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Integrative biology of interactions between bacteria, insects & entomopathogenic nematodes (BIBINE)


Our group focuses on the interactions between bacteria and their invertebrate hosts (insects and nematodes). Regarding the studies on the “mechanisms of interaction between microorganisms and their hosts” in Montpellier, we created in association with the Laboratoire des Symbioses Tropicales & Méditerranéennes, an animation research network named IMH. This topic is also developed in the training units of the Master IMHE in which members of our group are the leaders of the level 1 and 2 or responsible of training units.

Our models are bacteria belonging to the Photorhabdus and Xenorhabdus genera (family Enterobacteriaceae), the insects (Lepidoptera, Spodoptera) as the main studied host and to a lesser extent the entomopathogenic nematodes. Our research activities take into account taxonomy, phylogeny, genomics, mechanisms of the infectious process of the  pathogens involved in these interactions (bacteria and nematodes) and the immune response of the insect host. Photorhabdus and Xenorhabdus are pathogenic to many insect larvae while also maintaining a mutualistic relationship with nematodes from the families Heterorhabditis and Steinernema respectively, where the bacteria occupy the gut of the infective juvenile (IJ) stage (see Description of their life cycle in the figure below). The IJs are used against insect pests of crops in biological control. Photorhabdus and Xenorhabdus are academic models to understand the bacteria-invertebrate relationships. Moreover, our bacterial models are very original in the world of insect pathogens because their way of entry into the body of insects (the hemocoel) is direct, unlike most pathogens that cross the gut such as Bacillus thuringiensis (Nielsen-Leroux et al., 2012). Using syringes instead of nematodes, we have shown that these bacteria are highly pathogenic onto lepidopteran models studied in the DGIMI lab, moths of the genus Spodoptera. Against infections, insects, and invertebrates in general, oppose innate immunity involving both the cell-mediated and humoral aspects. However, Photorhabdus and Xenorhabdus rapidly develop in 24 hours in the insects.


Figure above: The life cycle of Photorhabdus and Xenorhabdus begins with the colonization of the intestinal tract of non-feeding stage of the nematode known as the infective juvenile (IJ). Actually, the IJ stage nematodes generally use natural openings of insect larvae (mouth and anus) as main route of entry (step 1), and end up in digestive track (gut; step 2) before entering in the hemocoel (step 3). However, the nematode Heterorhabditis can also enter into host's body by puncturing the larval cuticle. Within the hemocoel, nematodes release their bacterial symbionts that undergo insect infection (step 3). In the insect cadaver, occur bacterial multiplication and nematode reproduction (step 4). During this life cycle, Photorhabdus and Xenorhabdus must successfully accomplish three distinct roles within the insect host:

  • overcome insect immune response, and kill insects,
  • produce nutrients from the insect cadaver to facilitate development of the nematode, and
  • colonize the IJ stage of the nematode.

After rounds of nematode reproduction, progeny nematodes receive uncharacterized environmental cues that stimulate the development of a new generation of IJs colonized by the bacteria before emerging of several hundred thousand IJs from an insect cadaver. The five BIBINE group's themes of research are indicated in black boxes

The main issues we address are the following (indicated in the figure above):

  • Taxonomy and phylogeny of entomopathogenic bacteria and nematodes.
  • Genomics of the bacteria, Photorhabdus and Xenorhabdus, with particular specialization in genome plasticity.
  • Functional Genomics in Photorhabdus and Xenorhabdus, which allowed the characterization of the genetic basis of pathogenicity and the characterization of the main regulons involved in virulence.
  • Features of the infectious process in Photorhabdus and Xenorhabdus, specifically where and when bacterial virulence genes are expressed in the insect.
  • Impact of the bacterial virulence factors on the immune functions of the insect. Resistance to humoral immunity (antimicrobial peptides) was particularly studied in recent years in different bacteria-invertebrate relationships.
  • A final point that we address, which is transversal to all previous issues, is the characterization of the phenotypic heterogeneity in a clonal population observed in these two bacterial genera.

See also

NIELSEN-LEROUX CGAUDRIAULT S, RAMARAO N, LERECLUS D, GIVAUDAN A2012. How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus Photorhabdus occupy their hosts. Curr Opin Microbiol. 15:220-231.

OGIER JCPAGES SBISCH G, CHIAPELLO H, MEDIGUE C, ROUY Z, TEYSSIER C, VINCENT S, TAILLIEZ PGIVAUDAN AGAUDRIAULT S2014. Attenuated virulence and genomic reductive evolution in the entomopathogenic bacterial symbiont species, Xenorhabdus poinariiGenome Biol Evol. 6:1495-513.

JUBELIN G, LANOIS A, SEVERAC D, RIALLE S, LONGIN C, GAUDRIAULT S, GIVAUDAN A. 2013. FliZ is a global regulatory protein rheostatically affecting the expression of flagellar and virulence genes in individual Xenorhabdus bacterial cells. PLoS genetics. 9(10): e1003915. doi:10.1371/journal.pgen.1003915

DUVIC B, JOUAN V, ESSA N., GIRARD PA, PAGES S, ABI KHATTAR Z, VOLKOFF AN, GIVAUDAN A, DESTOUMIEUX-GARZON D, ESCOUBAS JM. 2012. Cecropins as a marker of Spodoptera frugiperda immunosuppression during entomopathogenic bacterial challenge. J Insect Physiol. 58:881-888.

Genomic of Photorhabdus et Xenorhabdus

Genomic diversity and phylogenomic of Photorhabdus and Xenorhabdus
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Adaptation of entomopathogenic bacteria to antimicrobial peptides produced by their hosts

How do insect pathogenic bacteria cope with antimicrobial peptides in host?
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Deciphering the "master" gene of virulence and studies of gene expression during infection.

The regulatory protein FliZ of Xenorhabdus creates two sub-populations which express different infectious potential within an isogenic population of...
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Taxonomy and phylogeny of symbiotic bacteria associated with entomopathogenic nematodes

Since the end of 1980s, our laboratory is considered as a reference laboratory in taxonomy and phylogeny of Photorhabdus and Xenorhabdus.
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