Section: New Results

Evolution of the genomes of endosymbionts in insects: the case of Hamiltonella defensa interacting with its various partners

Insect cells host many endosymbiotic bacteria, which are in general classified according to their importance for the host: “primary” symbionts are by definition mandatory and synthesize essential nutrients for the insects that feed on poor or unbalanced food sources, while “secondary” symbionts are optional and use mutualistic strategies and/or manipulation of reproduction to invade and persist within insect populations. Hamiltonella defensa is a secondary endosymbiont that established two distinct associations with phloemophagous insects. In aphids, it protects the host against parasitoid attacks. Its ability to infect many host tissues, notably the hemolymph, could promote its contact with parasitoid eggs. Despite this protective phenotype, the high costs associated with its presence within the host prevent its fixation in the population. In the whitefly Bemisia tabaci however, this symbiont is found only in cells specialised in hosting endosymbionts, the bacteriocytes. In these cells, it cohabits with other symbiotic species, such as the primary symbiont Portiera aleyrodidarum, a proximity that favors potential exchanges between the two symbionts. It is fixed in populations of B. tabaci, which suggests an important role for the consortium, probably nutritious.

We studied the specificities of each of these systems. First, in the bacteriocytes of B. tabaci, we identified a partitioning of the synthetic capacities of two endosymbionts, H. defensa and P. aleyrodidarum, in addition to a potential metabolic complementation between the symbionts and their host for the synthesis of essential amino acids. We proposed a key nutritive role for H. defensa, which would indicate a transition to a mandatory status in relation to the host and would explain its fixation in the population.

We also focused on the genomic evolution of the genus Hamiltonella, by comparing the strains infecting B. tabaci with a strain infecting the aphids. We highlighted the specialization of the symbionts to their hosts, and found that the genomes of the endosymbionts reflected their respective ecology. The aphid strain thus possesses many virulence factors and is associated with two partners, a bacteriophage and a recombination plasmid. These systems, inactive in the symbiont of B. tabaci, are directly related to the protection against and arms race with parasitoids. Conversely, the presumed avirulence of whitefly endosymbionts is consistent with their nutritional phenotype and a transition to a mandatory status to the host.

Finally, we studied the phenomenon of “accelerated mutation rate” in H. defensa, compared to its sister species Regiella insecticola, which is also a clade of protective endosymbionts of aphids. After excluding the assumption that the transition to the intracellular life occurred independently in the two lineages, we tried to establish a link between these differences in terms of evolvability in the endosymbionts and of their gene contents, particularly for genes involved in ecology and DNA repair. All the results obtained have provided insight into the evolution of the species H. defensa, since the last ancestor to the present species, by establishing a link between bacterial phenotype and genomic evolution.

The publications related to this area of research are either submitted or in preparation (to be submitted in the first months of the year).