The current status of Saprolegniales in Iran: calling mycologists for better taxonomic and ecological resolutions

Abtahi B, Shafiezade P, Nazari RM, Rassouli A. 2006. Comparison of antifungal therapeutic indices of formalin, malachite green, and potassium permanganate in treating Persian Sturgeon eggs. Journal of Applied Ichthyology 22(1): 291–293.

Adel M, Dadar M, Zorriehzahra MJ, Elahi R, Stadtlander T. 2020. Antifungal activity and chemical composition of Iranian medicinal herbs against fish pathogenic fungus, Saprolegnia parasitica. Iranian Journal of Fisheries Sciences 19(6): 3239–3254.

Armand A, Khodaparast SA, Masigol H, Grossart HP. 2020. Screening of fungal strains isolated from dead insects for production of plant litter-degrading enzymes. Mycologia Iranica 7(1): 155–61.

Moghaddam A, Hajimoradloo A, Ghiasi M, Ghorbani R. 2012. In vitro inhibition of growth in Saprolegnia sp. isolated from the eggs of Persian sturgeon Acipenser persicus (Pisces: Acipenseriformes) by Pseudomonas aeroginosa (PTCC: 1430). Caspian journal of environmental sciences 11(2): 233–240.

Akhlaghi A, Bahaoodini AA. 2012. Comparison of several treatment methods against saprolegniosis in rainbow trout fertilized eggs. Veterinary Researches & Biological Products 25(1): 18–24.

Alishah N, Firouzbakhsh F, Mehrabi Z. 2019. Bathing effects of nettle (Urtica dioica) hydroalcoholic extract on immunological and hematological indices in rainbow trout (Oncorhynchus mykiss) infected with Saprolegnia fungal. Iranian Scientific Fisheries Journal 28(2): 55–67.

Amiri H, Meshkini S. 2019. Antifungal effects of Achillea officinolis and Matricaria chamomilla plant extracts on control infection of rainbow trout eggs by Saprolegnia parasitica. Journal of Veterinary Microbiology 15(1): 97–107.

Azizi I, Hosseinifard SM, Rohi S, Moghtader H. 2014. Investigation and identification of fungal infection of Caspian salmon (Salmo trutta caspius) in fish farms of Mazandaran province. Animal biology 6(3): 45–53.

Azizi IG, Fard MH, Tahmasbipour S. 2012. The Effect of aquatic and alcoholic extracts of Citrullus colocynthis on growth of the Saprolegnia parasitica. World Journal of Fish and Marine Sciences 4: 258–62.

Bolboli Z, Mostowfizadeh-Ghalamfarsa R. 2019. Isolation and identification of aquatic saprolegnious stramenopiles in Fars and Kermanshah provinces (west of Iran). Rostaniha 20(1): 14–28.

Buaya A, Kraberg A, Thines M. 2019. Dual culture of the oomycete Lagenisma coscinodisci Drebes and Coscinodiscus diatoms as a model for plankton/parasite interactions. Helgoland Marine Research 73(1): 1–6.

Caruana S, Yoon GH, Freeman MA, Mackie JA, Shinn AP. 2012. The efficacy of selected plant extracts and bioflavonoids in controlling infections of Saprolegnia australis (Saprolegniales; Oomycetes). Aquaculture 358: 146–154.

Culp SJ, Mellick PW, Trotter RW, Greenlees KJ, Kodell RL, Beland FA. 2006. Carcinogenicity of malachite green chloride and leucomalachite green in B6C3F1 mice and F344 rats. Food and Chemical Toxicology 44(8): 1204–1212.

Cuenca Cambronero M, Marshall H, De Meester L, Davidson TA, Beckerman AP, Orsini L. 2018. Predictability of the impact of multiple stressors on the keystone species Daphnia. Scientific Reports 8(1): 1–11.

De Souza JI, Gleason FH, Ansari MA, Lastra CC, Garcia JJ, Pires-Zottarelli CL, Marano AV. 2014. Fungal and oomycete parasites of Chironomidae, Ceratopogonidae and Simuliidae (Culicomorpha, Diptera). Fungal Biology Reviews 28(1): 13–23.

Fadaeifard F, Bahrami H, Rahimi E, Najafipoor A. 2011. Freshwater fungi isolated from eggs and broodstocks with an emphasis on Saprolegnia in rainbow trout farms in west Iran. African Journal of Microbiology Research 5(22): 3647–3651.

Firouzbakhsh F, Zolfaghari A, Mehrabi Z, Khalesi MK. 2015. In vitro antifungal activity of Nettle (Urtica dioica) and Basil (Ocimum basilicum) extracts on Saprolegnia parasitica. Journal of Animal Environment 7(3): 211–216.

Firouzbakhsh F, Afsarian MH, Hooshangi S, Badali H. 2014. Evaluation of in vitro antifungal activity of Foeniculum, Achillea, Satureja, Cinnamomum and Artemisia against Saprolegnia parasitica. Arak Medical University Journal 17(5): 60–69.

Firouzbakhsh F, Mehrabi Z, Heydari M, Khalesi MK, Tajick MA. 2014a. Protective effects of a synbiotic against experimental Saprolegnia parasitica infection in rainbow trout (Oncorhynchus mykiss). Aquaculture Research 45(4): 609–618.

Gaulin E, Jacquet C, Bottin A, Dumas B. 2007. Root rot disease of legumes caused by Aphanomyces euteiches. Molecular Plant Pathology 8(5): 539–548.

Ghasemi Pirbalouti A, Taheri M, Raiesi M, Bahrami H, Abdizadeh R. 2009. In vitro antifungal activity of plant extracts on Saprolegnia parasitica from cutaneous lesions of rainbow trout (Oncorhynchus mykiss) eggs. Journal of Food, Agriculture & Environment 7(2): 94–96.

Ghiasi M, Khosravi AL, Soltani M, Sharifpour I, Binaii M, Ebrahimzadeh Mosavi H, Bahonar A. 2014. Evaluation of physiological aspects and molecular identification of Saprolegnia isolates from rainbow trout (Oncorhynchus mykiss) and Caspian trout (Salmo trutta caspius) eggs based on RAPD–PCR. Iranian fisheries science research institute 22(4): 82–93.

Ghiasi M, Shokri H, Binai M, Farabi SMV, Saeidi AA. 2012. Identification and comparison of the frequency of fungal agents isolated from the eggs of whitefish (Rutilus frisii kutum) in Mazandaran province. Journal of aquaculture development 6(1): 79–90.

Ghiasi M, Khosravi AR, Soltani M, Binaii M, Shokri H, Tootian Z, Rostamibashman M, Ebrahimzademousavi H. 2010. Characterization of Saprolegnia isolates from Persian sturgeon (Acipencer persicus) eggs based on physiological and molecular data. Journal de mycologie médicale 20(1): 1–7.

Ghorbani E, Azadikhah D. 2019. Identification and determination of prevalence of saprophytic fungi in the larval stage of the rainbow trout (Oncorhynchus mykiss) in hatcheries of west Azarbaijan province. Veterinary clinical pathology the quarterly scientific journal 13(49): 91-99.

Ggonani S, Taghavizad R. 2021. The effect of methanolic, aqueous and hydroalcoholic extracts of peacock and lemongrass on fish (Saprolegnia) in comparison with the effect of antibiotics. Aquaculture development (biological sciences) 14(4): 83–91.

Golchin MA, Jarkani Bayat S, Tarhami M. 2017. Experimental evaluation of antifungal effect of thyme extract (Thymus vulgaris) and marjoram (Origanum vulgare) on Saprolegnia fungi isolated from rainbow trout in Shahid Motahari breeding complex in Yasou. New technologies in aquaculture development (fisheries) 10(4): 11–18.

Grossart HP, Hassan EA, Masigol H, Arias-Andres M, Rojas-Jimenez K. 2020. Inland water fungi in the Anthropocene: Current and future perspectives. In: The Encyclopedia of Inland Waters, (Kendra Cheruvelil eds.): Elsevier Inc, Netherlands. https://doi.org/10.1016/B978-0-12-819166-8.00025-6.

Hashemi Karouei SM, Sadeghpour Haji M, Gholampour Azizi I. 2012. Isolation of Saprolegnia and the influence of root ethanolic extract of Ruta graveolens on Saprolegnia spp growth. International Journal of Bioscience, Biochemistry and Bioinformatics 2(1): 64–67.

Holdich DM, Sibley PJ. 2003. Crayfish in European overview of taxonomy, legislation, distribution, and crayfish plague outbreaks. Management & conservation of crayfish. 8(5): 15–34.

Hooshangi S, Firouzbakhsh F, Badalii H. 2016. Evaluation of Invitro Antifungal Activity of Mentha Piperita and Carum Capticum against Saprolegnia Parasitica. Journal of Veterinary Microbiology 12(2): 47–55.

Hussein MA, Hassan WH, Mahmoud MA. 2013. Pathogenicity of Achlya proliferoides and Saprolegnia diclina (Saprolegniaceae) associated with Saprolegniosis outbreaks in cultured Nile tilapia (Oreochromis niloticus). World Journal of Fish and Marine Sciences 2: 188–193.

Jeronimo H, Rocha SC, Goncalves DR, Boro MC. 2015. Achlya catenulata sp. nov., a new Saprolegniales (Oomycetes, Straminipila) from Brazilian mangrove swamp. Phytotaxa 212(3): 221–228.

Jalilpoor J, Shenavar Masouleh A, Masoumzadeh M. 2006. Fungal flora in Acipenser persicus eggs with particular emphasis on Saprolegnia sp. (Oomycetes) and mortality during mass incubation at the Shahid Beheshti hatchery. Journal of Applied Ichthyology 22: 265–8.

Jiang RH, de Bruijn I, Haas BJ, Belmonte R, Löbach L, Christie J, van den Ackerveken G, Bottin A, Bulone V, Díaz-Moreno SM, Dumas B. 2013. Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. PLoS genetics 9(6): e1003272.

Johari SA, Kalbassi MR, Soltani M, Yu IJ. 2015. Study of fungicidal properties of colloidal silver nanoparticles (AgNPs) on trout egg pathogen, Saprolegnia sp. International Journal of Aquatic Biology (3): 191–198.

Johari SA, Kalbassi MR, Yu IJ. 2014. Inhibitory effects of silver zeolite on in vitro growth of fish egg pathogen, Saprolegnia sp. Journal of Coastal Life Medicine 2(5): 357–361.

Jookar Z, Gholipour Kanani H, Jafarian H, Taheri Mirghaed A. 2019. A comparative study of the in vitro antimicrobial and antifungal effect of Trachyspermum ammi, Lavandula angustifolia and Eugenia aromatica essence on rainbow trout Some pathogen. Journal of applied ichthyological research 6(4): 109–126.

Kageyama K. 2014. Molecular taxonomy and its application to ecological studies of Pythium species. Journal of general plant pathology 80(4): 314–326.

Kalatehjari P, Yousefian M, Khalilzadeh MA. Assessment of antifungal effects of copper nanoparticles on the growth of the fungus Saprolegnia sp. on white fish (Rutilus frisii kutum) eggs. 2015. The Egyptian Journal of Aquatic Research 41(4): 303–306.

Kamilya D, Baruah A. 2014. Epizootic ulcerative syndrome (EUS) in fish: history and current status of understanding. Reviews in fish biology and fisheries (1): 369–380.

Khodabandeh S, Abtahi B. 2006. Effects of sodium chloride, formalin and iodine on the hatching success of common carp, Cyprinus carpio, eggs. Journal of Applied Ichthyology 22(1): 54–56.

Khodadadi A, Arabzadeh P, Rasouli S, Moradpour A, Abedian Amiri A. 2014. Investigation of the causes of rainbow trout losses in Cage Culture farms (Hasanloo Dam) Hasanlu Dam, West Azerbaijan Province. Pathology of veterinary clinic (Tabriz Veterinary) 8(2): 461–472.

Khosravi AR, Shokri H, Sharifrohani M, Mousavi HE, Moosavi Z. 2012. Evaluation of the antifungal activity of Zataria multiflora, Geranium herbarium, and Eucalyptus camaldolensis essential oils on Saprolegnia parasitica–infected rainbow trout (Oncorhynchus mykiss) eggs. Foodborne Pathogens and Disease (7): 674–679.

Levenfors JP, Wikström M, Persson L, Gerhardson B. 2003. Pathogenicity of Aphanomyces spp. from different leguminous crops in Sweden. European Journal of Plant Pathology 109(6): 535–543.

Malherbe W, Christison KW, Wepener V, Smit NJ. 2019. Epizootic ulcerative syndrome–First report of evidence from South Africa's largest and premier conservation area, the Kruger National Park. International Journal for Parasitology: Parasites and Wildlife 10: 207–210.

Martín-Torrijos L, Kawai T, Makkonen J, Jussila J, Kokko H, Diéguez-Uribeondo J. 2018. Crayfish plague in Japan: A real threat to the endemic Cambaroides japonicus. PLoS One 13(4): e0195353.

Martín-Torrijos L, Campos Llach M, Pou-Rovira Q, Diéguez-Uribeondo J. 2017. Resistance to the crayfish plague, Aphanomyces astaci (Oomycota) in the endangered freshwater crayfish species, Austropotamobius pallipes. PLoS One. 2017 Jul 27;12(7): e0181226.

Masigol H, Woodhouse JN, van West P, Mostowfizadeh-Ghalamfarsa R, Rojas-Jimenez K, Goldhammer T, Khodaparast SA, Grossart HP. 2021. Phylogenetic and Functional Diversity of Saprolegniales and Fungi Isolated from Temperate Lakes in Northeast Germany. Journal of Fungi 7(11): 968.

Masigol H, Khodaparast SA, Mostowfizadeh-Ghalamfarsa R, Rojas-Jimenez K, Woodhouse JN, Neubauer D, Grossart HP. 2020. Taxonomical and functional diversity of Saprolegniales in Anzali lagoon, Iran. Aquatic Ecology 54(1): 323–336.

Masigol H, Khodaparast SA, Woodhouse JN, Rojas‐Jimenez K, Fonvielle J, Rezakhani F, Mostowfizadeh‐Ghalamfarsa R, Neubauer D, Goldhammer T, Grossart HP. 2019. The contrasting roles of aquatic fungi and oomycetes in the degradation and transformation of polymeric organic matter. Limnology and Oceanography 64(6): 2662–2678.

Masigol H, Khodaparast SA, Mostowfizadeh-Ghalamfarsa R, Mousanejad S, Rojas-Jimenez K, Grossart HP. 2018. Notes on Dictyuchus species (Stramenopila, Oomycetes) from Anzali lagoon, Iran. Mycologia Iranica 5(2): 79–89.

Mehrabi Z, Firouzbakhsh F, Rahimi-Mianji G, Paknejad H. 2020. Immunity and growth improvement of rainbow trout (Oncorhynchus mykiss) fed dietary nettle (Urtica dioica) against experimental challenge with Saprolegnia parasitica. Fish & Shellfish Immunology 104: 74–82.

Mehrabi Z, Firouzbakhsh F, Rahimi-Mianji G, Paknejad H. 2019. Immunostimulatory effect of Aloe vera (Aloe barbadensis) on non-specific immune response, immune gene expression, and experimental challenge with Saprolegnia parasitica in rainbow trout (Oncorhynchus mykiss). Aquaculture (2019): 330–338.

Mehrabi Z, Firouzbakhsh F, Rahimi G, Kolangi H. 2017. The Effect of Adding Aloe Vera (Aloe barbadensis) in the Diet on Growth Performance and Some Blood Parameters and Serum Biochemical Indices in Rainbow Trout (Oncorhynchus mykiss) Challenged with Saprolegnia parasitica. Journal of Fisheries 70(1): 60–69.

Mousavi HA, Soltani M, Khosravi A, Mood SM, Hosseinifard M. 2009. Isolation and characterization of Saprolegniaceae from rainbow trout (Oncorhynchus mykiss) eggs in Iran. Journal of Fisheries and Aquatic Science 4(6): 330–333.

Mousavi HA. 2007. Isolation and identification of parasite and saprophyte fungi from fungal affected eggs of the rainbow trout [Oncorhynchus mykiss] in Mazandaran province. Iranian Journal of Veterinary Research 62(3): 163–168.

Mousavi H, Sharif Rouhani M, Khosravi AR, Mehrabi Yad E, Akhoundzadeh Basti. 2006. The Evaluation of Eucaliptus Camaldolensis Dehnh esscence application in control of fungal pollution of trout eggs. Journal of Medical Plants 5(20): 42–47.

Mostafa AA, Al-Askar AA, Yassin MT. 2020. Anti-saprolegnia potency of some plant extracts against Saprolegnia diclina, the causative agent of saprolengiasis. Saudi Journal of Biological Sciences 27(6): 1482–1487.

Nekuie Fard A, Motalebi AA, Jalali Jafari B, Aghazadeh Meshgi M, Azadikhah D, Afsharnasab M. 2011. Survey on fungal, parasites and epibionts infestation on the Astacus leptodactylus (Eschscholtz, 1823), in Aras Reservoir West Azarbaijan, Iran. Iranian Journal of Fisheries Sciences 10(2): 266–275.

Neitzel DA, Elston RA, Abernethy CS. 2004. Prevention of prespawning mortality: cause of salmon headburns and cranial lesions. Pacific Northwest National Lab. (PNNL), Richland, WA (United States).

Pazira AR. 2017. Antifungal activity of Thymus essential oil (Thymus vulgaris) on fungi isolated from the skin of Koi (Cyprinus carpio var. Koi). Journal of Aquaculture Development 11(2): 13–22.

Peyghan R, Rahnama R, Dezfuly ZT, Shokoohmand M. 2019. Achlya infection in an Oscar (Astronotus ocellatus) with typical symptoms of saprolegniosis. Veterinary Research Forum 10(1): 89–92.

 Põlme S, Abarenkov K, Henrik Nilsson R, Lindahl BD, Clemmensen KE, Kauserud H, Nguyen N, Kjøller R, Bates ST, Baldrian P, Frøslev TG. 2020. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Diversity 105(1): 1–16.

Rezakhani F, Khodaparast SA, Masigol H, Roja-Jimenez K, Grossart HP, Bakhshi M. 2019. A preliminary report of aquatic hyphomycetes isolated from Anzali lagoon (Gilan province, North of Iran). Rostaniha 20(2): 123–143.

Rocha SC, Lopez-Lastra CC, Marano AV, de Souza JI, Rueda-Páramo ME, Pires-Zottarelli CL. 2018. New phylogenetic insights into Saprolegniales (Oomycota, Straminipila) based upon studies of specimens isolated from Brazil and Argentina. Mycological Progress 17(6): 691–700.

Rocha SC, Sandoval-Sierra JV, Dieguez-Uribeondo J, Goncalves DR, Jeronimo GH, De Jesus AL, Marano AV, Pires-Zottarelli CL. 2016. Saprolegnia milanezii sp. nov., a new species of Saprolegniales (Oomycota, Straminipila) from Brazil. Phytotaxa 270(4): 286–294.

Salah M, Zorriezahra S, Sepahdari A, Hosseni A, Falahatnaserabad I, Rastiannasab A. 2021. Comparison of Huwa-San TR-50 solution efficiency with malachite green and Formalin on fungal contamination control of rainbow trout (Oncorhynchus mykiss) eggs in incubation stage. Journal of aquaculture development 14(1): 53–61.

Salimian F, Fattollahi M, Nematollahi A, Nikookhah F, Kharazian N. 2015. Antifungal activity in vitro of aqueous and total flavnoids extracts of plant Myrtus communis L. against two pathogenically important fungi, Saprolegnia and Fusarrium isolated from rainbow trout eggs. Journal of marine sciences and technology 16(1): 16–28.

Scanu B, Jung T, Masigol H, Linaldeddu BT, Jung MH, Brandano A, Mostowfizadeh-Ghalamfarsa R, Janoušek J, Riolo M, Cacciola SO. 2021. Phytophthora heterospora sp. nov., a New Pseudoconidia-Producing Sister Species of P. palmivora. Journal of Fungi 7(10): 870.

Sedighi A, Sodagar M, Hashemi-Koroni M, Hosseini SS. 2015. Comparing the effect of antifungal Zinc oxide nanoparticles and Malachite green on Saprolegnia sp. The Journal of Aquatic Exploitation and Breeding 4(1): 29–37.

Shahbazian NA, Ebrahimzadeh Mousavi HA, Soltani MA, Khosravi AR, Mirzargar S, Sharifpour I. 2010. Fungal contamination in rainbow trout eggs in Kermanshah province propagations with emphasis on Saprolegniaceae. Iranian Journal of Fisheries Sciences 9(1): 151–160.

Shahrani M, Azari Takami G, Sharif Rohani M, Motallebi A, Yazdani Sadati M. 2021. Antifungal effects of alcoholic extract of Thymus vulgaris on Siberian sturgeon (Acipenser baerii) eggs compared with malachite green effects. Iranian Journal of Fisheries Sciences 20(1): 218–229.

Sharifi A, Gorjipour R, Gorjipour AA, Mohammadi R, Jabarnejad A. 2012. Antifungal effect of quercus infectoria gall (oak) on saprolegnia fungi. Armaghane danesh 17(1): 78–84.

Sharifpour I, Mazandarani M, Khoshbavar Rostami HA. 2014. Investigation of farmed Cyprinidae contaminants from Golestan province. The Journal of Aquatic Exploitation and Breeding 3(3): 15–25.

Shokouh Saljoghi Z, Farhadian O, Ramezanian N, Mehraban Sangatash M. 2020. Synthesis and characterization of novel compounds and determining their antifungal properties against rainbow trout pathogen, Saprolegnia sp. in vitro. Iranian Journal of Fisheries Sciences 19(3): 1396–1414.

Sigoillot JC, Berrin JG, Bey M, Lesage-Meessen L, Levasseur A, Lomascolo A, Record E, Uzan-Boukhris E. 2012. Fungal strategies for lignin degradation. Advances in botanical research 61: 263–308.

Singer D, Lara E, Steciow MM, Seppey CV, Paredes N, Pillonel A, Oszako T, Belbahri L. 2016. High-throughput sequencing reveals diverse oomycete communities in oligotrophic peat bog micro-habitat. Fungal Ecology 1(23): 42–47.

Svoboda J, Mrugała A, Kozubíková‐Balcarová E, Petrusek A. 2017. Hosts and transmission of the crayfish plague pathogen Aphanomyces astaci: a review. Journal of fish diseases 40(1): 127–140.

Tandel RS, Dash P, Bhat RA, Thakuria D, Sawant PB, Pandey N, Chandra S, Chadha NK. 2021. Anti-oomycetes and immunostimulatory activity of natural plant extract compounds against Saprolegnia spp.: Molecular docking and in-vitro studies. Fish & Shellfish Immunology 114: 65–81.

SavadKouhi P, Ahari H, Anvar AA, Jafari B. 2021. Effect of Carum copticum nano-essence against Saprolegnia and Fusarium, and the use of multiplex PCR assay for the detection of these organisms in rainbow trout Oncorhynchus mykiss. Archives of Razi Institute 76(2): 231–241.

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 Biology Reviews 27(2): 33–42.

 Wolinska J, King KC, Vigneux F, Lively CM. 2008. Virulence, cultivating conditions, and phylogenetic analyses of oomycete parasites in Daphnia. Parasitology 135(14): 1667–1678.

Wu L, Chang KF, Conner RL, Strelkov S, Fredua-Agyeman R, Hwang SF, Feindel D. 2018. Aphanomyces euteiches: a threat to Canadian field pea production. Engineering 4(4): 542–551