How do symbionts produce the effects observed

With the phenotypic influence of symbionts having been only recently discovered, it is inevitably the case that we can only speculate on the mechanistic basis of symbiont-induced protection. There are two basic possibilities. The first is that the effect is mediated through existing host systems. The second is that the effect is direct, and has no element of interaction with the host. The former hypothesis has been suggested for Wolbachia-induced resistance to viruses. Teixera et al. (2008) suggested that resistance might be mediated through Wolbachia actively interfering with pro-apoptotic pathways of the host, in order to produce their maintenance. This interference prevents viruses accessing these pathways during their life cycle, slowing their transmission within the host. One can imagine also that bacterial symbionts may affect host innate immunity: they may prime it, giving prophylaxis, or secrete molecules that downregulate it, which would be associated with increased susceptibility.

The alternative mechanism by which sym-biont effects on resistance may function is a direct effect. Direct effects could come from secreted molecules that affect the invading species alone. A useful model may be the biology of the gamma proteobacterium Photorhabdus luminescens, which is a nematode-transmitted pathogen of insects. It inhabits nematode guts without pathology. When the nematode host invades an insect, Photorhabdus moves from nematode gut to insect haemocoel. In this latter context, the bacterium is a virulent pathogen, with a formidable array of secreted compounds that protect against the host innate immune system, and which cause active pathology to the host (for instance, through damage to the gut epithelia). Photorhabdus thus demonstrates context-dependent virulence. Change in host species (from nematode to insect) leads to radical change in bacterial behaviour (from commensal to pathogenic).

For a secondary symbiont bacterium, ingestion by a parasitoid may produce a similar change in bacterial behaviour towards virulence. For Hamiltonella and Serratia, RTX genes are notably present, as well as a variety of toxin genes associated with phage, such as a homologue of Stx (Shiga toxin), cdtB (cytolethal distending toxin), and YD-repeat containing open reading frames (allied to the Toxin Complex genes commonly found in entomopatho-genic bacteria such as Photorhabdus), each of which are known to harm eukaryotic cells (Moran et al., 2005a; Degnan and Moran, 2008). Whereas a role for these genes in symbiosis is possible, a role in pathology on exposure to parasitoids or other natural enemies is a very tempting hypothesis.

Aside from toxicity, the other feature required for this hypothesis is context-dependent behaviour. Cases where bacteria, including pathogens, alter behaviour in response to environmental cues are well known, and commonly encoded through two component systems (Hentschel et al., 2000). These are sensory-response circuits operating through kinase genes whose activity varies with environmental conditions. Under appropriate conditions, they are activated and alter the phosphorylation state of their cognate protein. In many cases the cognate protein is a transcription factor, and the alteration of phosphorlyation effects a change in the genes that are expressed, appropriate to the environment. In other cases, the cognate protein is a protease or demethylase, whose activity is then altered, producing a change in bacterial behaviour. The involvement of the PhoP/PhoQ two-component systems in the switch to insect symbiosis is established for Photorhabdus, and represents a promising avenue of research for regulation of symbiont behaviour in general, especially in the gamma pro-teobacteria (Derzelle et al, 2004).

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