Aphids are one of the most serious pests of crops worldwide, causing major yield and economic losses. To control aphids, natural enemies could be an option but their efficacy is sometimes limited by their dispersal in natural environment. Here we report the first isolation of a bacterium from the pea aphid Acyrthosiphon pisum honeydew, Staphylococcus sciuri, which acts as a kairomone enhancing the efficiency of aphid natural enemies. Our findings represent the first case of a host-associated bacterium driving prey location and ovipositional preference for the natural enemy. We show that this bacterium has a key role in tritrophic interactions because it is the direct source of volatiles used to locate prey. Some specific semiochemicals produced by S. sciuri were also identified as significant attractants and ovipositional stimulants. The use of this host-associated bacterium could certainly provide a novel approach to control aphids in field and greenhouse systems.

An intracellular symbiotic bacterium was isolated from the flora of a natural clone of the black bean aphid Aphis fabae. The strain was able to grow freely in aerobic conditions on a rich medium containing 1 % of each of the following substrates: glucose, yeast extract and casein peptone. Pure culture was achieved through the use of solid-phase culture on the same medium and the strain was designated CWBI-2.3T. 16S rRNA gene sequence analysis revealed that strain CWBI-2.3T was a member of the class Gammaproteobacteria, having high sequence similarity (>99 %) with ‘Candidatus Serratia symbiotica’, the R-type of secondary endosymbiont that is found in several aphid species. As strain CWBI-2.3T ( = LMG 25624T = DSM 23270T) was the first R-type symbiont to be isolated and characterized, it was designated as the type strain of Serratia symbiotica sp. nov.

Aphids feed on the phloem sap of plants, and are the most common honeydew-producing insects. While aphid honeydew is primarily considered to comprise sugars and amino acids, its protein diversity has yet to be documented. Here, we report on the investigation of the honeydew proteome from the pea aphid Acyrthosiphon pisum. Using a two-Dimensional Differential in-Gel Electrophoresis (2D-Dige) approach, more than 140 spots were isolated, demonstrating that aphid honeydew also represents a diverse source of proteins. About 66% of the isolated spots were identified through mass spectrometry analysis, revealing that the protein diversity of aphid honeydew originates from several organisms (i.e. the host aphid and its microbiota, including endosymbiotic bacteria and gut flora). Interestingly, our experiments also allowed to identify some proteins like chaperonin, GroEL and Dnak chaperones, elongation factor Tu (EF-Tu), and flagellin that might act as mediators in the plant-aphid interaction. In addition to providing the first aphid honeydew proteome analysis, we propose to reconsider the importance of this substance, mainly acknowledged to be a waste product, from the aphid ecology perspective.

In natural environment, semiochemicals are involved in many interactions between the different trophic levels involving insects, plants and hosts for parasitoids or prey for predators. These volatile compounds act as messengers within or between insect species, inducing particular behaviours, such as the localisation of a source of food, the orientation to an adequate oviposition site, the selection of a suitable breeding site and the localisation of hosts or prey. In this sense, bacteria have been shown to play an important role in the production of volatile compounds which ones act as semiochemicals. This review, focusing on the semiochemically mediated interactions between bacteria and insects, highlights that bacterial semiochemicals act as important messengers for insects. Indeed, in most of the studies reported here, insects respond to specific volatiles emitted by specific bacteria hosted by the insect itself (gut, mouthparts, etc.) or present in the natural environment where the insect evolves. Particularly, bacteria from the families Enterobacteriaceae, Pseudomonaceae and Bacillaceae are involved in many interactions with insects. Because semiochemicals naturally produced by bacteria could be a very interesting option for pest management, advances in this field are discussed in the context of biological control against insect pests.

The mutualistic relationships between certain ant and aphid species are well known, the primary benefits being protection for the aphids and carbohydrate-rich honeydew for the ants. Questions remain, however, as to the exact semiochemical factors that establish and maintain such relationships. In this study, we used a series of treatments and associated controls placed at the end of a two-way olfactometer to determine the degree of attractiveness of a complete plant-aphid-honeydew system as well as individual components of that system. Both the olfactometer branch selected by the black garden ant (Lasius niger) and the linear speed with which ants moved through the device were measured. Study results showed that ants were attracted not just to the complete plant system and the honeydew itself, but also to the microbial flora in the absence of plant or honeydew, and specifically to a bacterium from the black bean aphid (Aphis fabae) honeydew, Staphylococcus xylosus. This bacterium produces a blend of semiochemicals that attract the ant scouts. This information suggests the presence of a naturally occurring, reliable biotic cue for detection of potential aphid partners. This would have to be confirmed in natural conditions by further field experiments. Rather than being opportunistic species that coincidentally colonize a sugarrich environment, microorganisms living in aphid honeydew may be able to alter emissions of volatile organic compounds (VOCs), thus significantly mediating partner attraction. A bacterial involvement in this mutualistic relationship could alter the manner in which these and similar relationships are viewed and evaluated. Future studies into mutualism stability and function among macroscopic partners will likely need for transition from a two-partner perspective to a multiple-partner perspective, and consider the microbial component, with the potential for one or more taxa making significant contributions to the relationship.