Validating the identity of Paramoeba invadens, the causative agent of recurrent mass mortality of sea urchins in Nova Scotia, Canada

Diseases of Aquatic Organisms

Volumn 103, Issue 3, 2013, Pages 209-227

  Feehan, Colette J ^a   Johnson Mackinnon, Jessica ^a   Scheibling, Robert E ^a   Lauzon Guay, Jean Sébastien ^b   Simpson, Alastair G B ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b MAURICE LAMONTAGNE INSTITUTE   (Canada)

Author keywords

Disease; Neoparamoeba; Paramoeba invadens; Paramoebiasis; Parasite; Sea urchin; SSU rDNA

Indexed keywords

COASTAL ZONE; CONSPECIFIC; DISEASE INCIDENCE; DNA; INFECTIOUS DISEASE; INVERTEBRATE; LABORATORY METHOD; MARINE ECOSYSTEM; MASS MORTALITY; PHYLOGENETICS;

AMOEBOZOA; ANIMAL; ARTICLE; ATLANTIC OCEAN; CANADA; GENETICS; HOST PARASITE INTERACTION; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; SEA URCHIN; ULTRASTRUCTURE;

AMOEBOZOA; ANIMALS; ATLANTIC OCEAN; HOST-PARASITE INTERACTIONS; NOVA SCOTIA; PHYLOGENY; SEA URCHINS;

CANADA; NOVA SCOTIA;

AMOEBA (GENUS); DIADEMA; ECHINOIDEA; ENSIS; LOBSTER; NEOPARAMOEBA; NEOPARAMOEBA AESTUARINA; NEOPARAMOEBA BRANCHIPHILA; NEOPARAMOEBA PEMAQUIDENSIS; PARAMOEBA; PARAMOEBA INVADENS; STRONGYLOCENTROTUS DROEBACHIENSIS;

EID: 84876348744     PISSN: 01775103     EISSN: 16161580     Source Type: Journal    
DOI: 10.3354/dao02577     Document Type: Article

References (66)

1. Adams MB, Villavedra M, Nowak BF (2008) An opportunistic detection of amoebic gill disease in blue warehou, Seriolella brama Günther, collected from an Atlantic salmon, Salmo salar L., production cage in south eastern Australia. J Fish Dis 31: 713-717
2. Bermingham ML, Mulcahy MF (2006) Microfauna associated with amoebic gill disease in sea-farmed Atlantic salmon, Salmo salar L., smolts. J Fish Dis 29: 455-465 (Pubitemid 44179790)
3. Brady SM, Scheibling RE (2005) Repopulation of the shallow subtidal zone by green sea urchins (Strongylocentrotus droebachiensis) following mass mortality in Nova Scotia, Canada. J Mar Biol Assoc UK 85: 1511-1517 (Pubitemid 41607463)
4. Bridle AR, Crosbie PBB, Cadoret K, Nowak BF (2010) Rapid detection and quantification of Neoparamoeba perurans in the marine environment. Aquaculture 309: 56-61
5. Bustos PA, Young ND, Rozas MA, Bohle HM, Ildefonso RS, Morrison RN, Nowak BF (2011) Amoebic gill disease (AGD) in Atlantic salmon (Salmo salar) farmed in Chile. Aquaculture 310: 281-288
6. Caraguel CG, O'Kelly CJ, Legendre P, Frasca S and others (2007) Microheterogeneity and coevolution: an examination of rDNA sequence characteristics in Neoparamoeba pemaquidensis and its prokinetoplastid endosymbiont. J Eukaryot Microbiol 54: 418-426 (Pubitemid 47512289)
7. Clark A, Nowak BF (1999) Field investigations of amoebic gill disease in Atlantic salmon, Salmo salar L., in Tasmania. J Fish Dis 22: 433-443 (Pubitemid 30018231)
8. Crosbie PBB, Adams MB, Attard MGG, Nowak BF (2007) Development of an in vivo assay to assess attachment of Neoparamoeba sp. (an amphizoic gymnamoeba) to the gills of Atlantic salmon, Salmo salar L. J Fish Dis 30: 187-190 (Pubitemid 46375973)
9. Crosbie PBB, Bridle AR, Leef MJ, Nowak BF (2010a) Effects of different batches of Neoparamoeba perurans and fish stocking densities on the severity of amoebic gill disease in experimental infection of Atlantic salmon, Salmo salar L. Aquacult Res 41: 505-516
10. Crosbie PBB, Ogawa K, Nakano D, Nowak BF (2010b) Amoebic gill disease in hatchery-reared ayu, Plecoglossus altivelis (Temminck & Schlegel) in Japan caused by Neoparamoeba perurans. J Fish Dis 33: 455-458
11. Crosbie PBB, Bridle AR, Cadoret K, Nowak BF (2012) In vitro cultured Neoparamoeba perurans causes amoebic gill disease in Atlantic salmon and fulfils Koch's postulates. Int J Parasitol 42: 511-515
12. Douglas-Helders M, Saksida S, Raverty S, Nowak BF (2001) Temperature as a risk factor for outbreaks of Amoebic Gill Disease in farmed Atlantic salmon (Salmo salar). Bull Eur Assoc Fish Pathol 21: 114-116 (Pubitemid 33675882)
13. Douglas-Helders GM, Dawson DR, Carson J, Nowak BF (2002) Wild fish are not a significant reservoir for Neoparamoeba pemaquidensis (Page, 1987). J Fish Dis 25: 569-574 (Pubitemid 35301916)
14. Douglas-Helders GM, Tan C, Carson J, Nowak BF (2003) Effects of copper-based antifouling treatment on the presence of Neoparamoeba pemaquidensis Page, 1987 on nets and gills of reared Atlantic salmon (Salmo salar). Aquaculture 221: 13-22 (Pubitemid 36409056)
15. Dyková I, Novoa B (2001) Comments on diagnosis of amoebic gill disease (AGD) in turbot, Scophthalmus maximus. Bull Eur Assoc Fish Pathol 21: 40-44 (Pubitemid 33677088)
16. Dyková I, Figueras A, Novoa B, Casal JF (1998) Paramoeba sp., an agent of amoebic gill disease of turbot Scophthalmus maximus. Dis Aquat Org 33: 137-141 (Pubitemid 28331582)
17. Dyková I, Figueras A, Peric Z (2000) Neoparamoeba Page, 1987: light and electron microscopic observations on six strains of different origin. Dis Aquat Org 43: 217-223 (Pubitemid 32100030)
18. Dyková I, Nowak BF, Crosbie PBB, Fiala I and others (2005) Neoparamoeba branchiphila n. sp., and related species of the genus Neoparamoeba Page, 1987: morphological and molecular characterization of selected strains. J Fish Dis 28: 49-64 (Pubitemid 40191519)
19. Dyková I, Nowak B, Pecková H, Fiala I, Crosbie P, Dvorá - ková H (2007) Phylogeny of Neoparamoeba strains isolated from marine fish and invertebrates as inferred from SSU rDNA sequences. Dis Aquat Org 74: 57-65 (Pubitemid 46447420)
20. Dyková I, Fiala I, Pecková H (2008) Neoparamoeba spp. and their eukaryotic endosymbionts similar to Perkinsela amoebae (Hollande, 1980): coevolution demonstrated by SSU rRNA gene phylogenies. Eur J Protistol 44: 269-277
21. Dyková I, Lorenzo-Morales J, Kostka M, Valladares B, Pecková H (2011) Neoparamoeba branchiphila infections in moribund sea urchins Diadema aff. antillarum in Tene - rife, Canary Islands, Spain. Dis Aquat Org 95: 225-231
22. Feehan C, Scheibling RE, Lauzon-Guay JS (2012) An outbreak of sea urchin disease associated with a recent hurricane: support for the 'killer storm hypothesis' on a local scale. J Exp Mar Biol Ecol 413: 159-168
23. Fiala I, Dyková I (2003) Molecular characterisation of Neo - paramoeba strains isolated from gills of Scophthalmus maximus. Dis Aquat Org 55: 11-16 (Pubitemid 36872530)
24. Harvell D, Jordan-Dahlgren E, Merkel S, Rosenberg E and others (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20: 172-195
25. Jellett JF, Scheibling RE (1988a) Effect of temperature and prey availability on the growth of Paramoeba invadens in monoxenic culture. Appl Environ Microbiol 54: 1848-1854
26. Jellett JF, Scheibling RE (1988b) Virulence of Paramoeba invadens Jones (Amoebida, Paramoebida) from mono - xenic and polyxenic culture. J Protozool 35: 422-424
27. Jellet JF, Scheibling RE, Wardlaw AC (1988) Host specificity of Paramoeba invadens, a sea urchin pathogen. In: Burke RD, Mladenov PV, Lambert P, Parsley RL (eds) Echinoderm biology. Balkema, Rotterdam, p 755-761
28. Jellett JF, Novitsky JA, Cantley JA, Scheibling RE (1989) Non-occurrence of free-living Paramoeba invadens in water and sediments of Halifax Harbour, Nova Scotia, Canada. Mar Ecol Prog Ser 56: 205-209
29. Johnson PT (1977) Paramoebiasis in the blue crab, Calli - nectes sapidus. J Invertebr Pathol 29: 308-320
30. Jones GM (1985) Paramoeba invadens n. sp. (Amoebidae, Paramoebidae) a pathogenic amoeba from the sea urchin, Strongylocentrotus droebachiensis, in eastern Canada. J Protozool 32: 346-369
31. Jones GM, Scheibling RE (1985) Paramoeba sp. (Amoebida, Paramoebidae) as the possible causative agent of sea urchin mass mortality in Nova Scotia. J Parasitol 71: 559-565
32. Jones GM, Scheibling RE, Hebda AJ, Miller RJ (1985) Amoebae in tissues of diseased echinoids (Strongylocentrotus droebachiensis) in Nova Scotia. In: Keegan BF, O'Connor BDS (eds) Echinodermata: Proc Int Echinoderms Conf, Galway, 24-29 September 1984. AA Balkema, Rotterdam, p 289-293
33. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinf 9: 286-298 (Pubitemid 351890825)
34. Kent ML, Sawyer TK, Hedrick RP (1988) Paramoeba pe ma - quidensis (Sarcomastigophora: Paramoebidae) in fest a - tion of the gills of coho salmon Oncorhynchus kisutch reared in seawater. Dis Aquat Org 5: 163-169
35. Kudryavtsev A, Pawlowski J, Hausmann K (2011) Description of Paramoeba atlantica n. sp. (Amoebozoa, Dactylopodida)- a marine amoeba from the eastern Atlantic, with emendation of the dactylopodid families. Acta Protozool 50: 239-253
36. Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: What have we learned? Annu Rev Ecol Syst 19: 371-393
37. Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16Slike rDNA-coding regions. Gene 71: 491-499 (Pubitemid 19010867)
38. Messick GA (2002) A survey for prevalence of Paramoeba spp. in blue crabs along the Atlantic and Gulf coasts. Proc Annu Conf Southeast Assoc Fish and Wildl Agencies 56: 105-113
39. Miller RJ (1985) Succession in sea urchin and seaweed abundance in Nova Scotia, Canada. Mar Biol 84: 275-286
40. Morrison RN, Crosbie PBB, Cook MT, Adams MB, Nowak BF (2005) Cultured gill-derived Neoparamoeba pema - qui densis fails to elicit amoebic gill disease (AGD) in Atlantic salmon Salmo salar. Dis Aquat Org 66: 135-144 (Pubitemid 41413742)
41. Mullen TE, Russell S, Tucker MT, Maratea JL and others (2004) Paramoebiasis associated with mass mortality of American lobster Homarus americanus in Long Island Sound, USA. J Aquat Anim Health 16: 29-38 (Pubitemid 39147677)
42. Mullen TE, Nevis KR, O'Kelly CJ, Gast RJ, Frasca S (2005) Nuclear small-subunit ribosomal RNA gene-based characterization, molecular phylogeny and PCR detection of the Neoparamoeba from western Long Island Sound lobster. J Shellfish Res 24: 719-731
43. Munday BL, Foster CK, Roubal FR, Lester RGL (1990) Paramoebic gill infection and associated pathology of Atlantic salmon, Salmo salar, and rainbow trout, Salmo gairdneri, in Tasmania. In: Perkins FO, Cheng TC (eds) Pathology in marine science. Academic Press, San Diego, CA, p 215-222
44. Nowak BF, Bryan J, Jones SRM (2010) Do salmon lice, Lepeoptheirus salmonis, have a role in the epidemiology of amoebic gill disease caused by Neoparamoeba perurans? J Fish Dis 33: 683-687
45. Page FC (1970) Two new species of Paramoeba from Maine. J Protozool 17: 421-427
46. Page FC (1987) The classification of naked Amoebae (Phylum Rhizopoda). Arch Protistenkd 133: 199-217
47. Rodger HD, Murphy K, Mitchell SO, Henry L (2011) Gill disease in marine farmed Atlantic salmon at four farms in Ireland. Vet Rec 168: 668
48. Roubal FR, Lester RJG, Foster CK (1989) Studies on cultured and gill attached Paramoeba sp. (Gymnamoeba: Para - moebidae) and the cytopathology of paramoebic gill disease in Atlantic salmon, Salmo salar L., from Tasmania. J Fish Dis 12: 481-492
49. Scheibling RE (1984) Echinoids, epizootics and ecological stability in the rocky subtidal off Nova Scotia, Canada. Helgol Wiss Meeresunters 37: 233-242
50. Scheibling RE (1986) Increased macroalgal abundance following mass mortalities of sea urchins (Strongylocentrotus droebachiensis) along the Atlantic coast of Nova Scotia. Oecologia 68: 186-198
51. Scheibling RE (1988) Microbial control of sea urchins: Achilles' heel or Pandora's box? In: Burke RD, Mladenov PV, Lambert P, Parsley RL (eds) Proc 6th Int Echinoderms Conf, Victoria, BC, 22-28 Aug, 1987. Balkema, Rotterdam, p 745-754
52. Scheibling RE, Hennigar AW (1997) Recurrent outbreaks of disease in sea urchins Strongylocentrotus droebachiensis in Nova Scotia: evidence for a link with large-scale meteorologic and oceanographic events. Mar Ecol Prog Ser 152: 155-165 (Pubitemid 27299440)
53. Scheibling RE, Lauzon-Guay JS (2010) Killer storms: North Atlantic hurricanes and disease outbreaks in sea urchins. Limnol Oceanogr 55: 2331-2338
54. Scheibling RE, Stephenson RL (1984) Mass mortality of Strongylocentrotus droebachiensis (Echinodermata: Echino idea) off Nova Scotia, Canada. Mar Biol 78: 153-164
55. Scheibling RE, Feehan C, Lauzon-Guay JS (2010) Disease outbreaks associated with recent hurricanes cause mass mortality of sea urchins in Nova Scotia. Mar Ecol Prog Ser 408: 109-116
56. Senapin S, Phewsaiya K, Briggs M, Flegel TW (2007) Outbreaks of infectious myonecrosis virus (IMNV) in Indonesia confirmed by genome sequencing and use of an alternative RT-PCR detection method. Aquaculture 266: 32-38 (Pubitemid 46617713)
57. Sprague V, Beckett RL, Sawyer TK (1969) A new species of Paramoeba (Amoebida, Paramoebidae) parasitic in the crab Callinectes sapidus. J Invertebr Pathol 14: 167-174
58. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihoodbased phylogenetic analysis with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690 (Pubitemid 44642609)
59. Steinum T, Kvellestad A, Rønneberg LB, Nilsen H and others (2008) First cases of amoebic gill disease (AGD) in Norwegian seawater farmed Atlantic salmon, Salmo salar L., and phylogeny of the causative amoeba using 18S cDNA sequences. J Fish Dis 31: 205-214 (Pubitemid 351207250)
60. Villavedra M, Lemke S, To J, Broady K, Wallach M, Raison RL (2007) Carbohydrate epitopes are immunodominant at the surface of infectious Neoparamoeba spp. J Fish Dis 30: 191-199 (Pubitemid 46496666)
61. Vincent BN, Adams MB, Crosbie PBB, Nowak BF, Morrison RN (2007) Atlantic salmon (Salmo salar L.) exposed to cultured gill-derived Neoparamoeba branchiphila fail to develop amoebic gill disease (AGD). Bull Eur Assoc Fish Pathol 27: 112
62. Von der Heyden S, Cavalier-Smith T (2005) Culturing and environmental DNA sequencing uncover hidden kinetoplastid biodiversity and a major marine clade within ancestrally freshwater Neobodo designis. Int J Syst Evol Microbiol 55: 2605-2621 (Pubitemid 41646450)
63. Wong FYK, Carson J, Elliott NG (2004) 18S ribosomal DNAbased PCR identification of Neoparamoeba pema qui - densis, the agent of amoebic gill disease in sea-farmed salmonids. Dis Aquat Org 60: 65-76 (Pubitemid 39588279)
64. Young ND, Crosbie PBB, Adams MB, Nowak BF, Morrison RN (2007) Neoparamoeba perurans n. sp., an agent of amoebic gill disease of Atlantic salmon (Salmo salar L.). Int J Parasitol 37: 1469-1481 (Pubitemid 47417971)
65. Young ND, Dyková I, Snekvik K, Nowak BF, Morrison RN (2008) Neoparamoeba perurans is a cosmopolitan aetiological agent of amoebic gill disease. Dis Aquat Org 78: 217-223 (Pubitemid 351547558)
66. Zilberg D, Gross A, Munday BL (2001) Production of sal monid amoebic gill disease by exposure to Paramoeba sp. harvested from the gills of infected fish. J Fish Dis 24: 79-82