Phycology 2007, 19:271-276.
84. Talarico L.B., Zibetti R.G.M., Faria P.C.S., Scolaro L.A., Duarte M.E.R., Noseda M.D., Pujol C.A., Damonte E.B. Anti-herpes simplex virus activity of sulfated galactans from the red seaweeds Gymnogongrus griffithsiae and Cryptonemia crenulata. International Journal of Biological Macromolecules 2004, 34:63-71.
85. Taskinen J., Saarinen M. Increased parasite abundance associated with reproductive maturity of the clam Anodonta piscinalis. The Journal of Parasitology 1999, 85:588-591.
86. Tincu J.A., Taylor S.W. Antimicrobial peptides from marine invertebrates. Antimicrobial Agents and Chemotherapy 2004, 48:3645-3654.
87. Travers M.A., Le Goic N., Huchette S., Koken M., Paillard C. Summer immune depression associated with increased susceptibility of the European abalone, Haliotis tuberculata to Vibrio harveyi infection. Fish and Shellfish Immunology 2008, 25:800-808.
88. Travers M.A., Basuyaux O., Le GoïC N., Huchette S., Nicolas J.L., Koken M., Paillard C. Influence of temperature and spawning effort on Haliotis tuberculata mortalities caused by Vibrio harveyi: an example of emerging vibriosis linked to global warming. Global Change Biology 2009, 15:1365-1376.
89. Uki N. Abalone seedling production and its theory. International Journal Aquaculture Fisheries Technology 1989, 1:3-15.
90. Vakalia S., Benkendorff K. Antimicrobial activity in the haemolymph of Haliotis laevigata and the effects of a dietary immunostimulant. The 12th Annual Abalone Aquaculture Workshop 2005, Abalone Aquaculture Subprogram, Fisheries Research and Development Corporation, Canberra, Australia, McLaren Vale, South of Australia. A. Fleming (Ed.).
91. Wang J.Y., Guo Z.X., Feng J., Liu G.F., Xu L.W., Chen B.S., Pan J.P. Virus infection in cultured abalone, Haliotis diversicolor reeve in Guangdong Province, China. Journal of Shellfisheries Research 2004, 23:1163-1168.
92. Yasin B., Pang M., Turner J.S., Cho Y., Dinh N.N., Waring A.J., Lehrer R.I., Wagar E.A. Evaluation of the inactivation of infectious herpes simplex virus by host-defense peptides. European Journal of Clinical Microbiology and Infectious Diseases 2000, 19:187-194.
93. Zhao J., Song L., Li C., Ni D., Wu L., Zhu L., Wang H., Xu W. Molecular cloning, expression of a big defensin gene from bay scallop Argopecten irradians and the antimicrobial activity of its recombinant protein. Molecular Immunology 2007, 44:360-368.