Hostname: page-component-54dcc4c588-tfzs5 Total loading time: 0 Render date: 2025-10-12T18:25:42.267Z Has data issue: false hasContentIssue false
  • English
  • Français

A survey of entomopathogenic nematodes and their symbiotic bacteria in agricultural areas of northern Thailand

Published online by Cambridge University Press:  14 September 2020

J. Ardpairin ,
P. Muangpat ,
S. Sonpom ,
A. Dumidae ,
C. Subkrasae ,
S. Tandhavanant ,
A. Thanwisai  and
A. Vitta Open the ORCID record for A. Vitta [Opens in a new window]
J. Ardpairin
Affiliation:
Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand
P. Muangpat
Affiliation:
Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand
S. Sonpom
Affiliation:
Department of Agriculture Science, Faculty of Agriculture Natural Resources and Environment, Naresuan University, Phitsanulok, 65000, Thailand
A. Dumidae
Affiliation:
Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand
C. Subkrasae
Affiliation:
Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand
S. Tandhavanant
Affiliation:
Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok10400, Thailand
A. Thanwisai
Affiliation:
Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand Centre of Excellence in Medical Biotechnology (CEMB), Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand Center of Excellence for Biodiversity, Faculty of Sciences, Naresuan University, Phitsanulok, 65000Thailand
A. Vitta*
Affiliation:
Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand Centre of Excellence in Medical Biotechnology (CEMB), Faculty of Medical Science, Naresuan University, Phitsanulok, 65000, Thailand Center of Excellence for Biodiversity, Faculty of Sciences, Naresuan University, Phitsanulok, 65000Thailand
*
Author for correspondence: Apichat Vitta, E-mail: apichatv@nu.ac.th
Get access Rights & Permissions [Opens in a new window]

Abstract

Entomopathogenic nematodes (EPNs) Steinernema and Heterorhabditis and their symbiotic bacteria, Xenorhabdus and Photorhabdus, have been successfully used for the control of insect pests. The objectives of this study were to survey the EPNs and symbiotic bacteria in the agricultural areas of the Phitsanulok province, Thailand, and to study the association between the soil parameters and presence of EPNs. We collected 200 soil samples from 40 soil sites in agricultural areas (field crops, horticulture crops and forest). The prevalence of EPNs was 8.0% (16/200). Fifteen of the EPN isolates were molecularly identified (based on 28S ribosomal DNA and internal transcribed spacer regions) as Steinernema siamkayai. Seven isolates of Xenorhabdus stockiae were identified using recombinase A sequencing. Phylogenetic analysis revealed that all the Steinernema and Xenorhabdus isolates were closely related to S. siamkayai (Indian strain) and X. stockiae (Thai strain), respectively. Significantly more EPNs were recovered from loam than from clay. Although the association between soil parameters (pH, temperature and moisture) and the presence of EPNs was not statistically significant, the elevation levels of the soil sites with and without EPNs were found to be different. Moreover, statistical comparisons between the agricultural areas revealed no significant differences. Therefore, we concluded that S. siamkayai is associated with X. stockiae in agricultural areas and that there is no association between the soil parameters of agricultural areas and presence of EPNs, except for soil texture and the elevation. Steinernema siamkayai may be applied as a biocontrol agent in agricultural areas.

Keywords

Agricultureentomopathogenic nematodesphylogenysymbiotic bacteria

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e192
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Al-Zaidawi, JB, Karimi, J and Mahdikhani, ME (2020) Entomopathogenic nematodes as potential biological control agents of subterranean termite, Microcerotermes diversus (Blattodea: Termitidae) in Iraq. Environmental Entomology 49, 412–442.CrossRefGoogle Scholar
Arriaga, A and Cortez-Madrigal, H (2018) Susceptibility of Musca domestica larvae and adults to entomopathogenic nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) native to Mexico. Journal of Vector Ecology 43, 312–320.CrossRefGoogle ScholarPubMed
Banu, JG, Nguyen, KB and Rajendran, G (2005) Occurrence and distribution of entomopathogenic nematodes in Kerala, India. International Journal of Nematology 15, 9–16.Google Scholar
Bhat, S, Singh, J and Vig, A (2017) Instrumental characterization of organic wastes for evaluation of vermicompost maturity. Journal of Analytical Science and Technology 8, 2.CrossRefGoogle Scholar
Bussaman, P and Rattanasena, P (2016) Additional property of Xenorhabdus stockiae for inhibiting cow mastitis-causing bacteria. Biosciences Biotechnology Research Asia 13, 1871–1878.CrossRefGoogle Scholar
Bussaman, P, Sa-Uth, C, Rattanasena, P and Chandrapatya, A (2012) Acaricidal activities of whole cell suspension, cell-free supernatant, and crude cell extract of Xenorhabdus stokiae against mushroom mite (Luciaphorus sp.). Journal of Zhejiang University-Science 13, 261–266.CrossRefGoogle Scholar
Caoili, BL, Latina, RA, Sandoval, RFC and Orajay, JI (2018) Molecular identification of entomopathogenic nematode isolates from the Philippines and their biological control potential against lepidopteran pests of corn. Journal of Nematology 50, 99–110.CrossRefGoogle Scholar
de Brida, AL, Rosa, JM, Oliveira, CM, Castro, BM, Serrão, JE, Zanuncio, JC, Leite, LG and Wilcken, SR (2017) Entomopathogenic nematodes in agricultural areas in Brazil. Scientific Reports 7, 45254.CrossRefGoogle ScholarPubMed
Dilipkumar, A, Raja Ramalingam, K, Chinnaperumal, K, Govindasamy, B, Paramasivam, D, Dhayalan, A and Pachiappan, P (2019) Isolation and growth inhibition potential of entomopathogenic nematodes against three public health important mosquito vectors. Experimental Parasitology 197, 76–84.CrossRefGoogle ScholarPubMed
Dowds, BCA and Peters, A (2002) Virulence mechanisms. pp. 79–98in Gaugler, R (Ed) Entomopathogenic nematology. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Fayyaz, S and Javed, S (2009) Laboratory evaluation of seven Pakistani strains of entomopathogenic nematodes against a stored grain insect pest, pulse beetle Callosobruchus chinensis (L.). Journal of Nematology 41, 255–260.Google Scholar
Ferreira, T, van Reenen, CA, Endo, A, Sproer, C, Malan, AP and Dicks, LMT (2013) Description of Xenorhabdus khoisanae sp. nov., the symbiont of the entomopathogenic nematode Steinernema khoisanae. International Journal of Systematic and Evolutionary Microbiology 63, 3220–3224.CrossRefGoogle ScholarPubMed
Fukruksa, C, Yimthin, T, Suwannaroj, M, Muangpat, P, Tandhavanant, S, Thanwisai, A and Vitta, A (2017) Isolation and identification of Xenorhabdus and Photorhabdus bacteria associated with entomopathogenic nematodes and their larvicidal activity against Aedes aegypti. Parasites and Vectors 10, 440.CrossRefGoogle ScholarPubMed
Garcia del Pino, F and Palomo, A (1996) Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Spanish soils. Journal of Invertebrate Pathology 68, 84–90.CrossRefGoogle Scholar
Hara, AH, Gaugler, R, Kaya, HK and LeBeck, LM (1991) Natural populations of entomopathogenic nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) from the Hawaiian Islands. Environmental Entomology 20, 211–216.CrossRefGoogle Scholar
Hazir, S, Keskin, N, Stock, SP, Kaya, HK and Özcan, S (2003) Diversity and distribution of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Turkey. Biodiversity and Conservation 12, 375–386.CrossRefGoogle Scholar
Heve, WK, El-Borai, FE, Carrillo, D and Duncan, LW (2017) Biological control potential of entomopathogenic nematodes for management of Caribbean fruit fly, Anastrepha suspensa Loew (Tephritidae). Pest Management Science 73, 1220–1228.CrossRefGoogle Scholar
Hominick, WM (2002) Biogeography. pp. 115–144in Gaugler, R (Ed) Entomopathogenic nematology. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Hominick, WM, Briscoe, B, Del Pino, F, et al. (1997) Biosystematics of entomopathogenic nematodes: current status, protocols and definitions. Journal of Helminthology 71, 271–298.CrossRefGoogle ScholarPubMed
Hunt, DJ (2016) Introduction. pp. 1–11in Hunt, DJ and Nguyen, KB (Eds) Nematology monographs and perspectives volume 12: advanced in entomopathogenic nematode taxonomy and phylogeny. Leiden, Brill.Google Scholar
Kary, EN, Gholamreza, N, Christine, G, Seyed, M and Vahed, MM (2009) A survey of entomopathogenic nematodes of the families Steinernematidae and Heterorhabditidae (Nematoda: Rhabditida) in the north-west of Iran. Nematology 11, 107–116.CrossRefGoogle Scholar
Khatri-Chhetri, HB, Waeyenberge, L, Manandhar, HK and Moens, M (2010) Natural occurrence and distribution of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) in Nepal. Journal of Invertebrate Pathology 103, 74–78.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Kung, S, Gaugler, R and Kaya, HK (1990) Influence of soil, pH, and oxygen on persistence of Steinernema spp. Journal of Nematology 22, 440–445.Google ScholarPubMed
Kuwata, R, Qiu, LH, Wang, W, Harada, Y, Yoshida, M, Kondo, E and Yoshiga, T (2013) Xenorhabdus ishibashii sp. nov., isolated from the entomopathogenic nematode Steinernema aciari. International Journal of Systematic and Evolutionary Microbiology 63, 1690–1695.CrossRefGoogle ScholarPubMed
Lacey, L, Grzywacz, D, Shapiro-Ilan, D, Frutos, R, Brownbridge, M and Goettel, M (2015) Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology 132, 1–41.CrossRefGoogle ScholarPubMed
Malan, AP, Knoetze, R and Moore, SD (2011) Isolation and identification of entomopathogenic nematodes from citrus orchards in South Africa and their biocontrol potential against false codling moth. Journal of Invertebrate Pathology 108, 115–125.CrossRefGoogle ScholarPubMed
Maneesakorn, P, Grewal, PS and Chandrapatya, A (2010) Steinernema minutum sp. nov. (Rhabditida: Steinernema): a new entomopathogenic from Thailand. International Journal of Nematology 20, 27–42.Google Scholar
Modic, Š, Žigon, P, Kolmanič, A, Trdan, S and Razinger, J (2020) Evaluation of the field efficacy of Heterorhabditis Bacteriophora Poinar (Rhabditida: Heterorhabditidae) and synthetic insecticides for the control of Western corn rootworm larvae. Insects 11, 202.CrossRefGoogle ScholarPubMed
Mráček, Z and Webster, JM (1993) Survey of heterorhabditidae and steinernematidae (Rhaditida. Nematoda) in Western Canada. Journal of Nematology 25, 710–717.Google Scholar
Muangpat, P, Yooyangket, T, Fukruksa, C, Suwannaroj, M, Yimthin, T, Sitthisak, S and Thanwisai, A (2017) Identification and characterization of the antimicrobial activity against drug resistant bacteria of Photorhabdus and Xenorhabdus associated with entomopathogenic nematodes from Mae Wong National Park, Thailand. Frontiers in Microbiology 8, 1142.CrossRefGoogle Scholar
Namsena, P, Bussaman, P and Rattanasena, P (2016) Bioformulation of Xenorhabdus stockiae for controlling mushroom mite, Luciaphorus perniciosus Rack. Bioresources and Bioprocessing 3, 19.CrossRefGoogle Scholar
Phan, KL, Mráček, Z, Půža, V, Nermut, J and Jarošová, A (2014) Steinernema huense sp. n., a new entomopathogenic nematode (Nematoda: Steinernematidae) from Vietnam. Nematology 16, 761–775.CrossRefGoogle Scholar
Raja, RK, Sivaramakrishnan, S and Hazir, S (2011) Ecological characterisation of Steinernema siamkayai (Rhabditida: Steinernematidae), a warm-adapted entomopathogenic nematode isolate from India. Biocontrol 56, 789–798.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rosa, JS, Bonifassi, E, Amaral, J, Lacey, LA, Simões, N and Laumond, C (2000) Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernema, Heterorhabditis) in the Azores. Journal of Nematology 32, 215–222.Google Scholar
Shahina, F, Anis, M, Zainab, S and Maqbool, MA (1998) Entomopathogenic nematodes in soil samples collected from Sindh, Pakistan. Pakistan Journal of Nematology 16, 41–50.Google Scholar
Shapiro-Ilan, D, Hazir, S and Glazer, I (2017) Basic and applied research: entomopathogenic nematodes. pp. 91–105in Lacey, LA (Ed) Microbial control of insect and mite pests. Cambridge, Academic Press.CrossRefGoogle Scholar
Smart, GC (1995) Entomopathogenic nematodes for the biological control of insects. Journal of Nematology 27, 529–534.Google ScholarPubMed
Stock, SP, Somsook, V and Reid, AP (1998) Steinernema siamkayai n. sp. (Rhabditida: Steinernematidae), an entomopathogenic nematode from Thailand. Systematic Parasitology 41, 105–113.CrossRefGoogle Scholar
Stock, SP, Campbell, JF and Nadler, SA (2001) Phylogeny of Steinernema Travassos 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. Journal of Parasitology 87, 877–889.CrossRefGoogle ScholarPubMed
Suwannaroj, M, Yimthin, T, Fukruksa, C, Muangpat, P, Yooyangket, T, Tandhavanant, S, Thanwisai, A and Vitta, A (2020) Survey of entomopathogenic nematodes and associate bacteria in Thailand and their potential to control Aedes aegypti. Journal of Applied Entomology 144, 212–223.CrossRefGoogle Scholar
Tailliez, P, Pagès, S, Ginibre, N and Boemare, N (2006) New insight into diversity in the genus Xenorhabdus, including the description of ten novel species. International Journal of Systematic and Evolutionary Microbiology 56, 2805–2818.CrossRefGoogle ScholarPubMed
Tailliez, P, Laroui, C, Ginibre, N, Paule, A, Pages, S and Boemare, N (2010) Phylogeny of Photorhabdus and Xenorhabdus based on universally conserved protein-coding sequences and implications for the taxonomy of these two genera. Proposal of new taxa: X. vietnamensis sp. nov., P. luminescens subsp. caribbeanensis subsp. nov., P. luminescens subsp. hainanensis subsp. nov., P. temperata subsp. khanii subsp. nov., P. temperata subsp. tasmaniensis subsp. nov., and the reclassification of P. luminescens subsp. thracensis as P. temperata subsp. thracensis comb. nov. International Journal of Systematic and Evolutionary Microbiology 60, 1921–1937.CrossRefGoogle Scholar
Tailliez, P, Pages, S, Edgington, S, Tymo, LM and Buddie, AG (2012) Description of Xenorhabdus magdalenensis sp. nov., the symbiotic bacterium associated with Steinernema australe. International Journal of Systematic and Evolutionary Microbiology 62, 1761–1765.CrossRefGoogle ScholarPubMed
Tarasco, E, Clausi, M, Rappazzo, G, et al. (2015) Biodiversity of entomopathogenic nematodes in Italy. Journal of Helminthology 89, 359–366.CrossRefGoogle ScholarPubMed
Thanwisai, A, Tandhavanant, S, Saiprom, N, Waterfield, NR, Ke Long, P, Bode, HB and Chantratita, N (2012) Diversity of Xenorhabdus and Photorhabdus spp. and their symbiotic entomopathogenic nematodes from Thailand. PLoS ONE 7, 43835.CrossRefGoogle ScholarPubMed
Valadas, V, Laranjo, M, Mota, M and Oliveira, S (2014) A survey of entomopathogenic nematode species in continental Portugal. Journal of Helminthology 88, 327–341.CrossRefGoogle ScholarPubMed
Vitta, A, Yimthin, T, Fukruksa, C, Wongpeera, W, Yotpanya, W, Polseela, R and Thanwisai, A (2015) Distribution of entomopathogenic nematodes in lower northern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 46, 564–573.Google ScholarPubMed
Vitta, A, Fukruksa, C, Yimthin, T, Deelue, K, Sarai, C, Polseela, R and Thanwisai, A (2017) Preliminary survey of entomopathogenic nematodes in upper northern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 48, 18–26.Google ScholarPubMed
Vitta, A, Thimpoo, P, Meesil, W, Yimthin, T, Fukruksa, C, Polseela, R and Thanwisai, A (2018) Larvicidal activity of Xenorhabdus and Photorhabdus bacteria against Aedes aegypti and Aedes albopictus. Asian Pacific Journal of Tropical Biomedicine 8, 31–36.CrossRefGoogle Scholar
Wetchayunt, W, Rattanapan, A and Phairiron, S (2009) Temperature effect on novel entomopathogenic nematode Steinernema siamkayai Stock, Somsook and Reid (n. sp.) and its efficacy against Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Communications in Agricultural and Applied Biological Sciences 74, 587–592.Google Scholar
White, GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66, 302–303.CrossRefGoogle ScholarPubMed
Ye, W, Foye, S, MacGuidwin, AE and Steffan, S (2018) Incidence of Oscheius onirici (Nematoda: Rhabditidae), a potentially entomopathogenic nematode from the marshlands of Wisconsin, USA. Journal of Nematology 50, 9–26.CrossRefGoogle Scholar
Yooyangket, T, Muangpat, P, Polseela, R, Tandhavanant, S, Thanwisai, A and Vitta, A (2018) Identification of entomopathogenic nematodes and symbiotic bacteria from Nam Nao National Park in Thailand and larvicidal activity of symbiotic bacteria against Aedes aegypti and Aedes albopictus. PLoS ONE 13, 0195681.CrossRefGoogle ScholarPubMed