Skip to main content
Log in

Isolation, identification and characterization of the nematophagous fungus Arthrobotrys (Monacrosporium) sinense from China

  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

With the development of anthelmintic resistance of parastic nematodes, it is necessary to isolate and study nematophagous fungi to screen out the native isolates for their potential in the biocontrol of domestic animal nematodosis. This study aimed to isolate the Arthrobotrys sinense (Monacrosporium sinense) of nematophagous fungus, to characterize representative molecular isolates using scanning electron microscope (SEM), and to determine the effect of the temperature and pH values on radial growth of the isolate. Five isolates were isolated from 1532 samples of different types, and their occurrence frequencies were 0.32% of the total samples. They were identified as A. sinense by means of morphology and the sequence of the 5.8S, 18S, and 28S rDNA, as well as internal transcribed spacers 1 and 2. The isolate NBS003 could grow from 11°C to 35°C and had optimal growth at 30°C. The isolate could grow at pH 4 to 11, and its optimal value was obtained at pH 9. SEM results showed that 6 h after their addition, the second stage larvae (L2) and the third stage infective larvae (L3) of Haemonchus contortus were captured. L2 and L3 were penetrated by the fungus at 18 and 24 h post-capture, respectively. L2 and L3 were completely digested at 84 and 90 h post-capture, respectively. The NBS003 of the A. sinense should have a certain potential to be used for capturing the free-living stage of nematodes in sheep.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barçante, J.M., Barçante, T.A., Dias, S.R., Vieira, L.Q., Lima, W.S., Negrão-Corrêa D. 2003. A method to obtain axenic Angiostrongylus vasorum firststage larvae from dog feces. Parasitology Research, 89, 89–93. DOI: 10.1007/s00436-002-0719-z

    Article  Google Scholar 

  • Boguś M.I., Czygier, M., Kedra, E., Samborski J. 2005. In vitro assessment of the influence of nutrition and temperature on growing rates of five Duddingtonia flagrans isolates, their insecticidal properties and ability to impair Heligmosomoides polygyrus motility. Experimental Parasitology, 109, 115–123. DOI: 10.1016/j.exppara.2004.12.001

    Article  Google Scholar 

  • Braga, F.R., Araújo J.V. 2014. Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Applied Microbiology and Biotechnology, 98, 71–82. DOI: 10.1007/s00253-013-5366-z

    Article  CAS  Google Scholar 

  • Braga, F.R., Silva, A.R., Carvalho, R.O., Araújo, J.V., Guimarães P.H., Fujiwara R.T. et al. 2010. In vitro predatory activity of the fungi Duddingtonia flagrans, Monacrosporium thaumasium, Monacrosporium sinense and Arthrobotrys robusta on Ancylostoma ceylanicum third-stage larvae. Veterinary Microbiology, 20, 183–186. DOI: 10.1016/j.vetmic.2010.05.003

    Article  Google Scholar 

  • Cai, K.Z., Liu, J.L., Liu, W., Wang, B.B., Xu, Q., Sun, L.J., et al. 2016. Screening of different sample types associated with sheep and cattle for the presence of nematophagous fungi in China. Journal of Basic Microbiology, 56, 214–228. DOI: 10.1002/jobm.201500281

    Article  Google Scholar 

  • Campos, A.K., Araújo, J.V., Guimarães M.P. 2008. Interaction between the nematophagous fungus Duddingtonia flagrans and infective larvae of Haemonchus contortus (Nematoda: Trichostrongyloidea). Journal of Helminthology, 82, 337–341. DOI: 10.1017/S0022149X08032203

    Article  CAS  Google Scholar 

  • Campos, R.A., Boldo, J.T., Pimentel, I.C., Dalfovo, V., Araújo W.L., Azevedo, J.L., et al. 2010. Endophytic and entomopathogenic strains of Beauveria sp. to control the bovine tick Rhipicephalus (Boophilus) microplus. Genetics and Molecular Research, 9, 1421–1430. PMID:20662157

    Article  CAS  Google Scholar 

  • Duddington C.L. 1955. Notes on the technique of handling predaceous fungi. Transactions of the British Mycological Society, 38, 97–103

    Article  Google Scholar 

  • Falbo, M.K., Soccol, V.T., Sandini, I.E., Vicente, V.A., Robl, D., Soccol C.R. 2013. Isolation and characterization of the nematophagous fungus Arthrobotrys conoides. Parasitology Research, 112, 177–185. DOI: 10.1007/s00436-012-3123-3

    Article  Google Scholar 

  • Falzon, L.C., van Leeuwen, J., Menzies, P.I., Shakya, K.P., Jones-Bitton A., Sears, W., et al. 2013. Anthelmintic resistance in sheep flocks in Ontario. Canada Veterinary Parasitology, 193, 150–162. DOI: org/10.1016/j.vetpar.2012.11.014

    Article  CAS  Google Scholar 

  • Grønvold, J., Wolstrup, J., Nansen, P., Larsen, M., Henriksen, S.A., H. Bjørn., et al. 1999. Biotic and abiotic factors influencing growth rate and production of traps by the nematode-trapping fungus Duddingtonia flagrans when induced by cooperia oncophora larvae. Journal of Helminthology, 73, 129–136. DOI: 10.1017/S0022149X99000190

    Google Scholar 

  • He, S.Y., Ge Q.X. 1987. The mycoflora of cotton root-knot nematode (meloidogyne incognata). Acta Phytopathologica Sinica, 17, 14–21

    CAS  Google Scholar 

  • Hsueh, Y.P., Mahanti, P., Schroeder, F.C., Sternberg P.W. 2013. Nematode-trapping fungi eavesdrop on nematode pheromones. Current Biology, 23, 83–86. DOI: 10.1016/j.cub.2012.11.035

    Article  CAS  Google Scholar 

  • Inoué T., Osatake H. 1988. A new drying method of biological specimens for scanning electron microscopy: the t-butyl alcohol freeze-drying method. Archives of Histology and Cytology, 51, 53–59. PMID:3137948

    Article  Google Scholar 

  • Kelly, P., Good, B., Hanrahan, J.P., Fitzpatrick, R., de Waal T. 2009. Screening for the presence of nematophagous fungi collected from Irish sheep pastures. Veterinary Parasitology, 165, 345–349. DOI: 10.1016/j.vetpar.2009.07.026

    Article  Google Scholar 

  • Li, J., Zou, C., Xu, J., Ji, X., Niu, X., Yang, J., et al. 2015. Molecular mechanisms of nematode-nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Annual Review of Phytopathology, 53, 67–95. DOI: 10.1146/annurev-phyto-080614-120336

    Article  CAS  Google Scholar 

  • Li, T.F., Zhang, K.Q., Liu X.Z. 2000. Taxonomy of Nematophagous Fungi. Chinese Scientific and Technological Publication, Beijing

    Google Scholar 

  • Liu, W., Han, Y., Wang, B.B., Sun, L.J., Chen, M.Y., Cai, K.Z., et al. 2015. Isolation, identification, and characterization of the nematophagous fungus Monacrosporium salinum from China. Journal of Basic Microbiology, 55, 992–1001. DOI: 10.1002/jobm.201400909

    Article  Google Scholar 

  • Liu, X.Z., Zhang K.Q. 1994. Nematode-trapping species of Monacrosporium with special reNematode-trapping species of Monacrosporium with special reference to two new species ference to two new species. Mycological Progress, 98, 863. Doi: 10.1016/S0953-7562(09)80255-4

    Google Scholar 

  • Li, Y., Hyde, K.D., Jeewon, R., Cai, L., Vijaykrishna, D., Zhang K. 2005. Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Mycologia, 97, 1034–1046. PMID:16596955

    Article  CAS  Google Scholar 

  • Maciel, A.S., Araújo, J.V., Campos, A.K., Benjamin, L.A., Freitas L.G. 2009. Scanning electron microscopy of Ancylostoma spp. dog infective larvae captured and destroyed by the nematophagous fungus Duddingtonia flagrans. Micron, 40, 463–470. DOI: 10.1016/j.micron.2008.12.007

    Article  CAS  Google Scholar 

  • Manueli, P.R., Waller, P.J., Faedo, M., Mahommed F. 1999. Biological control of nematode parasites of livestock in Fiji: screening of fresh dung of small ruminants for the presence of nematophagous fungi. Veterinary Parasitology, 81, 39–45. PMID:9950327

    Article  CAS  Google Scholar 

  • Nordbring-hertz B. 1983. Dialysis membrane technique for studying microbial interaction. Applied and Environmental Microbiology, 45, 290–293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nordbring-Hertz, B., Friman, E., Veenhuis M. 1989. Hyphal fusion during initial stages of trap formation in Arthrobotrys oligospora. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 55, 237–244. PMID: 2757366

    Article  CAS  Google Scholar 

  • Ojedarobertos, N.F., Torresacosta, J.F., Ayalaburgos, A.J., Sandovalcastro C.A., Valerocoss, R.O., Mendozadegives P. 2009. Digestibility of Duddingtonia flagrans chlamydospores in ruminants: in vitro and in vivo studies. Bmc Veterinary Research, 5, 1–7. DOI: 10.1186/1746-6148-5-46

    Article  Google Scholar 

  • Olthof, H.A., Estey R.H. 1965. Relation of some environmental factors to growth of several nematophagous Hyphomycetes. Canadian Journal of Microbiology, 11, 939–946. PMID: 5893825

    Article  CAS  Google Scholar 

  • Paz-Silva, A., Francisco, I., Valero-Coss, R.O., Cortiñas, F.J., Sánchez J.A., Francisco, R., et al. 2011. Ability of the fungus Duddingtonia flagrans to adapt to the cyathostomin egg-output by spreading chlamydospores. Veterinary Parasitology, 30, 277–282. DOI: 10.1016/j.vetpar.2011.02.014

    Article  Google Scholar 

  • Saitou, N., Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425. PMID: 3447015

    CAS  Google Scholar 

  • Sargison N.D. 2012. Pharmaceutical treatments of gastrointestinal nematode infections of sheep—future of anthelmintic drugs. Veterinary Parasitology, 189, 79–84. DOI: 10.1016/j.vetpar.2012.03.035

    Article  CAS  Google Scholar 

  • Sissay, M.M., Asefa, A., Uggla, A., Waller P. J. 2006. Anthelmintic resistance of nematode parasites of small ruminants in eastern ethiopia: exploitation of refugia to restore anthelmintic efficacy. Veterinary Parasitology, 135, 337–346

    Article  CAS  Google Scholar 

  • Swe, A., Li, J., Zhang, K.Q., Pointing S.B. 2011. Nematode-trapping fungi. Current Research in Environmental and Applied Mycology, 1, 1–26

    Google Scholar 

  • Tucker, S.L., Talbot N.J. 2001. Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annual Review of Phytopathology, 39, 385–417. DOI: 10.1146/annurev.phyto.39.1.385

    Article  CAS  Google Scholar 

  • Tunlid, A., Jansson S. 1991. Proteases and their involvement in the infection and immobilization of nematodes by the nematophagous fungus Arthrobotrys oligospora. Applied and Environmental Microbiology, 57, 2868–2872. PMID: 16348563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, B.B., Liu, W., Chen, M.Y., Li, X., Han, Y., Xu, Q., et al. 2015. Isolation and characterization of china isolates of Duddingtonia flagrans, a candidate of the nematophagous fungi for biocontrol of animal parasitic nematodes. Journal of Parasitology, 101, 476–484. DOI: 10.1645/14-715.1

    Article  Google Scholar 

  • Wang, B.B., Wang, F.H., Xu, Q., Wang, K.Y., Xue, Y.J., Ren, R., et al. 2017(a). In vitro and in vivo studies of the native isolates of nematophagous fungi from China against the larvae of trichostronglides. Journal of Basic Microbiology, 57, 265–275. DOI: 10.1002/jobm.201600620

    Article  CAS  Google Scholar 

  • Wang, F.H., Xu, Q., Wang, B.B., Wang, K.Y., Xue, Y.J., Cai, B., et al. 2017(b). Isolation, identification and characterization of the nematophagous fungus Arthrobotrys thaumasia (Monacrosporium thaumasium) from China. Biocontrol Science and Technology, 27, 378–392. DOI: 10.1080/09583157.2017.1291908

    Article  Google Scholar 

  • White, T.J., Bruns, T., Lee, S., Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, 18, 315–322

    Google Scholar 

  • Zhang, K.Q., Hyde K.D. 2014. Nematode-trapping Fungi. In Fungal Diversity Research Series, 23, 41–210

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kui-Zheng Cai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xue, YJ., Li, EL., Jing, CX. et al. Isolation, identification and characterization of the nematophagous fungus Arthrobotrys (Monacrosporium) sinense from China. Acta Parasit. 63, 325–332 (2018). https://doi.org/10.1515/ap-2018-0037

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/ap-2018-0037

Keywords

Navigation