Insects, bacteria and viruses: Serratia symbiotica, a new candidate mediating defensive mutualism in the microbial symbiosis ?

Renoz, François [UCL] Pons-Guillouard, Inès [UCL] Gillis, Annika [UCL] Noël, Christine [UCL] Mahillon, Jacques [UCL] Hance, Thierry [UCL]

Antagonistic interactions between animals and their natural enemies have generated remarkable levels of polymorphism, have impacted adaptive evolution of the involved protagonists and explain the maintenance of sex. Usually focused on eukaryote-controlled mechanisms of host protection (e. g. immunity), researches currently recognize that symbiotic microbes also mediate interactions between natural enemies and their host. Microbial symbioses are widespread in insects, and the aphid superfamily represents a valuable model to assess the influence of symbiotic bacteria on the antagonistic interactions and the coevolution processes between insect hosts and their natural enemies. These sap-feeding insects typically harbor one nutritional obligate endosymbiont and a wide variety of facultative symbionts that can have beneficial effects in the context of specific environmental conditions. Hamiltonella defensa, one of the most common facultative symbiont found in aphids, has been reported as the first case of defensive symbiont found in insects. Its presence in the aphid tissues significantly reduces the rates of successful parasitism by parasitic wasps. This protection associated to H. defensa is due to the presence of a phage called APSE (Acyrthosiphon pisum secondary endosymbiont) in the symbiont genome that produces toxins specifically targeting wasp cells causing death of the developing wasp larvae. Despite evidences that bacterial symbionts and their associated viruses can interfere with parasitic relationships in insects, the possibility of finding these protective aptitudes in other facultative symbionts than H. defensa remain poorly investigated. Here, we examined these protective effects in another facultative symbiont that is regularly found in aphids: Serratia symbiotica. We firstly tested the potential protective effects against parasitoids associated to S. symbiotica strain CWBI-2.3T, a free-living that is routinely cultured in our lab. We found that, when ingested and infecting the black bean aphid Aphis fabae at the gut level, S. symbiotica strain CWBI-2.3T provided aphids protection against A. colemani parasitism at three levels. The strain significantly reduces the parasitism rate of A. fabae following parasitoid attack, the emergence rate of parasitoids from A. fabae and the weight of emerged parasitoids. We therefore investigated the presence of phages in the S. symbiotica CWBI-2.3T genome as well as in the genome of four other S. symbiotica strains. We found that two strains of the symbiont (including strain CWBI-2.3T) harbor an astonishing diversity of phage regions in their genomes. The potential role of this phage diversity in S. symbiotica is discussed in the context of the defensive mutualism in insects. Our study highlights the importance to consider bacterial symbionts and their associated viruses when assessing the antagonistic relationships between insects and their natural enemies.