Fungal Secondary Invaders of Fish

  • Nicolas Derome
  • Jeff Gauthier
  • Sébastien Boutin
  • Martin Llewellyn
Part of the Advances in Environmental Microbiology book series (AEM, volume 3)


Fungal and fungal-like opportunistic pathogens are of primary concern in aquaculture, because they affect a wide range of hosts (both vertebrate and invertebrate) and are very difficult to diagnose, control, or treat. One of the reasons for this difficulty is that some diseases caused by fungal and fungal-like pathogens have no clear external symptoms. Furthermore, the increasing emergence of fungal and fungal-like opportunistic pathogens is correlated with modern production cycles, relying on intensive techniques that often lead to poor water quality and high population density. This combination of stress factors is known as a catalyst for opportunistic infections in aquaculture due to the direct and indirect effects on the host immune response. Therefore, those suboptimal rearing conditions may lead to homeostatic imbalance in favor of secondary invaders. We have therefore covered fungal and fungal-like fish pathogens with significant impact in worldwide aquaculture (black yeasts, Oomycetes, and Microsporidia), as well as control and prevention strategies for pathogens belonging to these groups.


Opportunistic pathogens Fish Teleosts Black yeasts Oomycetes Microsporidia Control Prevention 


  1. Adl SM, Simpson AGB, Farmer MA et al (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451. doi: 10.1111/j.1550-7408.2005.00053.x PubMedCrossRefGoogle Scholar
  2. Ajello L (1986) Hyalohyphomycosis and phaeohyphomycosis: two global disease entities of public health importance. Eur J Epidemiol 2:243–251PubMedCrossRefGoogle Scholar
  3. Ajello L, McGinnis MR, Camper J (1977) An outbreak of phaeohyphomycosis in rainbow trout caused by Scolecobasidium humicola. Mycopathologia 62:15–22PubMedCrossRefGoogle Scholar
  4. Ali SE, Thoen E, Evensen Ø, Skaar I (2014) Boric acid inhibits germination and colonization of Saprolegnia spores in vitro and in vivo. PLoS One 9:e91878. doi: 10.1371/journal.pone.0091878 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Andreou D, Gozlan RE, Stone D et al (2011) Sphaerothecum destruens pathology in cyprinids. Dis Aquat Organ 95:145–151. doi: 10.3354/dao02356 PubMedCrossRefGoogle Scholar
  6. Andreou D, Arkush KD, Guégan J-F, Gozlan RE (2012) Introduced pathogens and native freshwater biodiversity: a case study of Sphaerothecum destruens. PLoS One 7:e36998. doi: 10.1371/journal.pone.0036998 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Badali H, De Hoog GS, Curfs-Breuker I et al (2009) In vitro activities of eight antifungal drugs against 70 clinical and environmental isolates of Alternaria species. J Antimicrob Chemother 63:1295–1297. doi: 10.1093/jac/dkp109 PubMedCrossRefGoogle Scholar
  8. Badali H, de Hoog GS, Sudhadham M, Meis JF (2011) Microdilution in vitro antifungal susceptibility of Exophiala dermatitidis, a systemic opportunist. Med Mycol 49:819–824. doi: 10.3109/13693786.2011.583285 PubMedGoogle Scholar
  9. Balajee SA, Sigler L, Brandt ME (2007) DNA and the classical way: identification of medically important molds in the 21st century. Med Mycol 45:475–490. doi: 10.1080/13693780701449425 PubMedCrossRefGoogle Scholar
  10. Baldauf SL (2003) The deep roots of eukaryotes. Science 300:1703–1706. doi: 10.1126/science.1085544 PubMedCrossRefGoogle Scholar
  11. Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26. doi: 10.1016/0959-8030(91)90019-G CrossRefGoogle Scholar
  12. Bhattacharya U (1988) Scolebasidium humicola, a new fungal fish infection from India. Environ Ecol 6:532–3Google Scholar
  13. Boutin S, Bernatchez L, Audet C, Derôme N (2012) Antagonistic effect of indigenous skin bacteria of brook charr (Salvelinus fontinalis) against Flavobacterium columnare and F.psychrophilum. Vet Microbiol 155:355–361. doi: 10.1016/j.vetmic.2011.09.002 PubMedCrossRefGoogle Scholar
  14. Boutin S, Audet C, Derome N (2013a) Probiotic treatment by indigenous bacteria decreases mortality without disturbing the natural microbiota of Salvelinus fontinalis. Can J Microbiol 59:662–670. doi: 10.1139/cjm-2013-0443 PubMedCrossRefGoogle Scholar
  15. Boutin S, Bernatchez L, Audet C, Derôme N (2013b) Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS One 8, e84772. doi: 10.1371/journal.pone.0084772 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Branson E (2002) Efficacy of bronopol against infection of rainbow trout (Oncorhynchus mykiss) with the fungus Saprolegnia species. Vet Rec 151:539–541PubMedCrossRefGoogle Scholar
  17. Bruno D, West PV, Beakes G (2011) Saprolegnia and other oomycetes. In: Woo P, Bruno D (eds) Fish diseases and disorders: viral, bacterial and fungal infections, 2nd edn. CABI, Wallingford, pp 669–720CrossRefGoogle Scholar
  18. Callinan RB, Fraser GC, Virgona JL (1989) Pathology of red spot disease in sea mullet, Mugil cephalus L., from eastern Australia. J Fish Dis 12:467–479. doi: 10.1111/j.1365-2761.1989.tb00558.x CrossRefGoogle Scholar
  19. Callinan R, Paclibare J, Bondad-Reantaso M et al (1995) Aphanomyces species associated with epizootic ulcerative syndrome (EUS) in the Philippines and red spot disease (RSD) in Australia: preliminary comparative studies. Dis Aquat Organ 21:233–238. doi: 10.3354/dao021233 CrossRefGoogle Scholar
  20. Campbell RE, Lilley JH, Taukhid V et al (2001) In vitro screening of novel treatments for Aphanomyces invadans. Aquacult Res 32:223–233. doi: 10.1046/j.1365-2109.2001.00551.x CrossRefGoogle Scholar
  21. Carbajal-González MT, Fregeneda-Grandes JM, Suárez-Ramos S et al (2011) Bacterial skin flora variation and in vitro inhibitory activity against Saprolegnia parasitica in brown and rainbow trout. Dis Aquat Organ 96:125–135. doi: 10.3354/dao02391 PubMedCrossRefGoogle Scholar
  22. Carbajal-González MT, Fregeneda-Grandes JM, González-Palacios C, Aller-Gancedo JM (2013) Adhesion to brown trout skin mucus, antagonism against cyst adhesion and pathogenicity to rainbow trout of some inhibitory bacteria against Saprolegnia parasitica. Dis Aquat Organ 104:35–44. doi: 10.3354/dao02582 PubMedCrossRefGoogle Scholar
  23. Chauvier G, Mortier-Gabet J (1982) Recherches sur les possibilités de traitement chimique de l’ichthyophonose. Rev Fr AquarolNancy 9:90Google Scholar
  24. Das BK, Pattnaik P, Debnath C et al (2013) Effect of β-glucan on the immune response of early stage of Anabas testudineus (Bloch) challenged with fungus Saprolegnia parasitica. SpringerPlus 2:197. doi: 10.1186/2193-1801-2-197 PubMedPubMedCentralCrossRefGoogle Scholar
  25. David JC, Kirk P (1997) Index of fungi. In: Ainsworth and Bisby’s dictionary of the Fungi, 8th edn. CAB International, Wallingford, UK, p 706Google Scholar
  26. De Hoog GS (1993) Evolution of black yeasts: possible adaptation to the human host. Antonie Van Leeuwenhoek 63:105–109PubMedCrossRefGoogle Scholar
  27. De Hoog GS, McGinnis MR (1987) Ascomycetous black yeasts. Stud Mycol 30:187–199Google Scholar
  28. De Hoog GS, Vicente VA, Najafzadeh MJ et al (2011) Waterborne Exophiala species causing disease in cold-blooded animals. Persoonia 27:46–72. doi: 10.3767/003158511X614258 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Didier ES (2005) Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop 94:61–76. doi: 10.1016/j.actatropica.2005.01.010 PubMedCrossRefGoogle Scholar
  30. Doty MS, Slater DW (1946) A new species of heterosporium pathogenic on young chinook salmon. Am Midl Nat 36:663. doi: 10.2307/2421459 CrossRefGoogle Scholar
  31. Egusa S, Masuda N (1971) A new fungal of Plecoglossus altivelis. Fish Pathol 6:41–46. doi: 10.3147/jsfp.6.41 CrossRefGoogle Scholar
  32. Faisal M, Elsayed E, Fitzgerald SD et al (2007) Outbreaks of phaeohyphomycosis in the chinook salmon (Oncorhynchus tshawytscha) caused by Phoma herbarum. Mycopathologia 163:41–48. doi: 10.1007/s11046-006-0084-z PubMedCrossRefGoogle Scholar
  33. Ferrer C, Colom F, Frasés S, Mulet E, Abad JL, Alió JL (2001) Detection and identification of fungal pathogens by PCR and by ITS2 and 5.8S ribosomal DNA typing in ocular infections. J Clin Microbiol 39:2873–2879. doi: 10.1128/JCM.39.8.2873-2879.2001 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Firouzbakhsh F, Ebrahimzadeh Mousavi H, Khosravi A (2005) Isolation and identification of pathogenic and saprophytic fungi from gill lesion in cultivated cyprinids (common carp, silver carp and grass carp). J Vet Res 60:15–9Google Scholar
  35. Foy DS, Trepanier LA (2010) Antifungal treatment of small animal veterinary patients. Vet Clin North Am Small Anim Pract 40:1171–1188. doi: 10.1016/j.cvsm.2010.07.006 PubMedCrossRefGoogle Scholar
  36. Franco-Sierra A (1994) Estudio de las infecciones por el hongo Ichthyophonus sp. en peces de interés comercial. Universitat Autónoma de BarcelonaGoogle Scholar
  37. Fraser GC, Callinan RB, Calder LM (1992) Aphanomyces species associated with red spot disease: an ulcerative disease of estuarine fish from eastern Australia. J Fish Dis 15:173–181. doi: 10.1111/j.1365-2761.1992.tb00651.x CrossRefGoogle Scholar
  38. Fregeneda-Grandes JM, Carbajal-González MT, Aller-Gancedo JM (2009) Prevalence of serum antibodies against Saprolegnia parasitica in wild and farmed brown trout Salmo trutta. Dis Aquat Organ 83:17–22. doi: 10.3354/dao01999 PubMedCrossRefGoogle Scholar
  39. Gaskins JE, Cheung PJ (1986) Exophiala pisciphila. A study of its development. Mycopathologia 93:173–184PubMedCrossRefGoogle Scholar
  40. Gill EE, Fast NM (2006) Assessing the microsporidia-fungi relationship: combined phylogenetic analysis of eight genes. Gene 375:103–109. doi: 10.1016/j.gene.2006.02.023 PubMedCrossRefGoogle Scholar
  41. Gjessing MC, Davey M, Kvellestad A, Vrålstad T (2011) Exophiala angulospora causes systemic inflammation in atlantic cod Gadus morhua. Dis Aquat Organ 96:209–219. doi: 10.3354/dao02381 PubMedCrossRefGoogle Scholar
  42. Gozlan RE, St-Hilaire S, Feist SW et al (2005) Biodiversity: disease threat to European fish. Nature 435:1046–1046. doi: 10.1038/4351046a PubMedCrossRefGoogle Scholar
  43. Gozlan RE, Peeler EJ, Longshaw M et al (2006) Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe. Microbes Infect 8:1358–1364. doi: 10.1016/j.micinf.2005.12.010 PubMedCrossRefGoogle Scholar
  44. Grünwald NJ, Werres S, Goss EM et al (2012) Phytophthora obscura sp. nov., a new species of the novel Phytophthora subclade 8d. Plant Pathol 61:610–622. doi: 10.1111/j.1365-3059.2011.02538.x CrossRefGoogle Scholar
  45. Harkness JE, Guselle NJ, Speare DJ (2013) Demonstrated efficacy of a pilot heterologous whole-spore vaccine against Microsporidial gill disease in rainbow trout. Clin Vaccine Immunol 20:1483–1484. doi: 10.1128/CVI.00340-13 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hatai K, Hoshiai G (1992) Mass mortality in cultured coho salmon (Oncorhynchus kisutch) due to Saprolegnia parasitica coker. J Wildl Dis 28:532–536. doi: 10.7589/0090-3558-28.4.532 PubMedCrossRefGoogle Scholar
  47. Hatai K, Egusa S, Takahashi S, Ooe K (1977) Study on the pathogenic fungus of mycotic granulomatosis—I. Fish Pathol 12:129–133. doi: 10.3147/jsfp.12.129 CrossRefGoogle Scholar
  48. Hershberger PK, Pacheco CA, Gregg JL (2008) Inactivation of Ichthyophonus spores using sodium hypochlorite and polyvinyl pyrrolidone iodine. J Fish Dis 31:853–858. doi: 10.1111/j.1365-2761.2008.00959.x PubMedCrossRefGoogle Scholar
  49. Hibbett DS, Binder M, Bischoff JF et al (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547. doi: 10.1016/j.mycres.2007.03.004 PubMedCrossRefGoogle Scholar
  50. Higgins MJ, Kent ML, Moran JD et al (1998) Efficacy of the fumagillin analog TNP-470 for Nucleospora salmonis and Loma salmonae infections in chinook salmon Oncorhynchus tshawytscha. Dis Aquat Organ 34:45–49. doi: 10.3354/dao034045 PubMedCrossRefGoogle Scholar
  51. Hontoria F, González MA, Sitjà-Bobadilla A et al (2009) Ketoconazole inhibits the growth and development of Ichthyophonus sp. (Mesomycetozoa) in vitro. J Eukaryot Microbiol 56:484–491. doi: 10.1111/j.1550-7408.2009.00427.x PubMedCrossRefGoogle Scholar
  52. Jacobson ES (2000) Pathogenic roles for fungal melanins. Clin Microbiol Rev 13:708–717PubMedPubMedCentralCrossRefGoogle Scholar
  53. James TY, Kauff F, Schoch CL et al (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822. doi: 10.1038/nature05110 PubMedCrossRefGoogle Scholar
  54. Keeling PJ, Luker MA, Palmer JD (2000) Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol Biol Evol 17:23–31PubMedCrossRefGoogle Scholar
  55. Kent ML, Speare DJ (2005) Review of the sequential development of Loma salmonae (Microsporidia) based on experimental infections of rainbow trout (Oncorhynchus mykiss) and Chinook salmon (O. tshawytscha). Folia Parasitol (Praha) 52:63–68CrossRefGoogle Scholar
  56. Kiryu Y, Shields JD, Vogelbein WK et al (2003) Infectivity and pathogenicity of the oomycete Aphanomyces invadans in Atlantic menhaden Brevoortia tyrannus. Dis Aquat Organ 54:135–146. doi: 10.3354/dao054135 PubMedCrossRefGoogle Scholar
  57. Kiseleva M, Balabanova L, Elyakova L et al (2014) Effect of treatment of chum salmon Oncorhynchus keta (Walbaum) eggs with 1,3;1,6-β-D-glucans on their development and susceptibility to Saprolegnia infection. J Fish Dis 37:3–10. doi: 10.1111/jfd.12043 PubMedCrossRefGoogle Scholar
  58. Kocan R, Hershberger P (2006) Differences in Ichthyophonus prevalence and infection severity between upper Yukon River and Tanana River chinook salmon, Oncorhynchus tshawytscha (Walbaum), stocks. J Fish Dis 29:497–503. doi: 10.1111/j.1365-2761.2006.00743.x PubMedCrossRefGoogle Scholar
  59. Kurata O, Munchan C, Wada S et al (2008) Novel Exophiala infection involving ulcerative skin lesions in Japanese flounder Paralichthys olivaceus. Fish Pathol 43:35–44. doi: 10.3147/jsfp.43.35 CrossRefGoogle Scholar
  60. Langdon J, McDonald W (1987) Cranial Exophiala pisciphila infection in Salmo salar in Australia. Bull Eur Assoc Fish Pathol 7:35–7Google Scholar
  61. Lilley JH, Callinan R, Chinabut S et al (1998) Epizootic ulcerative syndrome (EUS) technical handbook. Aquatic Animal Health Research Institute, BangkokGoogle Scholar
  62. Liu YJ, Hodson MC, Hall BD (2006) Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of Kingdom Fungi inferred from RNA polymerase II subunit genes. BMC Evol Biol 6:74. doi: 10.1186/1471-2148-6-74 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Liu Y, de Bruijn I, Jack AL et al (2014) Deciphering microbial landscapes of fish eggs to mitigate emerging diseases. ISME J. doi: 10.1038/ismej.2014.44 Google Scholar
  64. Lom J, Dyková I (2005) Microsporidian xenomas in fish seen in wider perspective. Folia Parasitol (Praha) 52:69–81CrossRefGoogle Scholar
  65. Malathi K, Rajendran K (2012) Isolation of fungi and bacteria from various tissues of freshwater fish Channa Punctatus (BLOCH). Asian J Microbiol Biotechnol Environ Sci 14:553–556Google Scholar
  66. McGinnis MR (1983) Chromoblastomycosis and phaeohyphomycosis: new concepts, diagnosis, and mycology. J Am Acad Dermatol 8:1–16PubMedCrossRefGoogle Scholar
  67. McGinnis MR, Ajello L (1974) A new species of Exophiala isolated from channel catfish. Mycologia 66:518–520PubMedCrossRefGoogle Scholar
  68. McKenzie RA, Hall WTK (1976) Dermal ulceration of mullet (mugil Cephalus). Aust Vet J 52:230–231. doi: 10.1111/j.1751-0813.1976.tb00076.x PubMedCrossRefGoogle Scholar
  69. McVicar AH (1982) Ichthyophonus infections in fish. Microbial Dis Fish 243–269Google Scholar
  70. McVicar AH (1999) Ichthyophonus and related organisms. In: Woo PTK, Bruno DW (eds) Fish diseases and disorders: viral, bacterial and fungal infections. CAB, WallingfordGoogle Scholar
  71. Mendoza L, Taylor JW, Ajello L (2002) The class mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annu Rev Microbiol 56:315–344. doi: 10.1146/annurev.micro.56.012302.160950 PubMedCrossRefGoogle Scholar
  72. Mohamed A, Refai MK (2010) The assessment of mycotic settlement of freshwater fishes in Egypt. J Am Sci 6:595–602Google Scholar
  73. Nyaoke A, Weber ES, Innis C et al (2009) Disseminated phaeohyphomycosis in weedy seadragons (Phyllopteryx taeniolatus) and leafy seadragons (Phycodurus eques) caused by species of Exophiala, including a novel species. J Vet Diagn Invest 21:69–79PubMedCrossRefGoogle Scholar
  74. Okamura B, Feist SW (2011) Emerging diseases in freshwater systems. Freshw Biol 56:627–637. doi: 10.1111/j.1365-2427.2011.02578.x CrossRefGoogle Scholar
  75. Oono H, Hatai K (2007) Antifungal activities of bronopol and 2-methyl-4-isothiazolin-3-one (MT) against saprolegnia. Biocontrol Sci 12:145–148PubMedCrossRefGoogle Scholar
  76. Otis EJ, Wolke RE, Blazer VS (1985) Infection of Exophiala salmonis in Atlantic salmon (Salmo salar L.). J Wildl Dis 21:61–64PubMedCrossRefGoogle Scholar
  77. Paps J, Medina-Chacón LA, Marshall W et al (2013) Molecular phylogeny of unikonts: new insights into the position of apusomonads and ancyromonads and the internal relationships of opisthokonts. Protist 164:2–12. doi: 10.1016/j.protis.2012.09.002 PubMedCrossRefGoogle Scholar
  78. Ragan MA, Goggin CL, Cawthorn RJ et al (1996) A novel clade of protistan parasites near the animal-fungal divergence. Proc Natl Acad Sci USA 93:11907–11912PubMedPubMedCentralCrossRefGoogle Scholar
  79. Reuter R, Ham W, Davis S (2003) Exophiala sp. infection in captured King George whiting, Sillaginodes punctata. Bull Eur Assoc Fish Pathol 23:128–34Google Scholar
  80. Roberts RJ, Frerichs GN, Tonguthai K, Chinabut S (1994) Epizootic ulcerative syndrome of farmed and wild fishes—a review. In: Roberts RJ, Muir JF (eds) Recent advances in aquaculture, vol 5. Blackwell, Oxford, pp 207–239Google Scholar
  81. Robinette D, Wada S, Arroll T, Levy MG, Miller WL, Noga EJ (1998) Antimicrobial activity in the skin of the channel catfish Ictalurus punctatus: characterization of broad-spectrum histone-like antimicrobial proteins. Cell Mol Life Sci 54:467–475PubMedCrossRefGoogle Scholar
  82. Rodriguez RJ, Acosta D (1996) Inhibition of mitochondrial function in isolated rat liver mitochondria by azole antifungals. J Biochem Toxicol 11:127–131. doi: 10.1002/(SICI)1522-7146(1996)11:3<127::AID-JBT4>3.0.CO;2-M PubMedCrossRefGoogle Scholar
  83. Rodríguez-Tovar LE, Becker JA, Markham RJF, Speare DJ (2006) Induction time for resistance to microsporidial gill disease caused by Loma salmonae following vaccination of rainbow trout (Oncorhynchus mykiss) with a spore-based vaccine. Fish Shellfish Immunol 21:170–175. doi: 10.1016/j.fsi.2005.11.009 PubMedCrossRefGoogle Scholar
  84. Rodriguez-Tovar LE, Markham RJF, Speare DJ, Sheppard J (2006) Cellular immunity in salmonids infected with the microsporidial parasite Loma salmonae or exposed to non-viable spores. Vet Immunol Immunopathol 114:72–83. doi: 10.1016/j.vetimm.2006.07.006 PubMedCrossRefGoogle Scholar
  85. Ross AJ, Yasutake WT (1973) Scolecobasidium humicola, a fungal pathogen of fish. J Fish Res Board Can 30:994–995. doi: 10.1139/f73-161 CrossRefGoogle Scholar
  86. Ruibal C, Gueidan C, Selbmann L et al (2009) Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud Mycol 64:123–133S7. doi: 10.3114/sim.2009.64.06 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Saikia D, Kamilya D (2012) Immune responses and protection in catla (Catla catla) vaccinated against epizootic ulcerative syndrome. Fish Shellfish Immunol 32:353–359. doi: 10.1016/j.fsi.2011.11.030 PubMedCrossRefGoogle Scholar
  88. Sarowar MN, van den Berg AH, McLaggan D et al (2013) Saprolegnia strains isolated from river insects and amphipods are broad spectrum pathogens. Fungal Biol 117:752–763. doi: 10.1016/j.funbio.2013.09.002 PubMedCrossRefGoogle Scholar
  89. Schaumann K, Priebe K (1994) Ochroconis humicola causing muscular black spot disease of Atlantic salmon (Salmo salar). Can J Bot 72:1629–1634. doi: 10.1139/b94-200 CrossRefGoogle Scholar
  90. Silphaduang U, Hatai K, Wada S, Noga E (2000) Cladosporiosis in a tomato clownfish (Amphiprion frenatus). J Zoo Wildl Med 31:259–261PubMedCrossRefGoogle Scholar
  91. Spanggaard B, Skouboe P, Rossen L, Taylor JW (1996) Phylogenetic relationships of the intercellular fish pathogen Ichthyophonus hoferi and fungi, choanoflagellates and the rosette agent. Mar Biol 126:109–115. doi: 10.1007/BF00571382 CrossRefGoogle Scholar
  92. Speare DJ, Ritter G, Schmidt H (1998) Quinine hydrochloride treatment delays xenoma formation and dissolution in rainbow trout challenged with Loma salmonae. J Comp Pathol 119:459–465PubMedCrossRefGoogle Scholar
  93. Speare DJ, Athanassopoulou F, Daley J, Sanchez JG (1999) A preliminary investigation of alternatives to fumagillin for the treatment of Loma salmonae infection in rainbow trout. J Comp Pathol 121:241–248. doi: 10.1053/jcpa.1999.0325 PubMedCrossRefGoogle Scholar
  94. Speare DJ, Markham RJF, Guselle NJ (2007) Development of an effective whole-spore vaccine to protect against microsporidial gill disease in rainbow trout (Oncorhynchus mykiss) by using a low-virulence strain of Loma salmonae. Clin Vaccine Immunol 14:1652–1654. doi: 10.1128/CVI.00365-07 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Stecher B, Maier L, Hardt W-D (2013) “Blooming” in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11:277–284. doi: 10.1038/nrmicro2989 PubMedCrossRefGoogle Scholar
  96. Strongman D, Morrison C, McClelland G (1997) Lesions in the musculature of captive American plaice Hippoglossoides platessoides caused by the fungus Hormoconis resinae (Deuteromycetes). Dis Aquat Organ 28:107–113. doi: 10.3354/dao028107 CrossRefGoogle Scholar
  97. Torruella G, Derelle R, Paps J et al (2012) Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. Mol Biol Evol 29:531–544. doi: 10.1093/molbev/msr185 PubMedCrossRefGoogle Scholar
  98. Valenzuela A, Campos V, Yañez F et al (2012) Application of artificial photoperiod in fish: a factor that increases susceptibility to infectious diseases? Fish Physiol Biochem 38:943–950. doi: 10.1007/s10695-011-9580-2 PubMedCrossRefGoogle Scholar
  99. Van den Berg AH, McLaggan D, Diéguez-Uribeondo J, van West P (2013) The impact of the water moulds Saprolegnia diclina and Saprolegnia parasitica on natural ecosystems and the aquaculture industry. Fungal Biol Rev 27:33–42. doi: 10.1016/j.fbr.2013.05.001 CrossRefGoogle Scholar
  100. Van Duijn C (1956) Diseases of fishes, 1st edn. Water Life, London, UKGoogle Scholar
  101. Vanden Bossche H, Marichal P, Gorrens J et al (1988) Mode of action studies: basis for the search of new antifungal drugs. Ann N Y Acad Sci 544:191–207. doi: 10.1111/j.1749-6632.1988.tb40404.x PubMedCrossRefGoogle Scholar
  102. Van Muiswinkel WB, Nakao M (2014) A short history of research on immunity to infectious diseases in fish. Dev Comp Immunol 43:130–150. doi: 10.1016/j.dci.2013.08.016 PubMedCrossRefGoogle Scholar
  103. Vishwanath TS (1997) Mycotic granulomatosis and seasonality are the consistent features of epizootic ulcerative syndrome of fresh and brackish water fishes of Karnataka, India. Asian Fish Sci 10:155–60Google Scholar
  104. Vitale RG, Perez-Blanco M, De Hoog GS (2009) In vitro activity of antifungal drugs against Cladophialophora species associated with human chromoblastomycosis. Med Mycol 47:35–40. doi: 10.1080/13693780802566333 PubMedCrossRefGoogle Scholar
  105. Voigt K, Marano AV, Gleason F (2013) Ecological and economical importance of parasitic and zoosporic true Fungi. In: Kempken F (ed) The Mycota vol XI: agricultural applications, 2nd edn. Springer, BerlinGoogle Scholar
  106. Wang H, Xu Z, Gao L, Hao B (2009) A fungal phylogeny based on 82 complete genomes using the composition vector method. BMC Evol Biol 9:195. doi: 10.1186/1471-2148-9-195 PubMedPubMedCentralCrossRefGoogle Scholar
  107. Willoughby LG (1994) Fungi and fish diseases. Pisces, StirlingGoogle Scholar
  108. Willoughby LG, Roberts RJ, Chinabut S (1995) Aphanomyces invaderis sp. nov., the fungal pathogen of freshwater tropical fish affected by epizootic ulcerative syndrome. J Fish Dis 18:273–276. doi: 10.1111/j.1365-2761.1995.tb00302.x CrossRefGoogle Scholar
  109. Yanong RPE (2003) Fungal diseases of fish. Vet Clin North Am Exot Anim Pract 6:377–400PubMedCrossRefGoogle Scholar
  110. Zahran E, Risha E (2013) Protective role of adjuvant and potassium permanganate on oxidative stress response of Nile tilapia (Oreochromis niloticus) challenged with Saprolegnia ferax. SpringerPlus 2:94. doi: 10.1186/2193-1801-2-94 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Zeng JS, Sutton DA, Fothergill AW, Rinaldi MG, Harrak MJ, de Hoog GS (2007) Spectrum of clinically relevant Exophiala species in the United States. J Clin Microbiol 45:3713–3720. doi: 10.1128/JCM.02012-06 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Nicolas Derome
    • 1
    • 2
  • Jeff Gauthier
    • 1
    • 2
  • Sébastien Boutin
    • 1
    • 2
    • 3
  • Martin Llewellyn
    • 1
    • 2
    • 4
  1. 1.Institut de Biologie Intégrative et des Systèmes (IBIS)Université LavalQuébecCanada
  2. 2.Département de BiologieUniversité LavalQuébecCanada
  3. 3.Department of Infectious Disease, Medical Microbiology and HygieneUniversität HeidelbergHeidelbergGermany
  4. 4.Molecular Ecology and Fisheries Genetics Laboratory, School of Biological SciencesBangor UniversityGwyneddUK

Personalised recommendations