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Entomopathogenic Nematodes- Nematode Information

Insect-parasitic nematodes that belong to both Steinernematidae and Heterorhabditidae families are also called as entomopathogenic nematodes because they cause disease to their insect hosts with the help of mutualistically associated symbiotic bacterial pathogens. The entomopathogenic nematodes that belong to families Steinernematidae (Steinernema spp.) Heterorhabditidae (Heterorhabditis spp.) are symbiotically associated with species specific bacteria, Xenorhabdus spp. and Photorhabdus spp., respectively.  The infective juveniles of entomopathogenic nematodes from both these families carry hundreds of specific bacterium cells in their guts and use them to cause disease and kill their insect host within 48 hours after infection.

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Infective juveniles of entomopathogenic nematodes- Photo by Ganpati Jagdale

Entomopathogenic nematodes and their symbiotic bacteria- Nematode Information

Molecular studies demonstrated that the closely related Photorhabdus, symbiotic bacteria of Heterorhabditis nematodes and Xenorhabdus, symbiotic bacteria of Steinernematid nematodes have developed totally different molecular strategies for the same objective of virulence to insects and symbiosis with the nematode.

These findings were presented by An, R. and Grewal, P.S. at the 50th annual meeting of the Society of Nematologists held in Corvallis, Oregon from July 17-20, 2011.

Entomopathogenic nematode symbiotic bacteria and antimicrobial activity

The compounds produced by entomopathogenic nematode symbiotic bacteria Xenorhabdus bovienii have showed antimicrtobial activity against two fungus species including Botrytis cinerea and Phytophthora capsici (Fang et al., 2011).  Both of these fungi causes diseases to many plant species.

Publications on antimicrobial activity of entomopathogenic nematode symbiotic bacteria.

1. Fang, X. L., Feng, J. T., Zhang, W. G., Wang, Y. H. and Zhang, X. 2010. Optimization of growth medium and fermentation conditions for improved antibiotic activity of Xenorhabdus nematophila TB using a statistical approach.  African Journal of Biotechnology 9: 8068-8077.
2. Fang, X.L., Li, Z.Z., Wang, Y.H. and Zhang, X. 2011.   In vitro and in vivo antimicrobial activity of Xenorhabdus bovienii YL002 against Phytophthora capsici and Botrytis cinerea. Journal of Applied Microbiology 111: 145-154.
3. Furgani, G., Boeszoermenyi, E., Fodor, A., Mathe-Fodor, A., Forst, S., Hogan, J.S., Katona, Z.,  Klein, M.G., Stackebrandt, E., Szentirmai, A., Sztaricskai, F. and Wolf, S. L. 2008.  Xenorhabdus antibiotics: a comparative analysis and potential utility for controlling mastitis caused by bacteria.  Journal of Applied Microbiology 104: 745-758.
4. Isaacson, P.J. and Webster, J.M. 2002.  Antimicrobial activity of Xenorhabus sp RIO (Enterobacteriaceae), symbiont of the entomopathogenic nematode, Steinernema riobrave (Rhabditida : Steinernematidae). Journal of Invertebrate Pathology 79: 146-153.
5. Wang, Y.H., Fang, X.L., Li, Y.P. and Zhang, X. 2010.  Effects of constant and shifting dissolved oxygen concentration on the growth and antibiotic activity of Xenorhabdus nematophila. Bioresource Technology 101: 7529-7536.
6. Wang, Y.H., Feng, J.T., Zhang, Q. and Zhang, X. 2008.  Optimization of fermentation condition for antibiotic production by Xenorhabdus nematophila with response surface methodology. Journal of Applied Microbiology 104s: 735-744.
7. Yang, X.F., Qiu, D.W., Yang, H.W., Liu, Z., Zeng, H.M. and Yuan, J.J. 2011.  Antifungal activity of xenocoumacin 1 from Xenorhabdus nematophilus var. pekingensis against Phytophthora infestans. World Journal of Microbiology and Biotechnology 27: 523-528.

Recently, Yang et al. (2011) tested a fungicidal activity of an antibacterial compound called Xenocoumacin 1 (Xcn1) from symbiotic bacterium, Xenorhabdus nematophila var. pekingensis against Potato late blight disease causing fungus, Phytophthora infestans.  These authors reported that this antibacterial compound strongly inhibits P. infestans mycelium growth and sporangia production.

Read following papers on antibacterial compounds from entomopathogenic nematode symbiotic bacteria.

Akhurst, R.J. 1982.  Aantibiotic-activity of xenorhabdus spp, bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae . Journal of General Microbiology 128: 3061.

Bowen, D. 1998. Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280 : 2129.

Fang, X. L., Feng, J.T., Zhang, W. G., Wang, Y. H. and Zhang, X. 2010.  Optimization of growth medium and fermentation conditions for improved antibiotic activity of Xenorhabdus nematophila TB using a statistical approach.  African Journal of Biotechnology: 9: 8068-8077.

Gualtieri, M. 2009. Identification of a new antimicrobial lysine-rich cyclolipopeptide family from Xenorhabdus nematophila. Journal of Antibiotics 62: 295.

Ji, D. 2004. Identification of an antibacterial compound, benzylideneacetone, from Xenorhabdus nematophila against major plant-pathogenic bacteria. FEMS Microbiology Letters 239: 241.

Li, J.X. 1995. Antimicrobial metabolites from a bacterial symbiont. Journal of Natural Products-Lloydia 58: 1081.

Li, J.X. 1997. Nematophin, a novel antimicrobial substance produced by Xenorhabdus nematophilus (Enterobactereaceae). Canadian Journal of Microbiology 43: 770.

Mcinerney, B.V. 1991. Biologically-active metabolites from Xenorhabdus spp .1. dithiolopyrrolone derivatives with antibiotic-activity. Journal of Natural Products 54: 774.

Mcinerney, B.V. 1991. Biologically-active metabolites from Xenorhabdus spp.2. BENZOPYRAN-1-ONE derivatives with gastroprotective activity. Journal of Natural Products 54: 785.

Paul, V.J. 1981. Antibiotics in microbial ecology – isolation and structure assignment of several new anti-bacterial compounds from the insect-symbiotic bacteria Xenorhabdus Spp. Journal of Chemical Ecology 7: 589.

Wang, Y.H.  2008. Enhanced antibiotic activity of Xenorhabdus nematophila by medium optimization. Bioresource Technology 99: 1708.

Yang , X.F., Qiu, D.W., Yang, H.W., Liu, Z., Zeng, H.M. and Yuan, J.J.  2011.  Antifungal activity of xenocoumacin 1 from Xenorhabdus nematophilus var. pekingensis against Phytophthora infestans . World Journal of Microbiology and Biotechnology 27: 523-528.

When the infective juveniles of entomopathogenic nematodes are applied to the soil surface in the fields or thatch layer on glf courses, they start searching for their insect hosts. Once insect larva has been located, the nematode infective juveniles penetrate into the larval body cavity via natural openings such as mouth, anus and spiracles. Infective juveniles of Heterorhabditis nematodes can also enter through the intersegmental membranes of the grub cuticle. Once in the body cavity, infective juveniles release symbiotic bacteria (Xenorhabdus spp. for Steinernematidae and Photorhabdus spp. for Heterorhabditidae) from their gut in insect blood. In the blood, multiplying nematode-bacterium complex causes septicemia and kill their insect host usually within 48 h after infection. Nematodes feed on multiplying bacteria, mature into adults, reproduce and then emerge as infective juveniles from the host cadaver to seek new larvae in the soil.

• Black vine weevil, Otiorhynchus sulcatus is a common insect pest of over 150 plant species that grown in the greenhouses and nurseries. Some of the plant species damaged by black vine weevils include Azalea, Cyclamen, Euonymus, Fuxia, Rosa, Rhododendron and Taxus. Grubs (Larvae) of these weevils generally girdle the main stem, and feed and damage roots leading to nutrient deficiencies. Adults feed on leaves and flowers by notching their edges thus reducing aesthetic value of plants.
• The entomopathogenic nematodes species including Heterorhabditis bacteriophora, H. megidis and Steinernema carpocapase, S. feltiae and S. glaseri have been found to be effective alternatives to chemical insecticides such as chlorpyrifos (Dursban) in controlling black vine weevils. Susceptibility of black vine weevil to nematodes is species and strain specific. The rate of application of the nematode species/strains that tested against black vine weevil varies (5,000- 60,000 infective juveniles/pot) among different studies but nematodes applied at the rate of 5000- 20,000 infective juveniles/pot can cause up to 100% grub mortality.  Nematodes can be easily applied in water suspension as spray applications to the surface of plant growing medium but if nematodes are injected at depths deeper than 5 cm i.e. near to grubs they can cause highest mortality of grubs (70-93%) than those nematodes applied to the surface. All the four larval stages (instars) and pupae of black vine weevil are susceptible to all entomopathogenic nematode species. However, Heterorhabdtis bacteriophora can cause higher mortality of first and second instars than S. carpocapase and S. glaseri. Also, all the three nematodes species are equally effective against third and fourth instars of black vine weevil.

How Entomopathogenic Nematodes Kill Black Vine Weevil

• When the infective juveniles are applied to the surface of plant growing medium or injected in the potting medium, they start searching for their hosts, in this case black vine weevil grubs and pupae. Once a grub/pupa has been located, the nematode infective juveniles penetrate into the grub or pupa body cavity via natural openings (mouth, anus and spiracles). Infective juveniles of Heterorhabditis also enter through the intersegmental members of the grub/pupa cuticle. Once in the body cavity, infective juveniles release symbiotic bacteria (Xenorhabdus spp. for Steinernematidae and Photorhabdus spp. for Heterorhabditidae) from their gut in the grub blood. Multiplying nematode-bacterium complex in the blood causes septicemia and kills the grub usually within 48 h after infection. Nematodes feed on multiplying bacteria, mature into adults, reproduce and then emerge as infective juveniles from the cadaver to seek new grubs or pupae in the potting medium/soil.

1. Heterorhabditis amazonensis- undescribed
2. H. argentinensis- P. temperata
3. H. bacteriophora- Photorhabdus luminescens subsp. laumondii TT01, P. luminescens kayaii subsp. nov., P. luminescens thracensis subsp. nov., P. temperate
4. H. baujardi- undescribed
5. H. brevicaudis- P. luminescens
6. H. downesi- Photorhabdus sp
7. H. floridensis- undescribed
8. H. georgiana- undescribed
9. H. hambletoni- undescribed
10. H. hawaiiensis- P. luminescens
11. H. heliothidis- undescribed
12. H. hepialius- P. luminescens
13. H. hoptha- undescribed
14. H. indica- P. luminescens
15. H. marelata- P. luminescens
16. H. megidis- P. temperata subsp. temperata XlNach
17. H. mexicana- undescribed
18. H. poinari- Photorhabdus sp
19. H. safricana- undescribed
20. H. taysearae- undescribed
21. H. zealandica- P. temperata

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1. Steinernema abbasi- undescribed
2. S. aciari- undescribed
3. S. affine-Xenorhabdus bovienii
4. S. akhursti- undescribed
5. S. anatoliense- undescribed
6. S. apuliae- undescribed
7. S. arenarium- X. kozodoii
8. S. ashiuense- undescribed
9. S. asiaticum- undescribed
10. S. backanense- undescribed
11. S. beddingi- undescribed
12. S. bicornutum- X. budapestensis
13. S. carpocapsae- X. nematophila
14. S. caudatum- undescribed
15. S. ceratophorum- undescribed
16. S. cholashanense- undescribed
17. S. cubanum- X. poinarii
18. S. cumgarense- undescribed
19. S. diaprepesi- undescribed
20. S. eapokense- undescribed
21. S. feltiae- X. bovienii
22. S. glaseri- X. poinarii
23. S. guangdongense- undescribed
24. S. hebeiense- undescribed
25. S. hermaphroditum- undescribed
26. S. intermedium – X. bovienii
27. S. jollieti-undescribed
28. S. karii- undescribed
29. S. khoisanae- undescribed
30. S. kraussei- X. bovienii
31. S. kushidai- X. japonica
32. S. leizhouense- undescribed
33. S. litorale- undescribed
34. S. loci- undescribed
35. S. longicaudum- undescribed
36. S. monticolum- undescribed
37. S. neocurtillae- undescribed
38. S. oregonense- undescribed
39. S. pakistanense- undescribed
40. S. puertoricense- X. romanii
41. S. rarum- X. szentirmaii
42. S. riobrave- Xenorhabdus sp
43. S. ritteri- Xenorhabdus sp
44. S. robustispiculum- undescribed
45. S. sangi- undescribed
46. S. sasonense- undescribed
47. S. scapterisci- X. innexi
48. S. scarabaei- X. koppenhoeferi
49. S. serratum- X. ehlersii
50. S. siamkayai- X. stockiae
51. S. sichuanense- X. bovienii
52. S. silvaticum- undescribed
53. S. tami- Xenorhabdus sp
54. S. texanum- undescribed
55. S. thanhi- undescribed
56. S. thermophilum- X. indica
57. S. websteri- undescribed
58. S. weiseri- undescribed
59. S. yirgalemense- undescribed

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known species of symbiotic bacterial genus Photorhabdus associated with a nematode genus Heterorhabditis.

Identification based on colony morphology and molecular techniques

1. Photorhabdus luminescens (Thomas and Poinar 1979) Boemare et al. 1993
2. P. temperata
3. P. luminescens subsp. luminescens subsp. nov., Fischer-Le Saux, Viallard, Brunel, Normand & Boemare, 1999
4. P. luminescens subsp. akhurstii subsp. nov., Fischer-Le Saux, Viallard, Brunel, Normand & Boemare, 1999
5. P. luminescens subsp. kayaii subsp. nov., Hazir, Stackebrandt, Lang, Schumann, Ehlers & Keskin, 2004
6. P. luminescens subsp. laumondii subsp. nov., Fischer-Le Saux, Viallard, Brunel, Normand & Boemare, 1999
7. P. temperata sp. nov., Fischer-Le Saux, Viallard, Brunel, Normand & Boemare, 1999
8. P. temperata subsp. temperata subsp. nov., Fischer-Le Saux, Viallard, Brunel, Normand & Boemare, 1999
9. P. luminescens subsp. thracensis subsp. nov., Hazir, Stackebrandt, Lang, Schumann, Ehlers & Keskin, 2004

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known species of symbiotic bacterial genus Xenorhabdus Thomas and Poinar 1979 associated with a nematode genus Steinernema.

Identification based on colony morphology and molecular techniques

1. Xenorhabdus beddingii (Akhurst 1986) Akhurst and Boemare 1993
2. X. bovienii (Akhurst 1983) Akhurst and Boemare 1993
3. X. budapestensis Lengyel, Lang, Fodor, Szállás, Schumann, Stackebrandt, 2005
4. X. cabanillasii Tailliez, Pagès, Ginibre & Boemare, 2006
5. X. doucetiae Tailliez, Pagès, Ginibre & Boemare, 2006
6. X. ehlersii Lengyel, Lang, Fodor, Szállás, Schumann, Stackebrandt, 2005
7. X. griffiniae Tailliez, Pagès, Ginibre & Boemare, 2006
8. X. hominickii Tailliez, Pagès, Ginibre & Boemare, 2006
9. X. indica Somvanshi, Lang, Ganguly, Swiderski, Saxena, & Stackebrandt 2006
10. X. innexi Lengyel, Lang, Fodor, Szállás, Schumann, Stackebrandt, 2005
11. X. japonica Nishimura et al. 1995
12. X. koppenhoeferi Tailliez, Pagès, Ginibre & Boemare, 2006
13. X. kozodoii Tailliez, Pagès, Ginibre & Boemare, 2006
14. X. mauleonii Tailliez, Pagès, Ginibre & Boemare, 2006
15. X. miraniensis Tailliez, Pagès, Ginibre & Boemare, 2006
16. X. nematophila (Poinar and Thomas 1965) Thomas and Poinar 1979
17. X. poinarii (Akhurst 1983) Akhurst and Boemare 1993
18. X. romanii Tailliez, Pagès, Ginibre & Boemare, 2006
19. X. stockiae Tailliez, Pagès, Ginibre & Boemare, 2006
20. X. szentirmaii Lengyel, Lang, Fodor, Szállás, Schumann, Stackebrandt, 2005

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