A Preliminary Study on the Interactions Between Some Entomopathogenic Fungi and the Entomopathogenic Nematode Steinernema feltiae

Öz

Entomopathogenic fungi (EPF) and entomopathogenic nematodes (EPN) are soil organisms that can infect and kill a wide variety of insects. These organisms are frequently used as biological control agents in the management of insect pests. Both EPF and EPN can be found in the same soil environment and can compete within the same insect host; they can show synergistic to antagonistic effects. This study was conducted to determine the relationship between EPN Steinernema feltiae and different EPF species and to investigate their possible effects on their use in biological control. According to the results obtained, EPN mortality was not detected in the applications of Purpureocillium lilacinum, the nematode egg pathogen, and the fungus could not be obtained in reisolation studies. Fusarium subgulitinans Fs-8 isolate was the least effective fungus in S. feltiae infective juvenile (IJs) mortality (3.5). Beauveria bassiana BIM-001, Metarhizium robertii, M. anisopliae ISP-12 and B. varroe isolates caused mortality on S. feltiae. While 15.3 IJs died in M. anisopliae ISP-1, 15.5 IJs died in B. bassiana BY-2, 16.3 IJs died in M. anisopliae ISP-17, 0.75 IJs died in P. lilacinum, and 3.5 IJs died in F. subglutinans Fs-8. According to the results obtained, it was determined that EPFs may have a lethal effect on S. feltiae and this effect varies depending on the species. This may be due to the differences in mechanism, pathogenicity, and toxin among EPFs. Detailed studies should be conducted on EPF and EPN combinations in the biological control of pests.

Anahtar Kelimeler

• Beauveria spp
• Biyolojik mücadele
• Fusarium subgulitinans
• Metarhizium spp.
• Purpureocillium lilacinum

Bazı Entomopatojen Fungusların Entomopatojen Nematod Steinernema feltiae ile Etkileşimlerine İlişkin Bir Ön Çalışma

Öz

Entomopatojen funguslar (EPF) ve entomopatojen nematodlar (EPN), çok çeşitli böcekleri enfekte edebilen ve öldürebilen toprak organizmalarıdır. Bu organizmalar böcek zararlılarının yönetiminde sıklıkla biyolojik kontrol etmenleri olarak kullanılır. Hem EPF hem de EPN’ler aynı toprak ortamında bulunabilirler ve aynı böcek konukçusu içerisinde rekabet edebilir; sinerjik etkilerden antagonistik etkiye kadar değişen sonuçlar gösterebilirler. Bu çalışma EPN Steinernema feltiae ile farklı EPF türleri arasındaki ilişkiyi belirlemek ve biyolojik kontrolde kullanımları üzerindeki olası etkilerini araştırmak için yapılmıştır. Elde edilen sonuçlara göre nematod yumurta patojeni olan Purpureocillium lilacinum uygulamalarında EPN ölümü belirlenmemiş ve reizolasyon çalışmalarında fungus elde edilememiştir. Fusarium subgulitinans Fs-8 izolatı S. feltiae’da infektif juvenil (IJs) ölümüne (3.5) en az etkili olan fungus olmuştur. Beauveria bassiana BIM-001, Metarhizium robertii, M. anisopliae ISP-12 ve B. varroe izolatları S. feltiae üzerinde ölümlere neden olmuştur. M. anisopliae ISP-1’de 15.3 IJs, B. bassiana’ BY-2 ‘de 15. 5 IJs, M. anisopliae ISP-17’de 16.3 IJs ölürken, P. lilacinum’de 0.75 IJs, F. subglutinans Fs-8’de ise 3.5 IJs ölümleri gözlenmiştir. Elde edilen sonuçlara göre, EPF’lerin S. feltiae üzerinde öldürücü etkisinin olabileceği ve bu etkinin tür bazında değişkenlik gösterdiği belirlenmiştir. Bunun nedeni EPF’ler arasındaki mekanizma, patojenite ve toksin farklılığı olabilir. Zararlıların biyolojik kontrolünde EPF ve EPN kombinasyonlarına yönelik ayrıntılı çalışmaların yapılması gerekmektedir.

Anahtar Kelimeler

• Beauveria spp
• Biyolojik mücadele
• Fusarium subgulitinans
• Metarhizium spp.
• Purpureocillium lilacinum

Kaynakça

1. Abd El Azim, A. M., Khashaba, E. H., & El Kady, G. A. (2024). Effectiveness study of the dual application of new Indigenous entomopathogenic nematode isolate Heterorhabditis taysearae and entomopathogenic fungi Beauveria bassiana against armyworm (Spodoptera frugiperda). Egyptian Journal of Biological Pest Control, 34(1), 41.
2. Ansari, M. A., Shah, F. A., & Butt, T. M. (2008). Combined use of entomopathogenic nematodes and Metarhizium anisopliae as a new approach for black vine weevil, Otiorhynchus sulcatus, control. Entomologia Experimentalis Et Applicata, 129(3), 340-347.
3. Ansari, M. A., Shah, F. A., Tirry, L., & Moens, M. (2006). Field trials against Hoplia philanthus (Coleoptera: Scarabaeidae) with a combination of an entomopathogenic nematode and the fungus Metarhizium anisopliae CLO 53. Biological Control, 39(3), 453-459.
4. Ansari, M. A., Tirry, L., & Moens, M. (2005). Antagonism between entomopathogenic fungi and bacterial symbionts of entomopathogenic nematodes. BioControl, 50, 465-475.
5. Ansari, M. A., Tirry, L., & Moens, M. (2004). Interaction between Metarhizium anisopliae CLO 53 and entomopathogenic nematodes for the control of Hoplia philanthus. Biological Control, 31(2), 172-180.
6. Bamisile, B. S., Siddiqui, J. A., Akutse, K. S., Ramos Aguila, L. C., & Xu, Y. (2021). General limitations to endophytic entomopathogenic fungi use as plant growth promoters, pests and pathogens biocontrol agents. Plants, 10(10), 2119.
7. Barberchek, M. E., & Kaya, H. K. (1990). Interactions between Beauveria bassiana and the entomogenous nematodes, Steinernema feltiae and Heterorhabditis heliothidis. Journal of Invertebrate Pathology, 55(2), 225-234.
8. Barra-Bucarei, L., France Iglesias, A., & Pino Torres, C. (2019). Entomopathogenic fungi. In Natural Enemies of Insect Pests in Neotropical Agroecosystems: Biological Control and Functional Biodiversity. (pp. 123-136)

9. Boemare, N. O. E. L., & Akhurst, R. (2006). The genera Photorhabdus and Xenorhabdus. Prokaryotes, 6, 451-494.
10. Campos-Herrera, R. (2015). Nematode pathogenesis of insects and other pests. In Ecology and applied technologies for sustainable plant and crop protection. (pp. 10-1007)
11. Cavigelli, M. A., Maul, J. E., & Szlavecz, K. (2012). Managing soil biodiversity and ecosystem services. In Soil Ecology and Ecosystem Services. (pp. 337-358)
12. Charnley, A. K., & Collins, S. A. (2007). 10 entomopathogenic fungi and their role in pest control. Environmental and Microbial Relationships, 4, 159.
13. Choo, H. Y., Kaya, H. K., Huh, J., Lee, D. W., Kim, H. H., Lee, S. M., & Choo, Y. M. (2002). Entomopathogenic nematodes (Steinernema spp. and Heterorhabditis bacteriophora) and a fungus Beauveria brongniartii for biological control of the white grubs, Ectinohoplia rufipes and Exomala orientalis, in Korean golf courses. Biocontrol, 47, 177-192.
14. Clarke, D. J., & Eberl, L. (2006). Interactions between bacteria and nematodes. In Intestinal Microorganisms of Termites and Other İnvertebrates. (pp. 55-64)
15. Correa-Cuadros, J. P., Sáenz-Aponte, A., & Rodríguez-Bocanegra, M. X. (2016). In vitro interaction of Metarhizium anisopliae Ma9236 and Beauveria bassiana Bb9205 with Heterorhabditis bacteriophora HNI0100 for the control of Plutella xylostella. SpringerPlus, 5, 1-8.
16. Donatti, A. C., Furlaneto-Maia, L., Fungaro, M. H. P., & Furlaneto, M. C. (2008). Production and regulation of cuticle-degrading proteases from Beauveria bassiana in the presence of Rhammatocerus schistocercoides cuticle. Current Microbiology, 56, 256-260.
17. Forst, S., Dowds, B., Boemare, N., & Stackebrandt, E. (1997). Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annual Review of Microbiology, 51(1), 47-72.
18. Furgani, G., Böszörményi, E., Fodor, A., Máthé‐Fodor, A., Forst, S., Hogan, J. S., ... & Wolf, S. L. (2008). Xenorhabdus antibiotics: a comparative analysis and potential utility for controlling mastitis caused by bacteria. Journal of Applied Microbiology, 104(3), 745-758.
19. Hussein, H. M., Skoková Habuštová, O., Půža, V., & Zemek, R. (2016). Laboratory evaluation of Isaria fumosorosea CCM 8367 and Steinernema feltiae Ustinov against immature stages of the Colorado potato beetle. PLoS One, 11(3), e0152399.
20. Hominick, W. M. (2002). Biogeography. In Entomopathogenic nematology. (pp. 115-143)
21. Kaya, H. K., & Gaugler, R. (1993). Entomopathogenic nematodes. Annual Review of Entomology, 38,181-206.
22. Koppenhöfer, A. M., & Grewal, P. S. (2005). Compatibility and interactions with agrochemicals and other biocontrol agents. In Nematodes as biocontrol aganta. (pp. 363-381)
23. Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., & Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132, 1-41.
24. Litwin, A., Nowak, M., & Różalska, S. (2020). Entomopathogenic fungi: unconventional applications. Reviews in Environmental Science and Bio/Technology, 19(1), 23-42.
25. Ma, M., Luo, J., Li, C., Eleftherianos, I., Zhang, W., & Xu, L. (2024). A life-and-death struggle: interaction of insects with entomopathogenic fungi across various infection stages. Frontiers in Immunology, 14, 1329843.
26. Maina, U. M., Galadima, I. B., Gambo, F. M., & Zakaria, D. J. J. O. E. (2018). A review on the use of entomopathogenic fungi in the management of insect pests of field crops. Journal of Entomology and Zoology Studies, 6(1), 27-32.
27. Navarro, P. D., McMullen II, J. G., & Stock, S. P. (2014). Interactions between the entomopathogenic nematode Heterorhabditis sonorensis (Nematoda: Heterorhabditidae) and the saprobic fungus Fusarium oxysporum (Ascomycota: Hypocreales). Journal of nvertebrate Pathology, 115, 41-47.
28. Půža, V., & Tarasco, E. (2023). Interactions between entomopathogenic fungi and entomopathogenic nematodes. Microorganisms, 11(1), 163.
29. San-Blas, E., Gowen, S. R., & Pembroke, B. (2008). Steinernemafeltiae: Ammonia triggers the emergence of their infective juveniles. Experimental Parasitology, 119(1), 180-185.
30. Sahab, A. F. (2012). Antimicrobial efficacy of secondary metabolites of Beauveria bassiana against selected bacteria and phytopathogenic fungi. Journal of Applied Sciences Research, 8(3), 1441-1444.
31. Shapiro-Ilan, D. I., Jackson, M., Reilly, C. C., & Hotchkiss, M. W. (2004). Effects of combining an entomopathogenic fungi or bacterium with entomopathogenic nematodes on mortality of Curculio caryae (Coleoptera: Curculionidae). Biological Control, 30(1), 119-126.
32. Shaurub, E. S. H., Reyad, N. F., Abdel-Wahab, H. A., & Ahmed, S. H. (2016). Mortality and nematode production in Spodoptera littoralis larvae in relation to dual infection with Steinernema riobrave, Heterorhabditis bacteriophora, and Beauveria bassiana, and the host plant. Biological Control, 103, 86-94.
33. Stock, S. P. (2015). Diversity, biology and evolutionary relationships. In Nematode pathogenesis of insects and other pests: Ecology and applied technologies for sustainable plant and crop protection. (pp. 3-27)
34. Strasser, H., Abendstein, D., Stuppner, H., & Butt, T. M. (2000). Monitoring the distribution of secondary metabolites produced by the entomogenous fungus Beauveria brongniartii with particular reference to oosporein. Mycological Research, 104(10), 1227-1233.
35. Tarasco, E., Santiago Alvarez, C., Triggiani, O., & Quesada Moraga, E. (2011). Laboratory studies on the competition for insect haemocoel between Beauveria bassiana and Steinernema ichnusae recovered in the same ecological niche. Biocontrol Science and Technology, 21(6), 693-704.
36. Thungrabeab, M., & Tongma, S. (2007). Effect of entomopathogenic fungi, Beauveria bassiana (Balsam) and Metarhizium anisopliae (Metsch) on non target insects. Current Applied Science and Technology, 7(1-1), 8-12. Webster, J. M., Chen GenHui, C. G., Hu KaiJi, H. K., & Li JianXiong, L. J. (2002). Bacterial metabolites. In Entomopathogenic Nematology. (pp. 99-114)
37. Wu, S., Youngman, R. R., Kok, L. T., Laub, C. A., & Pfeiffer, D. G. (2014). Interaction between entomopathogenic nematodes and entomopathogenic fungi applied to third instar southern masked chafer white grubs, Cyclocephala lurida (Coleoptera: Scarabaeidae), under laboratory and greenhouse conditions. Biological Control, 76, 65-73.