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State of the art

Our models are bacteria belonging to the genera Xenorhabdus and Photorhabdus (family Morganellaceae), insects (Lepidoptera, Spodoptera as main host studied) and entomopathogenic nematodes (EPNs). Xenorhabdus and Photorhabdus are pathogenic to the larvae of many insects while maintaining a mutualistic relationship with nematodes of the families Steinernema and Heterorhabditis, in which the bacteria occupy the gut of infective juvenile stages (IJ). These bacteria are novel academic models for understanding bacterial-host interactions, mutualism and pathogenesis in invertebrates. They are very original in the world of insect pathogens because their route of entry into the insect body (the hemocoele) is direct thanks to their vectoring by their nematode, unlike most pathogens that pass through the insect gut like Bacillus thuringiensis.

These insect parasites are used against insect pests of crops in the context of biocontrol. The parasite cycle of these nematobacterial complexes is as follows: IJs search for insects in the soil and enter their bodies. They release their bacterial symbiont directly into the hemocoele to cause sepsis (pathogenic phase) (Figure 1A). Using syringes instead of nematodes, we have shown that these bacteria are highly pathogenic on the model lepidopterans studied in the laboratory. Against bacterial infections, insects oppose an innate immunity involving both cell-mediated (hemocytes) and humoral (AntiMicrobial Peptides, AMPs) aspects. However, both Xenorhabdus and Photorhabdus develop rapidly within 24 hours in insects. The insect cadaver and symbiotic bacteria are then exploited as a nutritional resource during nematode reproduction (necrotrophic phase) (Figure 1B). Following a nutrient deficiency, a nematode larval stage (L3) re-associates with the bacterial symbiont, generating IJs that emerge, leave the cadaver, and can then forage for a new insect (Free phase) (Figure 1A).

Figure 1. Parasite cycle of nematobacterial complexes (J.-C. Ogier & S. De La Forest Divonne, unpublished)

The main objectives of the team are:

• A better knowledge of entomopathogenic agents belonging to the genera Xenorhabdus and Photorhabdus.
• The identification of the mechanisms that govern the different interactions (bacterial virulence and insect response, bacterial-bacterial interaction, nematode development).

In order to obtain an integrated vision of this tripartite interaction, the main questions we have addressed so far are the following:

• The taxonomy and genomics of bacteria, Photorhabdus and Xenorhabdus, with a particular focus on genome plasticity and evolutionary genomic history.
• The impact of bacterial virulence factors on insect immune functions. Resistance to humoral immunity has been particularly studied.
• The characterization of the phenotypic heterogeneity of these bacteria. Since 2015, the most studied mechanism is DNA methylation.

Recently our work has been more integrative by including:

• A consideration of the notion of pathobiome by a description of the nematode microbiota (metagenomic and culturomic) in view of a characterization of the functions of this microbiota in the parasite cycle.
• The study of social relationships (antagonism, cooperation, cheating, bet-hedging) between bacteria (symbionts, their different variants, members of the microbiota) and their dynamics within invertebrate hosts (nematode and insect).

4 axis are developed in the team:

Taxonomy and valuation of entomopathogenic nematodes and their symbiotic bacteria

The research work carried out on this theme by our team was initiated by Noël Boemare in the 1980s.

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Bacterial genomics, metagenomics and nematode microbiota

The study of the evolutionary genomic history of Xenorhabdus/Photorhabdus bacteria and the integration of the concept of pathobiome in the study of the...

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Characterization of the phenotypic heterogeneity in entompathogenic bacteria

What mechanisms contribute to the appearance of clonal bacterial subpopulations?

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Insect immune response and impact of the nematobacterial complex

How does the insect respond to the nematobacterial complex and how do pathogenic bacteria circumvent this invertebrate host response?

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Key publications

Ogier, J.-C., Pages, S., Frayssinet, M., Gaudriault, S. 2020. Entomopathogenic nematode-associated microbiota: from monoxenic paradigm to pathobiome. Microbiome, 8, 1-17. DOI : 10.1186/s40168-020-00800-5.

Huot, L., Bigourdan, A., Pages, S., Ogier, J.-C., Girard, P.-A., Nègre, N., Duvic, B. 2020. Partner-specific induction of Spodoptera frugiperda immune genes in response to the entomopathogenic nematobacterial complex Steinernema carpocapsae-Xenorhabdus nematophila. Dev Comp Immunol, 108, 103676. DOI : 10.1016/j.dci.2020.103676.

Cambon, M.C., Parthuisot, N., Pages, S., Lanois, A., Givaudan, A., Ferdy, J.-B. 2019. Selection of bacterial mutants in late infections: when vector transmission trades off against growth advantage in stationary phase. mBio, 10, 1-14. DOI : 10.1128/mBio.01437-19.

Pantel, L., Florin, T., Dobosz-Bartoszek, M., Racine, E., Sarciaux, M., Serri, M., Houard, J., Campagne, J.-M., de Figueiredo, R.M., Midrier, C., Gaudriault, S., Givaudan, A., Lanois, A., Forst, S., Aumelas, A., Cotteaux-Lautard, C., Bolla, J.M., Vingsbo Lundberg, C., Huseby, D.L., Hughes, D., Villain-Guillot, P., Mankin, A.S., Polikanov, Y.S., Gualtieri, M. 2018. Odilorhabdins, antibacterial agents that cause miscoding by binding at a new ribosomal site. Mol Cell, 70, 83-94.e7. DOI : 10.1016/j.molcel.2018.03.001.

Payelleville, A., Legrand, L., Ogier, J.-C., Roques, C., Roulet, A., Bouchez, O., Mouammine, A., Givaudan, A., Brillard, J. 2018. The complete methylome of an entomopathogenic bacterium reveals the existence of loci with unmethylated adenines. Sci Rep, 8, 1-14. DOI : 10.1038/s41598-018-30620-5.

Labreuche, Y., Chenivesse, S., Jeudy, A., Le Panse, S., Boulo, V., Ansquer, D., Pagès, S., Givaudan, A., Czjzek, M., Le Roux, F. 2017. Nigritoxin is a bacterial toxin for crustaceans and insects. Nat Commun, 8, 1248. DOI : 10.1038/s41467-017-01445-z.