Early host-pathogen interactions in a marine bivalve: Crassostrea virginica pallial mucus modulates Perkinsus marinus growth and virulence

Diseases of Aquatic Organisms

Volumn 104, Issue 3, 2013, Pages 237-247

  Espinosa, Emmanuelle Pales ^a   Winnicki, Sarah ^a   Allam, Bassem ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Dermo; Host specificity; Mucus; Virulence

Indexed keywords

BIVALVE; ENZYME ACTIVITY; GROWTH RATE; HOST SPECIFICITY; HOST-PATHOGEN INTERACTION; INFECTIVITY; INHIBITION; MARINE ECOSYSTEM; MUCUS; PARASITE; PROTIST; VIRULENCE;

ALVEOLATA; ANIMAL; ARTICLE; CRASSOSTREA; HOST PARASITE INTERACTION; MUCUS; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

ALVEOLATA; ANIMALS; CRASSOSTREA; HOST-PARASITE INTERACTIONS; MUCUS; VIRULENCE;

BIVALVIA; CRASSOSTREA GIGAS; CRASSOSTREA VIRGINICA; OSTREIDAE; PERKINSUS MARINUS; PROTISTA;

EID: 84879347405     PISSN: 01775103     EISSN: 16161580     Source Type: Journal    
DOI: 10.3354/dao02599     Document Type: Article

References (66)

1. Ahn HY, Sue LF, Ma JKH, Pinkstaff CA, Pore RS, Overman DO, Malanga CJ (1988) Synthesis and secretion of mucous glycoprotein by the gill of Mytilus edulis. I. Histochemical and chromatographic analysis of [14C]glu - co sa mine bioincorporation. Biochim Biophys Acta 966: 122-132
2. Allam B, Carden W, Ward E, Ralph G, Winnicki SM, Pales Espinosa E (2013) Early host-pathogen interactions in marine bivalves: evidence that the alveolate parasite Perkinsus marinus infects through the oyster mantle during rejection of pseudofeces. J Invertebr Pathol 113: 26-34
3. Anderson RS (1999) Perkinsus marinus secretory products modulate superoxide anion production by oyster (Crassostrea virginica) haemocytes. Fish Shellfish Immunol 9: 51-60
4. Azevedo C (1989) Fine-structure of Perkinsus atlanticus n. sp. (Apicomplexa, Perkinsea) parasite of the clam Ruditapes decussatus from Portugal. J Parasitol 75: 627-635
5. Banin E, Israely T, Fine M, Loya Y, Rosenberg E (2001) Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. FEMS Microbiol Lett 199: 33-37 (Pubitemid 32455460)
6. Benkendorff K, Bremner J, Davis A (2001) Indole derivatives from the egg masses of muricid molluscs. Molecules 6: 70-78 (Pubitemid 38982491)
7. Brown GD, Kaattari SL, Reece KS (2005) Effect of homo - genate from different oyster species on Perkinsus marinus proliferation and subtilisin gene transcription. J Shell - fish Res 24: 1027-1033 (Pubitemid 44188324)
8. Brun NT, Ross NW, Boghen AD (2000) Changes in the electrophoretic profiles of gill mucus proteases of the eastern oyster Crassostrea virginica in response to infection by the turbellarian Urastoma cyprinae. J Invertebr Pathol 75: 163-170 (Pubitemid 30186320)
9. Burreson EM, Calvo LMR (1996) Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985. J Shellfish Res 15: 17-34
10. Burreson EM, Ford SE (2004) A review of recent information on the Haplosporidia, with special reference to Haplo - sporidium nelsoni (MSX disease). Aquat Living Resour 17: 499-517 (Pubitemid 40059483)
11. Burreson EM, Reece KS, Dungan CF (2005) Molecular, morphological, and experimental evidence support the synonymy of Perkinsus chesapeaki and Perkinsus andrewsi. J Eukaryot Microbiol 52: 258-270 (Pubitemid 43923937)
12. Bushek D, Allen SK, Alcox KA, Gustafson RG, Ford SE (1997) Response of Crassostrea virginica to in vitro cultured Perkinsus marinus: preliminary comparisons of three inoculation methods. J Shellfish Res 16: 479-485 (Pubitemid 28104577)
13. Chintala MM, Bushek D, Ford SE (2002) Comparison of in vitro-cultured and wild-type Perkinsus marinus. II. Dosing methods and host response. Dis Aquat Org 51: 203-216 (Pubitemid 35211908)
14. Dahl SF, Thiel J, Allam B (2010) Field performance and QPX disease progress in cultured and wild-type strains of Mercenaria mercenaria in New York waters. J Shellfish Res 29: 83-90
15. Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Ngai MJ (2004) NO means 'yes' in the squid- vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6: 1139-1151 (Pubitemid 39517484)
16. Ducklow HW, Mitchell R (1979) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24: 715-725
17. Dungan CF, Hamilton RM, Burreson EM, Ragone-Calvo LM (1996) Identification of Perkinsus marinus portals of entry in histochemical immunoassays of challenged oysters. J Shellfish Res 15: 500
18. Earnhart CG, VogelbeinMA, Brown GD, Reece KS, Kaattari SL (2004) Supplementation of Perkinsus marinus cultures with host plasma or tissue homogenate enhances their infectivity. Appl Environ Microbiol 70: 421-431 (Pubitemid 38090233)
19. Ebran N, Julien S, Orange N, Saglio P, Lemaitre C, Molle G (1999) Pore-forming properties and antibacterial activity of proteins extracted from epidermal mucus of fish. Comp Biochem Physiol A 122: 181-189 (Pubitemid 29161469)
20. Fisher WS (1992) Occurrence of agglutinins in the pallial cavity mucus of oysters. J Exp Mar Biol Ecol 162: 1-13
21. Ford SE, Tripp MR (1996) Diseases and defense mechanisms. In: Newell RIE, Kennedy VS, Eble AF (eds) The eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park, MD
22. Ford SE, Chintala MM, Bushek D (2002a) Comparison of in vitro-cultured and wild-type Perkinsus marinus. I. Pathogen virulence. Dis Aquat Org 51: 187-201 (Pubitemid 35211907)
23. Ford SE, Kraeuter JN, Barber RD, Mathis G (2002b) Aquaculture- associated factors in QPX disease of hard clams: density and seed source. Aquaculture 208: 23-38 (Pubitemid 34592975)
24. Garreis KA, LaPeyre JF, Faisal M (1996) The effects of Perkinsus marinus extracellular products and purified proteases on oyster defence parameters in vitro. Fish Shellfish Immunol 6: 581-597 (Pubitemid 126160540)
25. Gauthier JD, Vasta GR (2002) Effects of plasma from bivalve mollusk species on the in vitro proliferation of the protistan parasite Perkinsus marinus. J Exp Zool 292: 221-230 (Pubitemid 34166134)
26. Goedken M, Morsey B, Sunila I, De Guise S (2005) Immuno - modulation of Crassostrea gigas and Crassostrea virginica cellular defense mechanisms by Perkinsus marinus. J Shellfish Res 24: 487-496 (Pubitemid 41209454)
27. Grimm-Jørgensen Y, Ducor ME, Piscatelli J (1986) Surface mucus production in gastropods is dependent on environmental salinity and humidity. Comp Biochem Physiol A 83: 415-419
28. Gustafson K, Andersen RJ (1985) Chemical studies of British Columbia nudibranchs. Tetrahedron 41: 1101-1108
29. Hughes FM, Foster B, Grewal S, Sokolova IM (2010) Apoptosis as a host defense mechanism in Crassostrea virginica and its modulation by Perkinsus marinus. Fish Shellfish Immunol 29: 247-257
30. Ireland C, Faulkner DJ (1978) The defensive secretion of the opisthobranch mollusc Onchidella binneyi. Bioorg Chem 7: 125-131 (Pubitemid 8380418)
31. Kleeman SN, Adlard RD, Lester RJG (2002) Detection of the initial infective stages of the protozoan parasite Marteilia sydneyi in Saccostrea glomerata and their development through to sporogenesis. Int J Parasitol 32: 767-784 (Pubitemid 34327595)
32. Kleinbaum DG, Klein M (2005) Survival analysis: a selflearning text. Springer, New York, NY
33. La Peyre JF, Schafhauser DY, Rizkalla EH, Faisal M (1995) Production of serine proteases by the oyster pathogen Perkinsus marinus (apicomplexa) in vitro. J Eukaryot Microbiol 42: 544-551
34. La Peyre MK, Nickens AD, Volety AK, Tolley GS, La Peyre JF (2003) Environmental significance of freshets in reducing Perkinsus marinus infection in eastern oysters Crassostrea virginica: potential management applications. Mar Ecol Prog Ser 248: 165-176 (Pubitemid 36339335)
35. Lee YK, Lim CY, Teng WL, Ouwehand AC, Tuomola EM, Salminen S (2000) Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells and their competition with enterobacteria. Appl Environ Microbiol 66: 3692-3697
36. Lin Z, Fernández-Robledo JA, Cellier MFM, Vasta GR (2011) The natural resistance associated macrophage protein from the protozoan parasite Perkinsus marinus mediates iron uptake. Biochemistry 50: 6340-6355
37. MacIntyre EA, Earnhart CG, Kaattari SL (2003) Host oyster tissue extracts modulate in vitro protease expression and cellular differentiation in the protozoan parasite, Perkinsus marinus. Parasitology 126: 293-302 (Pubitemid 36520943)
38. Mackin JG (1951) Histopathology of infection of Crassostrea virginica (Gmelin) by Dermocystidium marinum Mackin, Owen, and Collier. Bull Mar Sci 1: 72-87
39. Mackin JG, Boswell JL (1956) The life cycle and relationships of Dermocystidium marinum. Proc Natl Shellfish Assoc 46: 112-115
40. McDade JE, Tripp MR (1967) Lysozyme in oyster mantle mucus. J Invertebr Pathol 9: 581-582
41. Nagashima Y, Kikuchi N, Shimakura K, Shiomi K (2003) Purification and characterization of an antibacterial protein in the skin secretion of rockfish Sebastes schlegeli. Comp Biochem Physiol C 136: 63-71 (Pubitemid 38352655)
42. Navas JI, Castillo MC, Vera P, Ruizrico M (1992) Principal parasites observed in clams, Ruditapes decussatus (L.), Ruditapes philippinarum (Adams et Reeve), Venerupis pullastra (Montagu) and Venerupis aureus (Gmelin), from the Huelva coast (SW Spain). Aquaculture 107: 193-199
43. Ofek I, Doyle RJ (1994) Bacterial adhesion to cells and tissues. Chapman & Hall, New York, NY
44. Pales Espinosa E, Allam B (2006) Comparative growth and survival of juvenile hard clams, Mercenaria mercenaria, fed commercially available diets. Zoo Biol 25: 513-525 (Pubitemid 46071819)
45. Pales Espinosa E, Perrigault M, Ward JE, Shumway SE, Allam B (2009) Lectins associated with the feeding organs of the oyster Crassostrea virginica can mediate particle selection. Biol Bull 217: 130-141
46. Pales Espinosa E, Perrigault M, Ward JE, Shumway SE, Allam B (2010) Microalgal cell surface carbohydrates as recognition sites for particle sorting in suspension-feeding bivalves. Biol Bull 218: 75-86
47. Ragone Calvo LM, Walker JG, Burreson EM (1998) Pre - valence and distribution of QPX, Quahog Parasite Unknown, in hard clams Mercenaria mercenaria in Virginia, USA. Dis Aquat Org 33: 209-219 (Pubitemid 28398142)
48. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1-14 (Pubitemid 44606066)
49. Rodriguez F, Navas JI (1995) A comparison of gill and hemolymph assays for the thioglycolate diagnosis of Perkinsus atlanticus (Apicomplexa, Perkinsea) in clams, Ruditapes decussatus (L.) and Ruditapes philippinarum (Adams et Reeve). Aquaculture 132: 145-152
50. Romestand B, Corbier F, Roch P (2002) Protease inhibitors and haemagglutinins associated with resistance to the protozoan parasite, Perkinsus marinus, in the Pacific oyster, Crassostrea gigas. Parasitology 125: 323-329
51. Schott EJ, Vasta GR (2003) The PmSOD1 gene of the protistan parasite Perkinsus marinus complements the sod2 Delta mutant of Saccharomyces cerevisiae, and directs an iron superoxide dismutase to mitochondria. Mol Biochem Parasitol 126: 81-92 (Pubitemid 36120607)
52. Schott EJ, Pecher WT, Okafor F, Vasta GR (2003a) The protistan parasite Perkinsus marinus is resistant to selected reactive oxygen species. Exp Parasitol 105: 232-240 (Pubitemid 38264354)
53. Schott EJ, Robledo JAF, Wright AC, Silva AM, Vasta GR (2003b) Gene organization and homology modeling of two iron superoxide dismutases of the early branching protist Perkinsus marinus. Gene 309: 1-9 (Pubitemid 36513856)
54. Simkiss K, Wilbur KM (1977) The molluscan epidermis and its secretions. Symp Zool Soc Lond 39: 35-76
55. Smolowitz R, Leavitt D, Perkins F (1998) Observations of a protistan disease similar to QPX in Mercenaria mer - cenaria (hard clams) from the coast of Massachusetts. J Invertebr Pathol 71: 9-25 (Pubitemid 128352145)
56. Sunila I, LaBanca J (2003) Apoptosis in the pathogenesis of infectious diseases of the eastern oyster Crassostrea virginica. Dis Aquat Org 56: 163-170 (Pubitemid 37293075)
57. Tuomola EM, Ouwehand AC, Salminen SJ (1999) The effect of probiotic bacteria on the adhesion of pathogens to human intestinal mucus. FEMS Immunol Med Microbiol 26: 137-142 (Pubitemid 29490988)
58. Villalba A, Reece KS, Ordas MC, Casas SM, Figueras A (2004) Perkinsosis in molluscs: a review. Aquatic Living Resour 17: 411-432 (Pubitemid 40059478)
59. Vine NG, Leukes WD, Kaiser H (2004) In vitro growth characteristics of five candidate aquaculture probiotics and two fish pathogens grown in fish intestinal mucus. FEMS Microbiol Lett 231: 145-152 (Pubitemid 38177604)
60. Walker RP, Faulkner DJ (1981) Chlorinated acetylenes from the nudibranch Diaulula sandiegensis. J Org Chem 46: 1475-1478
61. Ward JE, Shumway SE (2004) Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300: 83-130 (Pubitemid 38583469)
62. Welsh MJ, Ramsey BW, Accurso F, Cutting GR (2001) Cystic fibrosis. In: Scriver CR, Beaudet AL, Sly W, Valle D (eds) The metabolic and molecular basis of inherited disease, Vol 3, 8th edn. McGraw-Hill, New York, NY, p 521-588
63. Winnicki SM, Carden W, Holohan B, Ralph G, Ward E, Allam B (2008) Establishment of Perkinsus marinus infection in Crassostrea virginica: insights into the portal of entry and the potential role of marine aggregates. J Shellfish Res 27: 1064
64. Xing J, Pales Espinosa E, Perrigault M, Allam B (2011) Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica. Fish Shellfish Immunol 30: 851-858
65. Xue QG, Waldrop GL, Schey KL, Itoh N and others (2006) A novel slow-tight binding serine protease inhibitor from eastern oyster (Crassostrea virginica) plasma inhibits perkinsin, the major extracellular protease of the oyster protozoan parasite Perkinsus marinus. Comp Biochem Physiol B 145: 16-26 (Pubitemid 44279480)
66. Yamazaki M (1993) Antitumor and antimicrobial glycoproteins from sea hares. Comp Biochem Physiol C 105: 141-146 (Pubitemid 23203977)