Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-26T08:26:49.542Z Has data issue: false hasContentIssue false

Effect of phenotypic variation in Xenorhabdus nematophila on its mutualistic relationship with the entomopathogenic nematode Steinernema carpocapsae

Published online by Cambridge University Press:  28 June 2005

M. SICARD
Affiliation:
Laboratoire Génome, Populations, Interactions, Adaptation UMR 5171 CNRS-UMII-IFREMER, Université de Montpellier, Montpellier, France
J. TABART
Affiliation:
Laboratoire Ecologie Microbienne des Insectes et Interactions Hôte-pathogène UMR 1133 INRA-UMII, Université de Montpellier, Montpellier, France
N. E. BOEMARE
Affiliation:
Laboratoire Ecologie Microbienne des Insectes et Interactions Hôte-pathogène UMR 1133 INRA-UMII, Université de Montpellier, Montpellier, France
O. THALER
Affiliation:
Laboratoire Ecologie Microbienne des Insectes et Interactions Hôte-pathogène UMR 1133 INRA-UMII, Université de Montpellier, Montpellier, France
C. MOULIA
Affiliation:
Laboratoire Génome, Populations, Interactions, Adaptation UMR 5171 CNRS-UMII-IFREMER, Université de Montpellier, Montpellier, France

Abstract

The entomopathogenic nematode Steinernema carpocapsae is mutualistically associated with the bacterium Xenorhabdus nematophila. Infective Juveniles (IJs) transport X. nematophila cells that provide them with good conditions to reproduce within the insect. In the laboratory, long term stationary-phase culture conditions sometimes lead X. nematophila's variant 1 cells, which were previously isolated from the worms, to spontaneously and irreversibly change into a new phenotypic variant (variant 2). In this paper, we tested the ability of each phenotypic variant to (i) be transmitted by IJs, (ii) to optimize the worm's fitness within the insect, and (iii) to counteract the effect of closely related antagonistic bacteria previously shown as being able to totally prevent S. carpocapsae's reproduction within the insect. We found that IJs did associate with cells of both phenotypes but that the variant 2 cells were preferentially retained by the nematodes when both variants were present in the insect. Both phenotypic variants led to the same fitness of S. carpocapsae in insects not infected by antagonistic bacteria. In insects infected by antagonistic bacteria, both variants were able to provide protection to S. carpocapsae. Nevertheless, this protection depended on the phenotypic variant and the antagonistic bacteria that were co-injected into the insect. Further analysis conduced in vitro showed that this variability could be partly linked to the sensitivity of each antagonistic bacterium to xenorhabdicin, produced by X. nematophila.

Type
Research Article
Copyright
© 2005 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.)

References

REFERENCES

Akhurst, R. J. ( 1980). Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes, Neoplectana and Heterorhabditis. Journal of General Microbiology 121, 303309.Google Scholar
Akhurst, R. J. ( 1982). Antibiotic activity of Xenorhabdus spp., bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. Journal of General Microbiology 128, 30613065.Google Scholar
Akhurst, R. J. and Boemare, N. E. ( 1988). A numerical taxonomic study of the genus Xenorhabdus (Enterobacteriaceae) and proposed elevation of the subspecies of X. nematophilus to species. Journal of General Microbiology 134, 18351845.CrossRefGoogle Scholar
Bird, A. F. and Akhurst, R. ( 1983). The nature of the intestinal vesicle in nematodes of the family Steinernematidae. International Journal for Parasitology 13, 599606.CrossRefGoogle Scholar
Boemare, N. E. and Akhurst, R. J. ( 1988). Biochemical and physiological characterization of colony form variants in Xenorhabdus spp. (Enterobacteriaceae) Journal of General Microbiology 134, 751761.CrossRefGoogle Scholar
Boemare, N. E. Boyer-Giglio, M. H., Thaler, J. O., Akhurst, R. J. and Brehelin, M. ( 1992). Lysogeny and bacteriocinogeny in Xenorhabdus nematophilus and other Xenorhabdus spp. Applied and Environmental Microbiology 58, 30323037.Google Scholar
Brunel, B., Givaudan, A., Lanois, A., Akhurst, R. J. and Boemare, N. E. ( 1997). Fast and accurate identification of Xenorhabdus and Photorhabdus species by restriction analysis of PCR-amplified 16S rRNA genes. Applied and Environmental Microbiology 63, 574580.Google Scholar
Givaudan, A. and Lanois, A. ( 2000). flhDC, the flagellar master operon of Xenorhabdus nematophilus: requirement for motility, lipolysis, extracellular hemolysis, and full virulence in insects. Journal of Bacteriology 182, 107115.CrossRefGoogle Scholar
Givaudan, A., Lanois, A. and Boemare, N. ( 1996). Cloning and nucleotide sequence of a flagellin encoding genetic locus from Xenorhabdus nematophilus: phase variation leads to differential transcription of two flagellar genes (fliCD). Gene 183, 243253.CrossRefGoogle Scholar
Laumond C., Mauléon H. and Kermarrec A. ( 1979). Données nouvelles sur le spectre d'hôtes et le parasitisme du nématode entomophage Neoplectana carpocapsae. Entomophaga 24, 1327.CrossRefGoogle Scholar
Leisman, G. B., Waukau, J. and Forst, S. A. ( 1995). Characterization and environmental regulation of outer membrane proteins in Xenorhabdus nematophilus. Applied and Environmental Microbiology 61, 200204.Google Scholar
Lengyel, K., Lang, E., Fodor, A., Szállás, E., Schummann, P. and Stackebrandt, E. ( 2005). Description of four novel species of Xenorhabdus, family Enterobacteriaceae: Xenorhabdus budapestensis sp. nov., Xenorhabdus ehlersii sp. nov., Xenorhabdus innexi sp. nov., Xenorhabdus szentirmaii sp. nov. Systematic and Applied Microbiology 28, 155122.Google Scholar
Martens, E. C., Heungens, K. and Goodrich-Blair, H. ( 2003). Early colonization events in the mutualistic association between Steinernema carpocapsae nematodes and Xenorhabdus nematophila bacteria. Journal of Bacteriology 185, 31473154.CrossRefGoogle Scholar
Morgan J. A., Kuntzelmann V., Taverno S., Ousley M. A. and Winstanley C. ( 1997). Survival of Xenorhabdus nematophilus and Photorhabdus luminescens in water and soil. Journal of Applied Microbiology 83, 665670.CrossRefGoogle Scholar
Poinar, G. O. and Thomas, G. M. ( 1966). Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteriaceae: Eubacteriales) in the development of the nematode, DD-136 (Neoplectana sp. Steinernematidae). Parasitology 56, 385390.CrossRefGoogle Scholar
Riley, M. A. and Gordon, D. M. ( 1999). The ecological role of bacteriocins in bacterial competition. Trends in Microbiology 7, 129133.CrossRefGoogle Scholar
Riley, M. A. and Wertz, J. E. ( 2002). Bacteriocins: evolution, ecology, and application. Annual Review of Microbiology 56, 117137.CrossRefGoogle Scholar
Sicard, M., Brugirard-Ricaud, K., Pagès, S., Lanois, A., Boemare, N. E., Brehélin, M. and Givaudan, A. ( 2004 a). Stages of infection during the tripartite interaction between Xenorhabdus nematophila, its nematode vector, and insect hosts. Applied and Environmental Microbiology 70, 64736480.Google Scholar
Sicard, M., Ferdy, J. B., Pagès, S., Le Brun, N., Godelle, B., Boemare, N. and Moulia, C. ( 2004 b). When mutualists are pathogens: an experimental study of the symbioses between Steinernema (entomopathogenic nematodes) and Xenorhabdus (bacteria). Journal of Evolutionary Biology 17, 985993.Google Scholar
Sicard, M., Le Brun, N., Pagès, S., Godelle, B., Boemare, N. and Moulia, C. ( 2003). Effect of native Xenorhabdus on the fitness of their Steinernema hosts: contrasting types of interaction. Parasitology Research 91, 520524.CrossRefGoogle Scholar
Smigielski, A., Akhurst, R. and Boemare, N. ( 1994). Phase variation in Xenorhabdus nematophilus and Photorhabdus luminescens: differences in respiratory activity and membrane energization. Applied and Environmental Microbiology 60, 120125.Google Scholar
Thaler, J.-O., Boyer-Giglio, M.-H. and Boemare, N. ( 1997). New antimicrobial barriers produced by Xenorhabdus spp. and Photorhabdus spp. to secure the monoxenic development of entomopathogenic nematodes. Symbiosis 22, 205215.Google Scholar
Thaler, J. O., Baghdiguian, S. and Boemare, N. ( 1995). Purification and characterization of xenorhabdicin, a phage tail-like bacteriocin, from the lysogenic strain F1 of Xenorhabdus nematophilus. Applied and Environmental Microbiology 61, 20492052.Google Scholar
Thaler, J. O., Duvic, B., Givaudan, A. and Boemare, N. ( 1998). Isolation and entomotoxic properties of the Xenorhabdus nematophilus F1 lecithinase. Applied and Environmental Microbiology 64, 23672373.Google Scholar
Volgyi, A., Fodor, A. and Forst, S. ( 2000). Inactivation of a novel gene produces a phenotypic variant cell and affects the symbiotic behavior of Xenorhabdus nematophilus. Applied and Environmental Microbiology 66, 16221628.CrossRefGoogle Scholar
Volgyi, A., Fodor, A., Szentirmai, A. and Forst, S. ( 1998). Phase variation in Xenorhabdus nematophilus. Applied and Environmental Microbiology 64, 11881193.Google Scholar
White, G. ( 1927). A method for obtaining infective nematode larvae from culture. Science 66, 302303.CrossRefGoogle Scholar
Yamamoto, K., Alberts, R., Benzinger, R., Lawthorne, L. and Trieber, G. ( 1970). Rapid bacteriophage sedimentation in the presence of polyrthyethylene glycol and its application to large-scale virus purification. Virology 40, 734744.CrossRefGoogle Scholar
Zhou, X., Kaya, H. K., Heungens, K. and Goodrich-Blair, H. ( 2002). Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Applied and Environmental Microbiology 68, 62026209.CrossRefGoogle Scholar