Heterorhabditis brevicaudis: A New Nematode Species Isolated from El-Dakhla Oasis in Egypt and Its Efficiency against Some Lepidopteran Pests

¹ Mona A. Hussein

Entomopathogenic nematodes in eco-friendly pest management

Abstract

Background: Entomopathogenic nematodes have been used as biopesticides for controlling insect pests in niche markets. Many new isolates have been recovered from soil of natural habitats in many parts of the world. Native EPNs may be more suitable for controlling local pests. Therefore, isolation and identification of native nematode-bacterial associations are necessary for the successful control of endemic pests. Methods: The occurrence of an EPN, Heterorhabditis brevicaudis and its symbiotic bacteria was newly isolated from Egypt and recorded for the first time in this report. Diagnosis was based on morphometric characteristics and cross-hyperdization. Biochemical characterization and antibiotic activity of its bacteria were investigated. The new species activity was studied against four lepidopteran pests under laboratory conditions. Results: The isolate was proved to be a new species and was congruently belongs to H. brevicadus. The bacteria produced very strong bioluminescence and its antimicrobial activity is of medium level. H. brevicaudis was highly pathogenic to G. mellonella; T. absoluta and A. ipsilon larvae when mature larvae were treated with doses of 150, 100, and 50 IJs/ml, respectively. Conclusion: This is the first report of H. brevicaudis from Egypt. Data showed that the isolate is a new heterorhabtid species. Its symbiotic bacteria belong to ideal criteria and parameters that support nematode growth and pathogenicity. The antibiotics production is an advantage for the successful culturing of EPNs. This new EPN had a good impact against the four tested economic insect pests and could be positively enrolled in an integrated pest management program.

Keywords: Entomopathogenic nematode, Heterorhabditis brevicaudis, Photorhabdus luminescens, Tuta absoluta, Spodoptera littoralis, Agrotis ipsilon, Egypt.

References

Abd El Azim A. M. (2022). Efficacy of the entomopathogenic nematode isolate Heterorhabditis taysearae to control the cotton leafworm, Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) Egyptian J. Biol. Pest Cont., 32(4): 1-5. https://doi.org/10.1186/s41938-022-00503-z

Adams B. J., Fodor A., Koppenhöfer H. S., Stackebrandt E., Stock S. P., Klein M. G. (2006). Biodiversity and systematics of nematode–bacterium entomopathogens. Biological Control 38: 4–21.

Akhurst, R.J., Brooks, W. M. (1984). The distribution of entomophilic nematodes (Heterorhabditidae and Steinernematidae) in North Carolina. J. Invert. Pathol., 44: 140-145.

Akhurst, R.J. (1980). Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoplectana and Heterorhabditis. J. Gen. Microb., 121:303–309.

Akhurst, R.J. (1982). Antibiotic activity of Xenorhabdus spp., bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. J. Gen. Microbiol. 128:3061-3065.

Akhurst, R.J., Bedding, R. A. (1986). Natural occurrence of insect pathogenic nematodes (Steinernematidae and Heterorhabditidae) in soil in Australia. J. Austr. Ent. Soc., 25: 241-244.

Arteaga-Hernandez, E. M., Mracek, Z. (1984). Heterorhabditis heliothidis, a parasite of insect pests in Cuba. Folia Parasitologica (Praha) 31, 11-17.

Bathon, H. (1996). Impact of entomopathogenic nematodes on non-target hosts, Biocontrol Sci Technol., 6: 421-434.

Bedding, R.A. (1990). Logistics and strategies for introducing entomopathogenic nematode technology in developing countries, pp. 233-248. In: Entomopathogenic nematodes for biological control (eds. R. Gaugler and H. K. Kaya). Boca Raton, FL, USA: CRC Press.

Bedding, R.A. (1998). Future possibilities for using entomopathogenic nematodes, Japanese J.Nematol. 28, 46-60.

Biondi A., Narciso R., Guedes C., Wan F.-H.,  Desneux N. (2018). Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future. Ann. Rev. Entomol. 63(1): 239-258.

Blackshaw, R. P. (1988). A survey of insect parasitic nematodes in Northern Ireland. Annals App. Biol.,113, 561-5.

Boemare N.E., Akhurst R.J. (1988). Biochemical and physiological characterization of colony form variants in Xenorhabdus spp. (Enterobacteriaceae). J Gen Microbiol 134:751–761

Boemare, N.E., Givaudan, A., Brehelin, M., Laumond, C. (1997). Symbiosis and pathogenicity of the nematode–bacterium complexes. Symbiosis 22, 21–45.

Burman, M., Abrahamasson, K., Ascard, J., Sjoberg, A., Eriksson, B. (1986). Distribution of insect parasitic nematodes in Sweden. In: Samson, R A, Vlak,J M. & Peters, D. (Eds). Proc. IVth int. Colloq. Invert. Pathol., Veldhoven, The Nelherlands: 300-303.

Deseo, K. V., Fantoni, P. & Lazzari, G. L. (1988). Presenzadi nematodi entomopatogeni (Sleinernema spp., Helerorhabdùisspp.) nei terreni agricolo in Italia. Alli Giornale/ùoparol., 2: 269-280.

Dix, I., Burnell, A M., Griffin, C. T., Joyce, S. A., Nugent, M. J (1992). The identification of biological species in the genus Heterorhabditis (Nematoda: Heterorhabditidae) by crossbreeding second generation amphimictic adults. Parasitol., 104: 509-518.

Downes, M. J., Griffin, C.T. (1991). Recovery of Heterorhabditid nematodes from Irish and Scottish soils. Proceedings of the Third European Meeting of the IOBC Working Group on Insect Pathogens and Insect Parasitic Nematodes, Wageningen, The Netherlands, 24-27 February 1991 (ed. Smits, P.H.), pp. 216-218. Wageningen: International Union of Biological Sciences.

Ehlers, RU. (1996). Current and future use of nematodes in biocontrol: practice and commercial aspects in regard to regulatory policies. Biocontrol Sci Technol 6:303–316

Grewal PS, Ehlers RU, Shapiro-Ilan DI. (2005). Nematodes as biocontrol agents. CABI, Wallingford, UK, pp 1–523.

Griffin, C.T., Joyce, S. A. Dix, I., Burnell, A M., Downes, M.J. (1994). Characterisation of the entomopathogenic nematode Heterorhabditis (Nematoda: Heterorhabditidae) from Ireland and Britain by molecular and crossbreeding techniques, and the occurrence of the genus in these islands. Fund. Appl. Nematol., 17, 245-254.

Griffin, C.T., Moore, J.F., Downes, M.J. (1991). Occurrence of insect parasitic nematodes (Steinrnematidae, Heterorhabditidae) in the Republic of Ireland. Nematologica, 37: 92-100.

Hara, A.H., Gaugler, R., Kaya, H. K., Lebeck, L. M. (1991). Natural populations of entomopathogenic nematodes. (Rhabditida, Heterorhabditidae, Steinernematidae) from Hawaiian Islands. Environ. Entomol., 20: 211-216.

Hominick, W.M., Briscoe, B.R. (1990). Survey of 15 sites over 28 months for entomopathogenic nematodes (Rhabditida: Steinernematidae). Parasitol., 100: 289-294.

Hsieh F.C., Tzeng C.Y., Kao S.S. (2005).  A new isolate of the entomopathogenic nematode, H. brevicaudis TG01 (Rhabditida: Heterorhabditidae). Taiwan Plant Prot Bull 4:263–271 (in Chinese with English summary).

Hsieh, F.C., Tzeng, C.Y., Tseng, J.T., Tsai, Y.S., Meng, M.H., Kao, S.S. (2009).  Isolation and Characterization of the Native Entomopathogenic Nematode, Heterorhabditis brevicaudis, and its Symbiotic Bacteria from Taiwan.  Curr. Microbiol., 58(6): 564-570.

Hussein M.A., El-Rahman R.A., El-Boraey H., Hilmy M., Attya E. (2018). The Impact of Cu Ion, Two Novel Schiff Base Ligands and their Copper (II) Complexes on the Biological Activity of the Entomopathogenic Nematodes. Microbial Bioactives, 1(2), 046-050

Hussein MA (2021). Efficacy of Egyptian parasitic nematodes, Heterorhabditis bacteriophora (BA1) and Steinernema carpocapsae (BA2) in biocontrol of economically important pests. Microbial Bioactives, 4(1), 150-155.

Hussein A. Mona and A. B Abou El- Soud (2006). Isolation and characterization of two Heterorhabditids and one Steinernematid nematode from Egypt. Int. J. Nematol., 16(1):7-12.

Hussein, Mona. A. (2004): Utilization of some entomopathogenic nematodes for the biological control of some lepidoterous pests. PhD. Entomology Dept., Faculty of Science, Ain Sham University, 203pp.

Ibrahim S.A., Mahfouz H.M., Mahasen M.Elshershaby, Mona A. Hussein, Dawod A.A. (2017). The role of entomopathogenic nematodes, Steinernema spp, in the biological control of Agrotis ipsilon (Lepidoptera: Noctuidae). Menoufia J Plant Prot., 2: 281– 289

Iraki N, Salah N, Sansour MA, Segal D, Glazer I, Johnigk SA, Hussein MA, Ehlers RU. (2000). Isolation and characterization of two entomopathogenic nematode strains, Heterorhabditis indica (Nematoda, Rhabditida), from the West Bank, Palestinian Territories. J. Appl. Ent. 124:375–380.

Johnigk, S. & Ehlers, R. (1999). Juvenile development and life cycle of Heterorhabditis bacteriophora and H. indica. Nematol., 1, 251-260.

Kaya, H. K & S. P. Stock (1997). Techniques in insect nematology, pp. 281-324. In: Manual of Techniques in Insect Pathology (Ed.L.Lacey). San Diego, CA, USA: Academic Press.

Labaude, S., Griffin, C. T. (2018). Transmission success of entomopathogenic nematodes used in pest control. Insects, 9(2), 72.

Liu, J (1994). A new species of the genus HelerorhabdùlS from China (Rhabditida: Heterorhabditidae). Acta zootax. sinica,19: 268-272.

Mracek, Z. (1980). The use of Galleria traps for obtaining nematodes parasites of insecrs in Czechoslovakia (Nemaroda:Steinernematidae). Acta ent. bohemosl., 77: 78-382.

Nguyen, K.B., Smart, G.C. Jr. (1996). Identification of entomopathogenic nematodes in the Steinernematidae and Heterorhabditidae (Nemata: Rhabditida). J. Nematol 28:286–300

Paniagua Voirol L.R., Frago E., Kaltenpoth M, Hilker M., Fatouros N.E. (2018). Bacterial symbionts in Lepidoptera: their diversity, transmission, and impact on the host. Front Microbiol 9:556. https://doi.org/10.3389/fmicb.2018.00556

Peel, M. M., Alfredson,D. A., Gerrad, J. G., Davis, J. M., Robson, M. McDougall, R. J., Scullie, B. L. Akhurst, R. J. (1999). Isolation, identification, and molecular characterization of strains of Photorhabdus luminescens from infected humans in Australia. J. Clin. Microbiol. 37: 3647-3653.

Poinar, GO (1990). Taxonomy and biology of Steinernematidae and Heterorhabditidae. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Florida, pp 23–61

Saleh M. M. E.; Mona A. Hussein; Gehan A. Hafez; M.A.Hussein; H.A. Salem, Hala M. S. Metwally (2015). Foliar application of entomopathogenic nematodes (Nematoda: Steinernematidae & Heterorhabditidae) for controlling Spodoptera littoralis and Agrotis ipsilon (Lepidoptera: Noctuidae) on corn (Zea mays) Advances in Applied Agricultural Science (AAAS) 1(1): 50-61

Sandhi, R. K., Pothula, R., Pothula, S. K., Adams, B. J., Reddy, G. (2020). First record of native entomopathogenic nematodes from Montana agroecosystems. J. Nematol., 52, 1–11. https://doi.org/10.21307/jofnem-2020-060

Seinhorst, J. W. (1959). A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4, 67-69.

Shamseldean, M.M.; Abou-Elsoud, A.B.; Abdel-Gawad, M.M., Saleh, M.M. (1996). Identification of a new heterorhabditid species from Egypt, Heterorhabditis tyserae n. Sp.(Rhabditida:  Heterorhabditidae) as afirst record in Egypt. Egypt. J. Biol. Pest Cont., 6(1): 15-24.

Smits, P.H., Groenen, T. M., De Raay, G. (1991). Characrerization of Heterorhabditis isolates using DNA restriction fragment length polymorphism. Revue Némarol.,14: 45-453.

Sobhy H.M., Abdel-Bary N. A., Harras F. A., Faragalla F. H., Husseinen H. I. (2020).  Efficacy of entomopathogenic nematodes against Spodoptera littoralis (Boisd.) and Agrotis ipsilon (H.) (Lepidoptera: Noctuidae). Egypt. J. Biol. Pest Cont., 30 (73): 1-8. https://doi.org/10.1186/s41938-020-00265-6

Stock, S.P. (1997). Heterorhabditis hepialus Stock, Strong & Gardner, 1996a junior synonym of H. marelatus Liu & Berry, 1996 (Rhabditida: Rhabditidae) with a redescription of the species. Nematologica 43, 455-463.

Stock, S.P. (2000). Systematics, Diversity and Biogeography of entomopathogenic Nematodes: A Decade of Exciting Research Accomplishments. http://ag.arizona.edu/PLP/faculty/stock.html

Stock, S.P., H.Y. Choo & H. K. Kaya (1997). An entomopathogenic nematodes Steinernema monticolum sp. Rhabditida: Steinernematidae) from Korea with the key to other species. Nematologica 43, 15- 29.

Strauch, O., Stoessel, S., Ehlers, R-U. (1994). Culture conditions define automictic or amphimictic reproduction in entomopathogenic rhabditid nematodes of the genus Heterorhabditis. Fund. Appl. Nematol. 17, 575-582.

Sun, B., Zhang, X., Song, L., Zheng, L., Wei, X., Gu, X., Cui, Y., Hu, B., Yoshiga, T., Abd-Elgawad, M., Ruan, W. (2021). Evaluation of indigenous entomopathogenic nematodes in Southwest China as potential biocontrol agents against Spodoptera litura (Lepidoptera: Noctuidae). J. Nematol., 53(1) 1-17. https://doi.org/10.21307/jofnem-2021-083

Thakur N, Tomar P, Kaur S, Kumari P. (2022). Virulence of native entomopathogenic nematodes against major lepidopteron insect species of tomato (Solanum lycopersicum L.) J Appl Biol Biotech;10 (Suppl 1):6-14.

Uribe-Lorio L, Mora M., Stock, S.P. (2005). First record of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) in Costa Rica. J. Invert. Pathol. 88:226–231

Vanninen, I., Husberg, G. B., Hokkanen, M. T. (1989). Occurrence of entomopathogenic fungi and entomoparasitic nematodes in cultivated soils in Finland. Acta Ent. Vennica, 53: 65-71.

Vivas, E.I., Goodrich-Blair, H. (2001). Xenorhabdus nematophilus as a model for host–bacterium interactions: rpoS is necessary for mutualism with nematodes. J. Bacteriol, 183: 4687–4693.

Webster, J. M. (2002). Bacterial metabolites, pp. 99-114. In: Entomopathogenic Nematology (Ed. R. Gaugler). Wallingford, UK: CABI Publishing.

White, G.F. (1927). A method for obtaining infective nematode larvae from cultures. Science 66, 302-303.

Woodring, J. L., Kaya, H. K. (1988). Steinernematid and heterorhabditid nematodes: A handbook of techniques. Arkansas Agricultural Experiment Station Southern Cooperative Bulletin 331, 30.