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Aquaculture International

, Volume 27, Issue 6, pp 1739–1749 | Cite as

Molecular identification of water molds (oomycetes) associated with chum salmon eggs from hatcheries in Japan and possible sources of their infection

  • Sakiko Orui Sakaguchi
  • Gen Ogawa
  • Hiroaki Kasai
  • Yuichi Shimizu
  • Hiroshi Kitazato
  • Katsunori Fujikura
  • Kiyotaka TakishitaEmail author
Article
  • 42 Downloads

Abstract

Oomycete infection of various freshwater animals, including salmonid eggs, causes significant economic damage to aquaculture worldwide. In this study, we detected oomycetes in infected chum salmon Oncorhynchus keta eggs at two hatcheries in northern Japan, in the source water used for egg incubation, and in the air at the hatcheries to clarify the source(s) of oomycete transmission using a DNA molecular marker. Seven oomycete taxa, belonging to Saprolegniaceae and Pythiaceae, were detected from the infected eggs. From the source water used for egg incubation and the air at the hatcheries, nine oomycete taxa, including those found on infected eggs, were detected, suggesting that both water and air are potential sources of oomycete transmission. There is no report of airborne transmission of these oomycetes detected in this study so far. Regarding protection and sterilization against oomycete infection in aquaculture hatcheries, not only water used at hatcheries but also the air in hatcheries may need to be considered hereafter.

Keywords

Oomycetes Chum salmon eggs Saprolegniaceae Pythiaceae Internal transcribed spacer 2 

Notes

Acknowledgments

We thank the staffs of the two salmon hatcheries for their help with sample collection and Ms. Midori Hagio for DNA analyses.

Funding information

This study was supported by the research project Tohoku Ecosystem-Associated Marine Sciences from the Ministry of Education, Culture, Sports, Science, and Technology.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

References

  1. Ali SE, Evensen Ø, Skaar I (2015) Recent advances in the mitigation of Saprolegnia infections in freshwater fish and their eggs. In: Méndez-Vilas A (ed) The battle against microbial pathogens: basic science, technological advances and educational programs. Formatex Research Center, Badajoz, pp 691–697Google Scholar
  2. Aylor D (2003) Spread of plant disease on a continental scale: role of aerial dispersal of pathogens. Ecology 84:1989–1997CrossRefGoogle Scholar
  3. Braidwood JC (2000) Use of bronopol for the treatment of diseases in fish. Vericore Limited, BasingstokeGoogle Scholar
  4. Bruno DW, van West P, Beakes GW (2011) Saprolegnia and other oomycetes. In: Woo PTK, Bruno DW (eds) Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections. CABI Publishing, Wallingford, pp 669–720Google Scholar
  5. Bruno DW, Noguera P, Poppe T (2013) Fungal and related oomycete infections. In: A Colour Atlas of Salmonid Diseases. Springer, Dordrecht, pp 99–106CrossRefGoogle Scholar
  6. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973CrossRefGoogle Scholar
  7. Czeczuga B, Bartel R, Kiziewicz B, Godlewska A, Muszyńska E (2005) Zoosporic fungi growing on the eggs of sea trout (Salmo trutta m. trutta L.) in river water of varied trophicity. Pol J Environ Stud 14:295–303Google Scholar
  8. Czeczuga B, Semeniuk A, Czeczuga-semeniuk E (2014) Effect of trophically different water bodies on the straminipilous fungal infection of Stenodus genus (Coregoninae) eggs. Afr J Microbiol Res 8:503–510CrossRefGoogle Scholar
  9. Densmore CL, Green DE (2007) Diseases of amphibians. ILAR J 48:235–254CrossRefGoogle Scholar
  10. Diéguez-Uribeondo J, Fregeneda-Grandes JM, Cerenius L, Pérez-Iniesta E, Aller-Gancedo JM, Tellería MT, Söderhäll K, Martín MP (2007) Re-evaluation of the enigmatic species complex Saprolegnia diclina-Saprolegnia parasitica based on morphological, physiological and molecular data. Fungal Genet Biol 44:585–601CrossRefGoogle Scholar
  11. Diéguez-Uribeondo J, García MA, Cerenius L, Kozubíková E, Ballesteros I, Windels C, Weiland J, Kator H, Söderhäll K, Martín MP (2009) Phylogenetic relationships among plant and animal parasites, and saprotrophs in Aphanomyces (Oomycetes). Fungal Genet Biol 46:365–376CrossRefGoogle Scholar
  12. Eissa AE, Abdelsalam M, Tharwat N, Zaki M (2013) Detection of Saprolegnia parasitica in eggs of angelfish Pterophyllum scalare (Cuvier–Valenciennes) with a history of decreased hatchability. Int J Vet Sci Med 1:7–14CrossRefGoogle Scholar
  13. Fernández-Benéitez MJ, Ortiz-Santaliestra ME, Lizana M, Diéguez-Uribeondo J (2011) Differences in susceptibility to Saprolegnia infections among embryonic stages of two anuran species. Oecologia 165:819–826CrossRefGoogle Scholar
  14. Fisher WS, Nilson EH, Shleser RA (1975) Effect of the fungus Haliphthoros milfordensis on the juvenile stages of the American lobster Homarus americanus. J Invertebr Pathol 26:41–45CrossRefGoogle Scholar
  15. Glais I, Montarry J, Corbière R, Pasco C, Marquer B, Magalon H, Andrivon D (2014) Long-distance gene flow outweighs a century of local selection and prevents local adaptation in the Irish famine pathogen Phytophthora infestans. Evol Appl 7:442–452CrossRefGoogle Scholar
  16. Hatai K (1980) Saprolegniasis in salmonids. Fish Pathol 14:199–206 [in Japanese with English abstract]CrossRefGoogle Scholar
  17. Heikkinen J, Mustonen SM, Eskelinen P, Sundberg LR, von Wright A (2013) Prevention of fungal infestation of rainbow trout (Oncorhynchus mykiss) eggs using UV irradiation of the hatching water. Aquac Eng 55:9–15CrossRefGoogle Scholar
  18. Hussein MM, Hatai K, Nomura T (2001) Saprolegniosis in salmonids and their eggs in Japan. J Wildl Dis 37:204–207CrossRefGoogle Scholar
  19. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefGoogle Scholar
  20. Kim DK, Kang DH (2018) UVC-LED irradiation effectively inactivates aerosolized viruses, bacteria, and fungi in a chamber-type air disinfection system. Appl Environ Microbiol 84:e00944-18PubMedPubMedCentralGoogle Scholar
  21. Kimura T, Yoshimizu M, Tajima K (1980) Disinfection of hatchery water supply by ultraviolet (U.V.) irradiation-II. U.V. susceptibility of some fish pathogenic fungi. Fish Pathol 14:133–137 [in Japanese with English abstract]Google Scholar
  22. Kitancharoen N, Hatai K, Yamamoto A (1997) Aquatic fungi developing on eggs of salmonids. J Aquat Anim Health 9:314–316CrossRefGoogle Scholar
  23. Kujundzic E, Matalkah F, Howard CJ, Hernandez M, Miller SL (2006) UV air cleaners and upper-room air ultraviolet germicidal irradiation for controlling airborne bacteria and fungal spores. J Occup Environ Hyg 3:536–546CrossRefGoogle Scholar
  24. Kujundzic E, Hernandez M, Miller SL (2007) Ultraviolet germicidal irradiation inactivation of airborne fungal spores and bacteria in upper-room air and HVAC in-duct configurations. J Environ Eng Sci 6:1–9CrossRefGoogle Scholar
  25. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  26. Lefort V, Longueville JE, Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34:2422–2424CrossRefGoogle Scholar
  27. Lévesque CA, De Cock AWAM (2004) Molecular phylogeny and taxonomy of the genus Pythium. Mycol Res 108:1363–1383CrossRefGoogle Scholar
  28. Liu Y, de Bruijn I, Jack AL, Drynan K, van den Berg AH, Thoen E, Sandoval-Sierra V, Skaar I, van West P, Diéguez-Uribeondo J, van der Voort M, Mendes R, Mazzola M, Raaijmakers JM (2014) Deciphering microbial landscapes of fish eggs to mitigate emerging diseases. ISME J 8:2002–2014CrossRefGoogle Scholar
  29. Miura M, Oono H, Tuchida N, Hatai K, Kiryu T (2005) Control of water mold infection in rainbow trout eggs by using copper fiber. Fish Pathol 40:81–86CrossRefGoogle Scholar
  30. Miura M, Hatai K, Tojo M, Wada S, Kobayashi S, Okazaki T (2010) Visceral mycosis in ayu Plecoglossus altivelis larvae caused by Pythium flevoense. Fish Pathol 45:24–30CrossRefGoogle Scholar
  31. Noga EJ (1993) Water mold infections of freshwater fish: recent advances. Annu Rev Fish Dis 3:291–304CrossRefGoogle Scholar
  32. Ogawa G (2014) Fluctuations in the stock size and return rate, and the damage and recovery from the great East Japan earthquake in hatchery for the chum salmon Oncorhynchus keta in Iwate Prefecture. J North Japan Fish Econ 42:20–23 [in Japanese]Google Scholar
  33. Ota S, Vaulot D, Le Gall F, Yabuki A, Ishida K (2009) Partenskyella glossopodia gen. et sp. nov., the first report of a chlorarachniophyte that lacks a pyrenoid. Protist 160:137–150CrossRefGoogle Scholar
  34. Phillips AJ, Anderson VL, Robertson EJ, Secombes CJ, van West P (2008) New insights into animal pathogenic oomycetes. Trends Microbiol 16:13–19CrossRefGoogle Scholar
  35. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefGoogle Scholar
  36. Sandoval-Sierra JV, Latif-Eugenin F, Martín MP, Zaror L, Diéguez-Uribeondo J (2014a) Saprolegnia species affecting the salmonid aquaculture in Chile and their associations with fish developmental stage. Aquaculture 434:462–469CrossRefGoogle Scholar
  37. Sandoval-Sierra JV, Martín MP, Diéguez-Uribeondo J (2014b) Species identification in the genus Saprolegnia (Oomycetes): defining DNA-based molecular operational taxonomic units. Fungal Biol 118:559–578CrossRefGoogle Scholar
  38. Sudova E, Machova J, Svobodova Z, Vesely T (2007) Negative effects of malachite green and possibilities of its replacement in the treatment of fish eggs and fish: a review. Vet Med 52:527–539CrossRefGoogle Scholar
  39. Suzuki S (1960) Ecological studies on the genus Aphanomyces (aquatic fungi) in Japanese lakes. Jpn J Limnol 21:25–31 [in Japanese]CrossRefGoogle Scholar
  40. Tambong JT, de Cock AWAM, Tinker NA, Lévesque CA (2006) Oligonucleotide array for identification and detection of Pythium species. Appl Environ Microbiol 72:2691–2706CrossRefGoogle Scholar
  41. 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 27:33–42CrossRefGoogle Scholar
  42. Vlasenko ML (1969) Ultraviolet rays as a method for the control of diseases of fish eggs and young fishes. Probl Ichthyol 9:697–705Google Scholar
  43. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703CrossRefGoogle Scholar
  44. Xu Z, Wu Y, Shen F, Chen Q, Tan M, Yao M (2011) Bioaerosol science, technology, and engineering: past, present, and future. Aerosol Sci Technol 45:1337–1349CrossRefGoogle Scholar
  45. Yanong RPE, Erlacher-Reid C (2012) Biosecurity in aquaculture, part 1: an overview. South Reg Aquac Cent 4707:1–16Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Sakiko Orui Sakaguchi
    • 1
  • Gen Ogawa
    • 2
    • 3
  • Hiroaki Kasai
    • 4
  • Yuichi Shimizu
    • 2
  • Hiroshi Kitazato
    • 1
  • Katsunori Fujikura
    • 1
  • Kiyotaka Takishita
    • 1
    • 5
    Email author
  1. 1.Japan Agency for Marine-Earth Science and TechnologyYokosukaJapan
  2. 2.Iwate Fisheries Technology CenterIwateJapan
  3. 3.Iwate Prefectural Government Department of Agriculture, Forestry and FisheriesIwateJapan
  4. 4.School of Marine BioscienceKitasato University, 1-15-1 Kitasato, Minami-kuSagamiharaJapan
  5. 5.International College of Arts and SciencesFukuoka Women’s UniversityFukuokaJapan

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