A preliminary report of aquatic hyphomycetes isolated from Anzali lagoon (Gilan province, North of Iran)

Document Type : Research Paper

Authors

1 Graduated MSc Student, Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

2 Associate Prof., Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

3 PhD Student, Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

4 Prof., Escuela de Biologia, Universidad de Costa Rica, 11501 San Jose, Costa Rica

5 Prof., Department of Experimental Limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Alte Fischerhuette 2, D-16775 Stechlin and Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany

6 Research Assistant Prof., Department of Botany, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran

Abstract

Aquatic hyphomycetes equipped with a rich array of extracellular enzymes are involved in bioremediation of anthropogenic pollutants, plastics, aromatic contaminants and petroleum hydrocarbons. The current study contributes to the knowledge of Iranian aquatic hyphomycetes. Sampling was conducted in Anzali lagoon, Gilan province, Iran during 2017. Among 55 fungal isolates obtained during this study, eight species including Arthrobotrys oligosporus, Ceratorhiza hydrophila, Fusarium cf. ensiforme, F. incarnatum species complex, Myrmecridium schulzeri, Paecilomyces variotii, Sarocladium subulatum, and Volutella citrinella were identified based on their morphological characteristics. Furthermore, three species assigned to the genera Arthrobotrys, Fusarium and Sarocladium remained unidentified. Molecular studies using mainly ITS, LSU and SSU rDNA and in some cases β-tubulin (tub2) and translation elongation factor 1-a (tef1) determined the phylogenetic position of the isolates among closely related species. The occurrence of members of Fusarium, Sarocladium, and Ceratorhiza, known as rice disease agents, in freshwater ecosystems is interesting. This is the first report of aquatic hyphomycetes communities in Anzali lagoon, Iran. In this study, Sarocladium subulatum, Myrmecridium schulzeri, and Volutella citrinella are reported for the first time for Iran.
 
 

Keywords


Article Title [Persian]

گزارش مقدماتی از هیفومیست‌های آبزی تالاب انزلی (استان گیلان)

Authors [Persian]

  • فروغ رضاخانی 1
  • سید اکبر خداپرست 2
  • حسین مسیگل 3
  • کیلور روخاس-خیمنز 4
  • هانس-پیتر گروسارت 5
  • مونس بخشی 6
1 دانش‌آموخته کارشناسی ارشد، گروه گیاه‌پزشکی، دانشکده علوم کشاورزی، دانشگاه گیلان، رشت، ایران
2 دانشیار گروه گیاه‌پزشکی، دانشکده علوم کشاورزی، دانشگاه گیلان، رشت، ایران
3 دانشجوی دوره دکتری، گروه گیاه‌پزشکی، دانشکده علوم کشاورزی، دانشگاه گیلان، رشت، ایران
4 استاد بخش زیست‌شناسی، دانشگاه کاستاریکا، کاستاریکا
5 استاد بخش آب شیرین‌شناسی تجربی، مؤسسه اکولوژی آب شیرین و شیلات لیبنیتز (آی.جی.بی.)، آلمان
6 استادیار پژوهش بخش تحقیقات رستنی‌ها، مؤسسه تحقیقات گیاه‌پزشکی کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، تهران، ایران
Abstract [Persian]

 
هیفومیست‌های آبزی تولید‌کننده تعدادی زیادی آنزیم‌های خارج سلولی هستند که در تجزیه زیستی آلودگی‌های ناشی از فعالیت‌های انسانی، پلاستیک، ترکیبات آروماتیک و هیدروکربن‌های نفتی نقش دارند. مطالعه حاضر با هدف افزایش دانش ما از هیفومیست‌های آبزی در ایران صورت گرفت. نمونه‌برداری طی سال 1396 از تالاب انزلی در استان گیلان انجام گرفت. از میان 55 جدایه قارچی که در این مطالعه به دست آمد، تعداد هشت گونه شامل Arthrobotrys oligosporus، Ceratorhiza hydrophila، Fusarium cf. ensiforme، F. incarnatum species complex، Myrmecridium schulzeri،Paecilomyces variotii، Sarocladium subulatum و Volutella citrinella برمبنای خصوصیات ریخت‌شناختی شناسایی شدند. علاوه براین، سه گونه متعلق به جنس‌های Arthrobotrys ، Fusarium  وSarocladium  ناشناخته باقی ماندند. شناسایی مولکولی اغلب گونه‌ها با استفاده از سه ناحیه ژنی شامل فاصله ترانویسی‌شده داخلی (ITS)، زیرواحد کوچک (SSU) و بزرگ (LSU) دی اِن اِی ریبوزومی (rDNA)، همچنین در مواردی از سازه امتداد ترجمه یک آلفا (tef1) و بتاتوبولین (tub2) موقعیت جدایه‌ها را در میان گونه‌های نزدیک نشان داد. حضور جنس‌هایی نظیر Fusarium، Sarocladium وCeratorhiza  در زیست‌بوم‌های آب شیرین که به عنوان عوامل بیماری‌زای برنج مطرح هستند، جالب توجه است. این نخستین گزارش از جمعیت‌های هیفومیستی در تالاب انزلی است. در این تحقیق، Sarocladium subulatum، Myrmecridium schulzeri و Volutella citrinella برای نخستین بار از ایران گزارش می‌شوند.
 
 

Keywords [Persian]

  • آلودگی‌های محیطی
  • تنوع زیستی
  • قارچ‌های آب‌های شیرین
  • قارچ‌های میتوسپوریک
  • قارچ‌های آنامورفیک
Amirmijani, A.R., Khodaparast, S.A., Padasht, F. & Souhani, M.M. 2012. Morphology, pathogenicity and partial sequencing of rDNA region of Ceratorhiza hydrophila on rice from Iran. Iranian Journal of Plant Pathology 48(3): 137–139.
Andrassy, I. & Gibson, J. 2007. Nematodes from saline and freshwater lakes of the Vestfold Hills, East Antarctica, including the description of Hypodontolaimus antarcticus sp. n. Polar Biology 30: 669–678.
Aoki, T., O’Donnell, K. & Geiser, D.M. 2014. Systematics of key phytopathogenic Fusarium species: current status and future challenges. Journal of General Plant Pathology 80(3):
189–201.
Arzanlou, M., Groenewald, J.Z., Gams, W., Braun, U., Shin, H.D. & Crous, P.W. 2007. Phylogenetic and morphotaxonomic revision of Ramichloridium and allied genera. Studies in Mycology 58: 57–93.
Ayyadurai, N., Kirubakaran, S.I., Srisha, S. & Sakthivel, N. 2005. Biological and molecular variability of Sarocladium oryzae, the sheath rot pathogen of rice (Oryza sativa L.). Current Microbiology 50(6): 319–323.
Bigirimana, V.D.P., Hua, G.K., Nyamangyoku, O.I. & Höfte, M. 2015. Rice sheath rot: an emerging ubiquitous destructive disease complex. Frontiers in Plant Science 6: 1066.
Blackwell, M. 2011. The fungi: 1, 2, 3. . . 5.1 million species? American Journal of Botany 98:
426–438.
Booth, C. 1971. The genus Fusarium. Commonwealth Mycological Institute, Surrey.
Butcheli, T.D., Wettstein, F.E., Hartmann, N., Erbs, M., Vogelgsang, S., Forrer, H.R. & Schwarzenbach, R.P. 2008. Fusarium mycotoxins: overlooked aquatic micropollutants? Journal of Agricultural and Food Chemistry 56(3): 1029–1034.
Campos, R., Kandelbauer, A., Robra, K.H., Cavaco-Paulo, A. & Gübitz, G.M. 2001. Indigo degradation with purified laccases from Trametes hirsuta and Sclerotium rolfsii. Journal of Biotechnology 89(2–3): 131–139.
Can, V.O. 1985. Taxonomy of the Dactylaria complex. V. A review of Arthrobotrys and allied genera. Studies in Mycology 26: 61–96.
Carascal, M., del Rosario, M.J.G., Norarte, K.I.R., Huyop, F., Yuguchi, T. & dela Cruz, T.E.E. 2017. Butachlor biodegradation potential of fungi isolated from submerged wood and surface water collected in Taal Lake, Philippines. Philippine Science Letters 10(2): 81–88.
Casas, J.J. & Descals, E. 1997. Aquatic hyphomycetes from Mediterranean streams contrasting in chemistry and riparian canopy. Limnetica 13:
45–55.
Cedeno, L., Nass, H., Carrero, C., Cardona, R., Rodriguez, H. & Aleman, L. 1997. Sclerotium hydrophilum en arroz en Venezuela. Fitopatologia Venezolana 10: 9–12.
Chauvet, E., Cornut, J., Sridhar, K.R., Selosse, M.A. & Bärlocher, F. 2016. Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecology 19: 112–127.
Chehri, K., Salleh, B. & Zakaria, L. 2015. Morphological and phylogenetic analysis of Fusarium solani species complex in Malaysia. Microbial Ecology 69(3): 457–471.
Chilton, J.E. 1954. Volutella species on alfalfa. Mycologia 46: 800–809.
Cintas, N.A. & Webster, R.K. 2001. Effects of rice straw management on Sclerotium oryzae inoculum, stem rot severity, and yield of rice in California. Plant Disease 85(11): 1140–1144.
Descals, E. & Moralejo, E. 2001. Water and asexual reproduction in the ingoldian fungi. Botanica Complutensis 25: 13–71.
Descals, E. 1997. Ingoldian fungi: some field and laboratory techniques. Bolletí de la Societat d'Història Natural de les Balears 40: 169–221.
Desjardins, A.E., Manandhar, H.K., Plattner, R.D., Manandhar, G.G., Poling, S.M. & Maragos, C.M. 2000. Fusarium species from Nepalese rice and production of mycotoxins and gibberellic acid by selected species. Applied and Environmental Microbiology 66(3): 1020–1025.
Downes, F.P. & Ito, K. 2001. Compendium of Methods for the Microbiological Examination of Foods, 4th ed., APHA, Washington D.C.
Ebadi, M., Riahi, H. & Zare, R. 2014. Genetic diversity of Fusarium semitectum isolates from rice, using RAPD and REP-PCR markers. Mycologia Iranica 1(1): 19–26.
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.
Gallowey, L.D. & Burgess, R. 1952. Applied Mycology and Bacteriology, 3rd ed., Leonard Hill, London.
Gao, J.X., Jing, J., Liu, T. & Chen, J. 2015. Identification of Clt-1-regulated proteins associated with the production of non-host-specific toxin and pathogenicity in Cochliobolus lunatus. Journal of Phytopathology 163: 33–41.
Gerlach, W. & Nirenberg, H. 1982. The genus Fusarium - a Pictorial Atlas. Mitteilungen aus der Biologischen Bundesanstalt fur Land-und Forstwirtschaft,Berlin.
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, A.R., Soltani, M., Binaii,
M., Shokri, H., Tootian, Z., Rostami Bashman,
M. & Ebrahimzadeh Mousavi, H. 2010. Characterization of Saprolegnia isolates from Persian sturgeon (Acipencer persicus) eggs based on physiological and molecular data. Journal de Mycologie Medicale 20(1): 1–7.
Giraldo, A., Gené, J., Sutton, D.A., Madrid, H., De Hoog, G.S., Cano, J., Decock, C., Crous, P.W. & Guarro, J. 2015. Phylogeny of Sarocladium (Hypocreales). Persoonia 34: 10–24.
Gräfenhan, T., Schroers, H.J., Nirenberg, H.I. & Seifert, K.A. 2011. An overview of the taxonomy, phylogeny, and typification of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella, and Volutella. Studies in Mycology 68: 79–113.
Grinhut, T., Hertkorn, N., Schmitt-Kopplin, P., Hadar, Y. & Chen, Y. 2011. Mechanisms of humic acids degradation by white rot fungi explored using 1H NMR spectroscopy and FTICR mass spectrometry. Environmental Science & Technology 45: 2748–2754.
Grossart, H.P., Van den Wyngaert, S., Kagami, M., Wurzbacher, C., Cunliffe, M. & Rojas-Jimenez, K. 2019. Fungi in aquatic ecosystems. Nature Reviews Microbiology 17: 339–354.
Grossart, H.P. & Rojas-Jimenez, K. 2016. Aquatic fungi: targeting the forgotten in microbial ecology. Current Opinion in Microbiology 3: 140–145.
Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41(41): 95–98.
Haard, K. 1968. Taxonomic studies on the genus Arthrobotrys Corda. Mycologia 60(6): 1140–1159.
Helfer, W. 1991. Pilze auf Pilzfruchtkörpern. Untersuchungen zur Ökologie, Systematik und Chemie. Libri Botanici 1: 1–157.
Houbraken, J., Verweij, P.E., Rijs, A.J., Borman, A.M. & Samson, R.A. 2010. Identification of Paecilomyces variotii in clinical samples and settings. Journal of Clinical Microbiology 48(8): 2754–2761.
Hughes, S.J. 1951. Studies on Microfungi 5. Acrotheca. Mycological Papers 38: 1–8.
Ingold, C.T. 1942. Aquatic hyphomycetes of decaying alder leaves. Transactions of the British Mycological Society 25: 339–417.
Jafari, N. 2009. Ecological integrity of wetland, their functions and sustainable use. Journal of Ecology and the Natural Environment 1(3): 045–054.
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: 265–268.
Janipour, S., Khodaparast, S.A., Elahinia, S. & Padasht, F. 2009. A survey of sclerogenic fungal pathogens of rice plant (Oryza sativa L.) in Guilan province. Journal of Plant Protection 23(1): 1–8.
Katoh, K. & Standley, D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4): 772–780.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C. & Thierer, T. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12): 1647–1649.
Kisand, V., Gebhardt, S., Rullkotter, J., & Simon, M. 2013. Significant bacterial transformation of riverine humic matter detected by pyrolysis GC-MS in serial chemostat experiments. Marine Chemistry 149: 23–31.
Khosravi, A.R., Shokri, H., Sharifrohani, M., Mousavi, H.E. & Moosavi, Z. 2012. Evaluation of the antifungal activity of Zataria multiflora, Geranium herbarium, and Eucalyptus camaldolensis essential oils on Saprolegni aparasitica–infected rainbow trout (Oncorhynchus mykiss) eggs. Foodborne Pathogens and Disease 9(7): 674–679.
Kumar, S., Stecher, G. & Tamura, K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874.
Leslie, J.F. & Summerell, B.A. 2008. The Fusarium Laboratory Manual. John Wiley & Sons, New Jersey.
Liu, X.B., Guo, Z.K. & Huang, G.X. 2017. Sarocladium brachiariae sp. nov., an endophytic fungus isolated from Brachiaria brizantha. Mycosphere 8: 827–834.
Maddison, W.P. & Maddison, D.R. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org.
Masigol, H., Khodaparast, S.A., Woodhouse, J.N., Rojas-Jimenez, K., Fonvielle, J., Rezakhani, F., Mostowfizadeh-Ghalamfarsa, R., Neubauer, D., Goldhammer, T. & Grossart, H.P. 2019. The contrasting roles of aquatic fungi and oomycetes in the degradation and transformation of polymeric organic matter. Limnology and Oceanography 64: 2662–2678.
Masigol, H., Khodaparast, S.A., Mostowfizadeh-Ghalamfarsa, R., Mosanejad, S., Rojas-Jimenez, K. & Grossart, H.P. 2018. Notes on Dictyuchus species (Stramenopila, Oomycetes) from Anzali lagoon, Iran. Mycologia Iranica 5(2): 79–89.
Montero-Pau, J., Gómez, A. & Muñoz, J. 2008. Application of an inexpensive and high throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnology and Oceanography: Methods 6(6): 218–222.
Murray, P.R., Baron, E.J., Jorgensen, J.H., Pfaller, M.A. & Yolken, R.H. 2003. Manual of Clinical Microbiology, ASM, Washington D.C.
Naeimi, S., Okhovvat, S.M., Hedjaroude, G.A. & Khosravi, V. 2003. Sheath rot of rice in Iran. Communications in Agricultural and Applied Biological Sciences 68: 681–684.
Nalim, F.A., Samuels, G.J., Wijesundera, R.L. & Geiser, D.M. 2011. New species from the Fusarium solani species complex derived from perithecia and soil in the old world tropics. Mycologia 103(6): 1302–1330.
Nekuiefard, A., Motalebi, A.A., 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.
Nelson, P.E., Toussoun, T.A. & Marasas, W.F.O. 1983. Fusarium species: an Illustrated Manual for Identification. Pennsylvania State University Press, Pennsylvania.
Nguyen, T.T.T., Paul, N.C. & Lee, H.B. 2016. Characterization of Paecilomyces variotii and Talaromyces amestolkiae in Korea based on the morphological characteristics and multigene phylogenetic analyses. Mycrobiology 44(4):
248–259.
Noorhosseini, S.A., Allahyari, M.S., Damalas, C.A. & Moghaddam, S.S. 2017. Public environmental awareness of water pollution from urban growth: The case of Zarjub and Goharrud rivers in Rasht, Iran. Science of the Total Environment 599: 2019–2025.
Nylander, J.A.A. 2004. MrModeltest ver. 2.0. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala.
O’Donnell, K., Sutton, D.A., Rinaldi, M.G., Gueidan, C., Crous, P.W. & Geiser, D.M. 2009. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-equiseti and
F. chalmydosporum species complexes within the United States. Journal of Clinical Microbiology 47: 3851–3861.
Park, D. 1972. On the ecology of heterotrophic microorganisms in freshwater. Transactions of the British Mycological Society 58: 291–299.
Pascoal, C., Marvanová, L. & Cássio, F. 2005. Aquatic hyphomycete diversity in streams of Northwest Portugal. Fungal Diversity 19: 109–128.
Peintner, U., Knapp, M., Fleischer, V., Walch, G. & Dresch, P. 2016. Myrmecridium hiemale sp. nov. from snow-covered alpine soil is the first eurypsychrophile in this genus of anamorphic fungi. International Journal of Systematic and Evolutionary Microbiology 66(7): 2592–2598.
Révay, A. & Gönczöl, J. 1990. Longitudinal distribution and colonization patterns of wood-inhabiting fungi in a mountain stream in Hungary. Nova Hedwigia 51: 505–520.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542.
Rossman, A.Y., Cavan Allen, W., Braun, U., Castlebury, L.A., Chaverri, P., Crous, P.W., Hawksworth, D.L., Hyde, K.D., Johnston, P., Lombard, L. & Romberg, M. 2016. Overlooked competing asexual and sexually typified generic names of Ascomycota with recommendations for their use or protection. IMA fungus 7(2): 289–308.
Šafránková, I. 2007. Volutella leaf blight and stem canker on Japanese pachysandra in the Czech Republic. Plant Protection Science 43: 10–12.
Saravanakumar, D., Lavanya, N., Muthumeena, K., Raguchander, T. & Samiyappan, R. 2009. Fluorescent pseudomonad mixtures mediate disease resistance in rice plants against sheath rot (Sarocladium oryzae) disease. Biocontrol 54(2): 273.
Samson, R.A., Houbraken, J., Varga, J. & Frisvad, J.C. 2009. Polyphasic taxonomy of the heat resistant ascomycete genus Byssochlamys and its Paecilomyces anamorphs. Persoonia 22: 14–27.
Samson, R.A. 1974. Paecilomyces and some allied hyphomycetes. Studies in Mycology 6: 1–119.
Sandoval-Denis, M., Guarnaccia, V., Polizzi, G. & Crous, P.W. 2018. Symptomatic Citrus trees reveal a new pathogenic lineage in Fusarium and two new Neocosmospora species. Persoonia 40: 1–25.
Sautour, M., Edel-Hermann, V., Steinberg, C., Sixt, N., Laurent, J., Dalle, F., Aho, S., Hartemann, P., L’Ollivier, C., Goyer, M. & Bonnin, A. 2012. Fusarium species recovered from the water distribution system of a French university hospital. International Journal of Hygiene and Environmental Health 215(3): 286–292.
Schroers, H.J., Samuels, G.J., Zhang, N., Short, D.P., Juba, J. & Geiser, D.M. 2016. Epitypification of Fusisporium (Fusarium) solani and its assignment to a common phylogenetic species in the Fusarium solani species complex. Mycologia 108(4): 806–819.
Seifert, K.A. 1985. A monograph of Stilbella and allied hyphomycetes. Studies in Mycology 27: 1–235.
Selosse, M.A., Vohnık, M. & Chauvet, E. 2008. Out of the rivers: are some aquatic hyphomycetes plant endophytes? New Phytology 178: 3–7.
Shearer, C.A., Descals, E., Kohlmeyer, B., Kohlmeyer, J., Marvanová, L., Padgett, D., Porter, D., Raja, H.A., Schmit, J.P., Thorton, H.A. & Voglymayr, H. 2007. Fungal biodiversity in aquatic habitats. Biodiversity and Conservation 16(1): 49–67.
Simister, R., Poutasse, C., Thurston, A., Reeve, J., Baker, M. & White, H. 2015. Degradation of oil by fungi isolated from Gulf of Mexico beaches. Marine Pollution Bulletin 100: 327–333.
Spatafora, J.W., Sung, G.H., Johnson, D., Hesse, C., O’Rourke, B., Serdani, M., Spotts, R., Lutzoni, F., Hofstetter, V., Miadlikowska, J. & Reeb, V. 2006. A five-gene phylogeny of Pezizomycotina. Mycologia 98(6): 1018–1028.
Sridhar, K.R., Karamchand, K.S. & Bhat, R. 2006. Arboreal water-borne hyphomycetes with oak-leaf basket fern Drynaria quercifolia. Sydowia 58: 309–320.
Steinberg, C., Laurent, J., Edel-Hermann, V., Barbezant, M., Sixt, N., Dalle, F., Aho, S., Bonnin, A., Hartemann, P. & Sautour, M. 2015. Adaptation of Fusarium oxysporum and Fusarium dimerum to the specific aquatic environment provided by the water systems of hospitals. Water Research 76: 53–65.
Udaiyan, K. & Hosagoudar, V.S. 1991. Some interesting fungi from the industrial water cooling towers of Madras II. Journal of Economic and Taxonomic Botany 15: 649–66.
Webster, J. 1992. Anamorph-teleomorph relationships, pp. 99–117. In: The Ecology of Aquatic Hyphomycetes (Baerlocher, F., ed). Springer, Berlin.
Wurzbacher, C.M., Bärlocher, F. & Grossart, H.P. 2010. Fungi in lake ecosystems. Aquatic Microbial Ecology 59(2): 125–149.
Xu, Z., Harrington, T.C., Gleason, M.L. & Batzer, J.C. 2010. Phylogenetic placement of plant pathogenic Sclerotium species among teleomorph genera. Mycologia 102(2): 337–346.
Yang, J., Wang, L., Ji, X., Feng, Y., Li, X., Zou, C., Xu, J., Ren, Y., Mi, Q., Wu, J. & Liu, S. 2011. Genomic and proteomic analyses of the fungus Arthrobotrys oligosporus provide insights into nematode-trap formation. PLOS Pathogens 7(9): e1002179.
Yang, Y., Yang, E.C., An, Z.Q. & Liu, X.Z. 2007. Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proceedings of the National Academy of Sciences of the US 104: 8379–8384.
Zare-Maivan, H. & Ghaderian, M. 1993. Freshwater leaf-inhabiting hyphomycetes of an Iranian river. Mycologia 85(3): 355–357.
Zhang, Y., Qiao, M., Xu, J., Cao, Y., Zhang, K.Q. & Yu, Z.F. 2013. Genetic diversity and recombination in natural populations of the nematode-trapping fungus Arthrobotrys oligospora from China. Ecology and Evolution 3(2): 312–325.
Ziarati, P., Asgarpanah, J. & Mirmohammad-Makki, F. 2015. Phytoremediation of heavy metal contaminated water using potential Caspian sea wetland plant: Nymphaeaceae. Biosciences Biotechnology Research Asia 12(3): 2467–2473.