Possible impacts of zoosporic parasites in diseases of commercially important marine mollusc species: part II. Labyrinthulomycota

References

Adl, S.M., A.G.B. Simpson, C.E. Lane, J. Lukeš, D. Bass, S.S. Bowser, M.W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, L. Le Gall, D.H. Lynn, H. McManus, E.A.D. Mitchell, S.E. Mozley-Standridge, L.W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C.L. Schoch, A. Smirnov and F.W. Spiegel. 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59: 429–493.10.1111/j.1550-7408.2012.00644.xSearch in Google Scholar

Alderman, D.J. 1976. Fungal diseases of marine animals. In: (E.B.G. Jones, ed) Recent advances in aquatic mycology. ELEK Science, London. pp. 223–260.Search in Google Scholar

Alderman, D.J. and P. Gras. 1969. “Gill disease” of Portuguese oysters. Nature224: 616–617.10.1038/224616a0Search in Google Scholar

Alderman, D.J. and E.B.G. Jones. 1971. Physiological requirements of two marine phycomycetes, Althornia crouchii and Ostracoblabe implexa. Trans. Brit. Mycol. Soc. 57: 213–225.10.1016/S0007-1536(71)80003-7Search in Google Scholar

Anderson, R.S., B.S. Kraus, S.E. McGladdery and R. Smolowitz. 2003a. Mucoid secretions protect QPX from antimicrobial agents. J. Shellfish Res. 22: 205–208.Search in Google Scholar

Anderson, R.S., B.S. Kraus, S.E. McGladdery, K.S. Reece and N.A. Stokes. 2003b. A thraustochytrid protist isolated from Mercenaria mercenaria: molecular characterization and host defense responses. Fish Shellfish Immun. 15: 183–194.10.1016/S1050-4648(02)00157-2Search in Google Scholar

Ansell, A. 1968. The rate of growth of the hard clam Mercenaria mercenaria (L.) throughout the geographical range. J. Cons. Int. Explor. Mer.31: 364–409.10.1093/icesjms/31.3.364Search in Google Scholar

Baldauf, S.L. 2003. The deep route of Eukaryotes. Science300: 1703–1706.10.1126/science.1085544Search in Google Scholar

Beakes, G.W., M. Thines and D. Honda. 2015. Straminipile “Fungi”–taxonomy. eLS. 1–9.10.1002/9780470015902.a0001984Search in Google Scholar

Bower, S.M. 1987a. Labyrinthuloides haliotidis n.sp. (Protozoa: Labyrinthomorpha), a pathogenic parasite of small juvenile abalone in a British Columbia mariculture facility. Can. J. Zool. 65: 1996–2007.10.1139/z87-304Search in Google Scholar

Bower, S.M. 1987b. The life cycle and ultrastructure of a new species of thraustochytrid (Protozoa: Labyrinthomorpha) pathogenic to small abalone. Aquaculture 67: 269–272.10.1016/0044-8486(87)90054-8Search in Google Scholar

Bower, S.M. 1987c. Artificial culture of Labyrinthuloides haliotidis (Protozoa: Labyrinthulomorpha), a pathogenic parasite of abalone. Can. J. Zool. 65: 2013–2020.10.1139/z87-306Search in Google Scholar

Bower, S.M. 1987d. Pathogenicity and host specificity of Labyrinthuloides haliotidis (Protozoa: Labyrinthulomorpha), a parasite of juvenile abalone. Can. J. Zool. 65: 2008–2012.10.1139/z87-305Search in Google Scholar

Bower, S.M., N. McLean and D.J. Whitaker. 1989. Mechanism of infection by Labyrinthuloides haliotidis (Protozoa: Labyrinthomorpha), a parasite of abalone (Haliotis kamtschatkana) (Mollusca: Gastropoda). J. Invertebr. Pathol.53: 401–409.10.1016/0022-2011(89)90106-7Search in Google Scholar

Bowie, P.D. 1970. The isolation and characterization of Thraustochytrium pachydermum from the Salton Sea, California. The University of Arizona. pp. 49.Search in Google Scholar

Brothers, C., E. Marks III and R. Smolowitz. 2000. Conditions affecting the growth and zoosporulation of the protistan parasite QPX in culture. Biol. Bull. 199: 200–201.10.2307/1542897Search in Google Scholar

Brown, S.P., D.M. Cornforth and N. Mideo. 2012. Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol.20: 336–342.10.1016/j.tim.2012.04.005Search in Google Scholar

Buggé, D.M. and B. Allam. 2007. Effects of starvation and macroalgae extracts on the survival and growth of quahog parasite unknown (QPX). J. Exp. Mar. Biol. Ecol. 348: 60–69.10.1016/j.jembe.2007.04.013Search in Google Scholar

Burge, C.A., C.J.S. Kim, J.M. Lyles and C.D. Harvell. 2013. Special issue oceans and humans health: the ecology of marine opportunists. Microb. Ecol. 65: 869–879.10.1007/s00248-013-0190-7Search in Google Scholar

Burge, C.A., C.M. Eakin, C.S. Friedman, B. Froelich, P.K. Hershberger, E.E. Hofmann, L.E. Petes, K.C. Prager, E. Weil, B.L. Willis, S.E. Ford and C.D. Harvell. 2014. Climate change influences on marine infectious diseases: implications for management and society. Ann. Rev.Mar. Sci. 6: 249–277.10.1146/annurev-marine-010213-135029Search in Google Scholar

Casadevall, A., J.N. Steenbergen and J.D. Nosanchuk. 2003. ‘Ready made’ virulence and ‘dual use’ virulence factors in pathogenic environmental fungi – the Cryptococcus neoformans paradigm. Curr. Opin.Microbiol. 6: 332–337.10.1016/S1369-5274(03)00082-1Search in Google Scholar

Castagna, M. and P. Chanley. 1973. Salinity tolerance of some marine bivalves from inshore estuarine environments inshore environments in Virginia waters on the western mid-Atlantic coast. Malacologia 12: 47–96.Search in Google Scholar

Collado Mercado, E., J.C. Radway and J.L. Collier. 2010. Novel uncultivated Labyrinthulomycetes revealed by 18S rDNA sequences from seawater and sediment samples. Aquat. Microb. Ecol. 58: 215–228.10.3354/ame01361Search in Google Scholar

Cox, B.A. and J.G. Mackin 1974. Studies on a new species of Labyrinthula (Labyrinthulales) isolated from the marine gastropod Thais haemastoma floridana. Trans. Am. Microsc. Soc. 93:62–70.10.2307/3225220Search in Google Scholar

Dahl, S.F. and B. Allam. 2007. Laboratory transmission studies of QPX disease in the northern Quahog (=hard clam): development of an infection procedure. J. Shellfish Res. 26: 383–389.10.2983/0730-8000(2007)26[383:LTSOQD]2.0.CO;2Search in Google Scholar

Dahl, S.F. and B. Allam. 2015. Hard clam relocation as a potential strategy for QPX disease mitigation within an enzootic estuary. Aqua. Res. 47: 3445–3454.10.1111/are.12793Search in Google Scholar

Dahl, S.F., M. Perrigault and B. Allam. 2008. Laboratory transmission studies of QPX disease in the hard clam: interactions between different host strains and pathogen isolates. Aquaculture280: 64–70.10.1016/j.aquaculture.2008.04.026Search in Google Scholar

Dahl, S.F., J. Thiel and B. Allam. 2010. Field performance and QPX disease progress in cultured and wild-type strains of Mercenaria mercenaria in New York waters. J. Shellfish Res. 29: 83–90.10.2983/035.029.0131Search in Google Scholar

Dahl, S.F., M. Perrigault, Q. Liu, J.L. Collier, D.A. Barnes and B. Allam. 2011. Effects of temperature on hard clam (Mercenaria mercenaria) immunity and QPX (Quahog Parasite Unknown) disease development: I. Dynamics of QPX disease. J. Invertebr. Pathol. 106: 314–321.10.1016/j.jip.2010.11.005Search in Google Scholar

Dove, A.D.M., P.R. Bowser and R.M. Cerrato. 2004. Histological analysis of an outbreak of QPX disease in wild hard clams Mercenaria mercenaria in New York. J. Aquat. Anim. Health16: 246–250.10.1577/H03-052.1Search in Google Scholar

Drinnan, R.E. and E.B. Henderson. 1963. 1962 mortalities and a possible disease organism in Neguac quahaugs. Ellerslie Biological Station Annual Report 1962–63, Department of Fisheries and Oceans, St. Andrews, New Brunswick, Canada. pp. 18–20.Search in Google Scholar

Ford, S.E., J.N. Kraeuter, R.D. Barber and G. Mathis. 2002. Aquaculture-associated factors in QPX disease of hard clams: density and seed source. Aquaculture 208: 23–28.10.1016/S0044-8486(01)00795-5Search in Google Scholar

Garcia-Vedrenne, A.E., M. Groner, A. Page-Karjian, G.-F. Siegmund, S. Singhal, J. Sziklay and S. Roberts. 2013. Development of genomic resources for a thraustochytrid pathogen and investigation of temperature influences on gene expression. PLoS One8: e74196.10.1371/journal.pone.0074196Search in Google Scholar

Gast, R.J., E. Cushman, D.M. Moran, K.R. Uhlinger, D. Leavitt and R. Smolowitz. 2006. DGGE-based detection method for Quahog Parasite Unknown (QPX). Dis. Aquat. Organ.70: 115–122.10.3354/dao070115Search in Google Scholar

Gast, R.J., D.M. Moran, C. Audemard, M.M. Lyons, J. DeFavari, K.S. Reece, D. Leavitt and R. Smolowitz. 2008. Environmental distribution and persistence of Quahog Parasite Unknown (QPX). Dis. Aquat. Organ. 81: 219–229.10.3354/dao01948Search in Google Scholar

Guo, X. and S.E. Ford. 2016. Infectious diseases of marine molluscs and host responses as revealed by genomic tools. Philos. Tr. Soc. B.371: 20150206.10.1098/rstb.2015.0206Search in Google Scholar

Harvell, D., R. Aronson, N. Baron, J. Connell, A. Dobson, S. Ellner, L. Gerber, K. Kim, A. Kuris, H. McCallum, K. Lafferty, B. McKav, J. Porter, M. Pascual, G. Smith, K. Sutherland and J. Ward. 2004. The rising tide of ocean diseases: unsolved problems and research priorities. Front. Ecol.2: 375–382.10.1890/1540-9295(2004)002[0375:TRTOOD]2.0.CO;2Search in Google Scholar

Honda, D., T. Yokochi, T. Nakahara, S. Raghukumar, A. Nakagiri, K. Schaumann and T. Higashihara. 1999. Molecular phylogeny of labyrinthulids and thraustochytrids based on the sequencing of 18S ribosomal RNA gene. J. Eukaryot. Microbiol. 46: 637–647.10.1111/j.1550-7408.1999.tb05141.xSearch in Google Scholar

Jones, E.B.G. and D.J. Alderman. 1971. Althornia crouchii gen. et sp. nov., a marine biflagellate fungus. Nova Hedw. 21: 381–400.Search in Google Scholar

Jones, G.M. and R.K. O’Dor. 1983. Ultrastructural observations on a thraustochytrid fungus parasitic in the gills of squid (Illex illecebrosus LeSueur). J. Parasitol. 69: 903–911.10.2307/3281055Search in Google Scholar

Kleinschuster, S.J., R. Smolowitz and J. Parent. 1998. In vitro life cycle and propagation of Quahog Parasite Unknown. J. Shellfish Res. 17: 75–78.Search in Google Scholar

Kraeuter, J.N., S. Ford, D. Bushek, E. Scarpa, W.C. Walton, D.C. Murphy, G. Flimlin and G. Mathis. 2011. Evaluation of three Northern Quahog (=hard clam) Mercenaria mercenaria (Linnaeus) strains grown in Massachusetts and New Jersey for QPX-resistance. J. Shellfish Res. 30: 805–812.10.2983/035.030.0321Search in Google Scholar

Lafferty, K.D., J.W. Porter and S.E. Ford. 2004. Are diseases increasing in the ocean? Ann. Rev. Ecol. Evol. Syst.35: 31–54.10.1146/annurev.ecolsys.35.021103.105704Search in Google Scholar

Leander, C.A. and D. Porter. 2001. The Labyrinthulomycota is comprised of three distinct lineages. Mycologia93: 459–464.10.2307/3761732Search in Google Scholar

Leander, C.A., D. Porter and B.S. Leander. 2004. Comparative morphology and molecular phylogeny of aplanochytrids, Eur. J. Protistol. 40: 317–328.10.1016/j.ejop.2004.07.003Search in Google Scholar

Li, Q., X. Wang, X. Liu, N. Jiao and G. Wang. 2013. Abundance and novel lineages of thraustochytrids in Hawaiian waters. Microb. Ecol. 66: 823–830.10.1007/s00248-013-0275-3Search in Google Scholar

Liu, Q. 2010. Investigation of the dynamics of QPX, a pathogen of the hard clam, Mercenaria mercenaria, in the environment and clams. Ph.D. thesis Stony Brook University, New York. pp. 133.Search in Google Scholar

Liu, Q., B. Allam and J.L. Collier. 2009. Quantitative real-time PCR assay for QPX (Thraustochytriidae), a parasite of the hard clam (Mercenaria mercenaria). Appl. Env. Microbiol. 75: 4913–4918.10.1128/AEM.00246-09Search in Google Scholar

Liu, Q., J.L. Collier. and B. Allam. 2016. Seasonality of QPX disease in the Raritan Bay (NY) wild hard clam (Mercenaria mercenaria) population. Aqua. Res. 48: 1–10.10.1111/are.12969Search in Google Scholar

Lyons, M.M., R. Smolowitz, K.R. Uhlinger, R.J. Gast and J.E. Ward. 2005. Lethal marine snow: pathogen of bivalve mollusc concealed in marine aggregates. Limnol. Oceanogr. 50: 1983–1988.10.4319/lo.2005.50.6.1983Search in Google Scholar

Lyons, M.M., R. Smolowitz, C.F. Dungan and S.B. Roberts. 2006. Development of a real time quantitative PCR assay for the hard clam pathogen Quahog Parasite Unknown (QPX). Dis. Aquat. Organ. 72: 45–52.10.3354/dao072045Search in Google Scholar

Lyons, M.M., R. Smolowitz, M. Gomez-Chiarri and J.E. Ward. 2007. Epizootiology of Quahog Parasite Unknown (QPX) disease in Northern Quahogs (=hard clams) Mercenaria mercenaria. J. Shellfish Res. 26: 371–381.10.2983/0730-8000(2007)26[371:EOQPUQ]2.0.CO;2Search in Google Scholar

MacCallum, G.S. and S.E. McGladdery. 2000. Quahog Parasite Unknown (QPX) in the Northern Quahog Mercenaria mercenaria (Linnaeus, 1758) and M. mercenaria var. notata from Atlantic Canada, survey results from three Maritime Provinces. J. Shellfish Res. 19: 43–50.Search in Google Scholar

McLean, N. and D. Porter. 1982. The yellow-spot disease of Tritonia diomedea Bergh, 1894 (Mollusca: Gastropoda: Nudibranchia): encapsulation of the thraustochytriaceous parasite by host amoebocytes. J. Parasitol.68: 243–252.10.2307/3281182Search in Google Scholar

McLean, N. and D. Porter. 1987. Lesions produced by a thraustochytrid in Tritonia diomedea (mollusca: Gastropoda: Nudibranchia). J. Invertebr. Pathol. 49: 223–225.10.1016/0022-2011(87)90165-0Search in Google Scholar

Perkins, F.O. 1969. Ultrastructure of vegetative stages in Labyrinthomyxa marina (=Dermocystidium marinum), a commercially significant oyster pathogen. J. Invertebr. Pathol. 13: 199–222.10.1016/0022-2011(69)90211-0Search in Google Scholar

Perkins, F.O. 1972. The ultrastucture of holdfasts, ‘rhizoids’, and ‘slime tracks’ in thraustochtyriaceous fungi and Labyrinthula spp. Arch. Mikrobiol. 84: 95–118.10.1007/BF00412431Search in Google Scholar

Perkins, F.O. 1973. A new species of marine labyrinthulid Labyrinthuloides yorkensis gen. nov. spec. nov. – cytology and fine structure. Arch. Mikrobiol. 90: 1–17.10.1007/BF00424819Search in Google Scholar

Perrigault, M. and B. Allam. 2009. Cytotoxicity of quahog parasite unknown (QPX) toward hard clam (Mercenaria mercenaria) haemocytes and interactions between different pathogen isolates and host strains. Parasitology.136: 1281–1289.10.1017/S0031182009990606Search in Google Scholar

Perrigault, M., D.M. Buggé and B. Allam. 2010. Effect of environmental factors on survival and growth of quahog parasite unknown (QPX) in vitro. J. Invertebr. Pathol. 104: 83–89.10.1016/j.jip.2010.02.005Search in Google Scholar

Perrigault, M., S.F. Dahl, E.P. Espinosa, L. Gambino and B. Allam. 2011. Effects of temperature on hard clam (Mercenaria mercenaria) immunity and QPX (Quahog Parasite Unknown) disease development: II. Defense parameters. J. Invertebr. Pathol. 106: 322–332.10.1016/j.jip.2010.11.004Search in Google Scholar

Perrigault, M., S.F. Dahl, E.P. Espinosa and B. Allam. 2012. Effects of salinity on hard clam (Mercenaria mercenaria) defense parameters and QPX disease dynamics. J. Invertebr. Pathol. 110: 73–82.10.1016/j.jip.2012.02.004Search in Google Scholar

Polglase, J.L. 1980. A preliminary report on the Thraustochytrid(s) and Labyrinthulid(s) associated with a pathological condition in the lesser octopus Eledone cirrhosa. Bot. Mar. 22: 699–706.10.1515/botm-1980-1106Search in Google Scholar

Polglase, J.L., D.J. Alderman and R.H. Richards. 1986. Aspects of the progress of mycotic infections in marine animals. In: (S.T. Moss, ed) Biology of marine fungi. Cambridge University Press, Cambridge. pp. 155–164.Search in Google Scholar

Qian, H., Q. Liu, B. Allam and J.L. Collier. 2007. Molecular genetic variation within and among isolates of QPX (Thraustochytridae), a parasite of the hard clam Mercenaria mercenaria. Dis. Aquat. Organ. 77: 159–168.10.3354/dao01848Search in Google Scholar

Quick, J.A., Jr. 1972. A new thraustochytrideacous fungus endoparasitic to the American oyster. Soc. Invert. Pathol. Newslet. 4: 13.Search in Google Scholar

Ragan, M.A., G.S. MacCallum, C.A. Murphy, J. J. Cannone, R.R. Gutell and S.E. McGladery. 2000. Protistian parasite QPX of hard-shell clam Mercinaria mercinaria is a member of Labyrinthulomycota. Dis. Aquat. Organ. 42: 185–190.10.3354/dao042185Search in Google Scholar

Raghukumar, S. 2002. Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Eur. J. Protistol. 38: 127–145.10.1078/0932-4739-00832Search in Google Scholar

Raghukumar, S. and V.S. Damare. 2011. Increasing evidence for the important role of Labyrinthulomycetes in marine ecosystems. Bot. Mar. 54: 3–11.10.1515/bot.2011.008Search in Google Scholar

Ragone-Calvo, L.M., J.G. Walker and E.M. Burreson. 1998. Prevalence and distribution of QPX, Quahog Parasite Unknown, in hard clams, Mercenaria mercenaria in Virginia, USA. Dis. Aquat. Organ. 33: 209–219.10.3354/dao033209Search in Google Scholar

Ragone-Calvo, L.M., S.E. Ford, J.N. Kraeuter, D.F. Leavitt, R. Smolowitz and E.M. Burreson. 2007. Influence of host genetic origin and geographic location on QPX Disease in Northern Quahogs (=hard clams), Mercenaria mercenaria. J. Shellfish Res. 26: 109–119.10.2983/0730-8000(2007)26[109:IOHGOA]2.0.CO;2Search in Google Scholar

Rubin, E., A. Tanguy, M. Perrigault, E.P. Espinosa and B. Allam. 2014. Characterization of the transcriptome and temperature-induced differential gene expression in QPX, the thraustochytrid parasite of hard clams. BMC Genomics. 15: 245.10.1186/1471-2164-15-245Search in Google Scholar PubMed PubMed Central

Rubin, E., E.P. Espinosa, A. Koller and B. Allam. 2015. Characterisation of the secretome of the clam parasite, QPX. Int. J. Parasitol. 45: 187–196.10.1016/j.ijpara.2014.10.008Search in Google Scholar PubMed

Smolowitz, R., D. Leavitt and F. Perkins. 1998. Observations of protistan disease similar to QPX in Mercenaria mercenaria (Hard Clams) from the coast of Massachusetts. J. Invertebr. Pathol.71: 9–25.10.1006/jipa.1997.4706Search in Google Scholar PubMed

Tsui, C.K.M. and L.L.P. Vrijmoed. 2012. A re-visit to the evolution and ecophysiology of the Labyrinthulomycetes. In: (A. Cruzado, ed) Marine Ecosytems. InTech Open Access Publisher. pp. 161–176.10.5772/35979Search in Google Scholar

Ward, J.R. and K.D. Lafferty. 2004. The elusive baseline of marine disease: are diseases in ocean ecosystems increasing? PLoS Biol. 2: e120.10.1371/journal.pbio.0020120Search in Google Scholar PubMed PubMed Central

Whyte, S.K., R.J. Cawthorn and S.E. McGladdery. 1994. QPX (Quahaug Parasite X), a pathogen of Northern Quahaug Mercenaria mercenaria from the Gulf of St.Lawrence, Canada. Dis. Aquat. Organ. 19: 129–136.10.3354/dao019129Search in Google Scholar