Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants

Symbiosis is a common phenomenon in nature that substantially affects organismal ecology and evolution. Fundamental questions regarding how mutualistic associations arise and evolve in nature remain, however, poorly studied. The aphid-Serratia symbiotica bacterium interaction represents a valuable model to study mechanisms shaping these symbiotic interspecific interactions. S. symbiotica strains capable of living independently of aphid hosts have recently been isolated. These strains probably resulted from horizontal transfers and could be an evolutionary link to an intra-organismal symbiosis. In this context, we used the tripartite interaction between the aphid Aphis fabae, a cultivable S. symbiotica bacterium, and the host plant Vicia faba to evaluate the bacterium ability to circulate in this system, exploring its environmental acquisition by aphids and horizontal transmission between aphids via the host plant. Using molecular analyses and fluorescence techniques, we showed that the cultivable S. symbiotica can enter the plants and induce new bacterial infections in aphids feeding on these new infected plants. Remarkably, we also found that the bacterium can have positive effects on the host plant, mainly at the root level. Furthermore, our results demonstrated that cultivable S. symbiotica can be horizontally transferred from infected to uninfected aphids sharing the same plant, providing first direct evidence that plants can mediate horizontal transmission of certain strains of this symbiont species. These findings highlight the importance of considering symbiotic associations in complex systems where microorganisms can circulate between different compartments. Our study can thus have major implications for understanding the multifaceted interactions between microbes, insects and plants

Evolution of bacterial mutualism in insects: the case of Serratia symbiotica in aphids

Serratia symbiotica, one of most frequent symbiont found in aphids, is a valuable symbiont candidate for studying the evolution of bacterial mutualism in insects. Indeed, this bacterial symbiont species includes a wide variety of strains ranging from a free-living to intracellular lifestyles, being either facultative, either co-obligate partners for the host aphid. The main purpose of this work was to investigate how symbiotic bacteria form new associations and extend their influence in insect populations. A culture-dependent approach was used to decipher the microbial diversity hosted by several aphid species. Novel microbial partners of aphids were identified and several novel S. symbiotica strains were isolated. Genomic features displayed by S. symbiotica strain CWBI-2.3T that likely play a role in the establishment of symbiosis were scrutinized. Our analysis supports for the presence of many genes potentially involved in host interactions. We demonstrate that the aphid gut is a suitable environment for the multiplication of S. symbiotica whose does not induce immediate pathogenic effects and do not trigger the aphid immune defenses that were investigated. In addition, the symbiont is able to express a wide range of molecular effectors that are potentially required during the initial stages of host colonization. Finally, we highlight the existence of gut-associated S. symbiotica strains in wild aphids and ants populations, illustrating the extraordinary diversity and versatility of the symbiont. Although the symbiotic status of these extracellular S. symbiotica strains has not yet been clearly identified, it appears that both facultative and co-obligate intracellular strains are derived from free-living S. symbiotica strains that have been gradually domesticated by the host insect. In view of these results, S. symbiotica strains exhibiting a free-living capacity represent tremendous candidates to investigate the origins of bacterial mutualism in insects

Evolution of bacterial mutualism in insects : the case of Serratia symbiotica in aphids

Serratia symbiotica, one of most frequent symbiont found in aphids, is a valuable symbiont candidate for studying the evolution of bacterial mutualism in insects. Indeed, this bacterial symbiont species includes a wide variety of strains ranging from a free-living to intracellular lifestyles, being either facultative, either co-obligate partners for the host aphid. The main purpose of this work was to investigate how symbiotic bacteria form new associations and extend their influence in insect populations. A culture-dependent approach was used to decipher the microbial diversity hosted by several aphid species. Novel microbial partners of aphids were identified and several novel S. symbiotica strains were isolated. Genomic features displayed by S. symbiotica strain CWBI-2.3T that likely play a role in the establishment of symbiosis were scrutinized. Our analysis supports for the presence of many genes potentially involved in host interactions. We demonstrate that the aphid gut is a suitable environment for the multiplication of S. symbiotica whose does not induce immediate pathogenic effects and do not trigger the aphid immune defenses that were investigated. In addition, the symbiont is able to express a wide range of molecular effectors that are potentially required during the initial stages of host colonization. Finally, we highlight the existence of gut-associated S. symbiotica strains in wild aphids and ants populations, illustrating the extraordinary diversity and versatility of the symbiont. Although the symbiotic status of these extracellular S. symbiotica strains has not yet been clearly identified, it appears that both facultative and co-obligate intracellular strains are derived from free-living S. symbiotica strains that have been gradually domesticated by the host insect. In view of these results, S. symbiotica strains exhibiting a free-living capacity represent tremendous candidates to investigate the origins of bacterial mutualism in insects.(SC - Sciences) -- UCL, 201

The nutritional dimension of facultative bacterial symbiosis in aphids: Current status and methodological considerations for future research

Aphids are valuable models for studying the functional diversity of bacterial symbiosis in insects. In addition to their ancestral obligate nutritional symbiont Buchnera aphidicola, these insects can host a myriad of so-called facultative symbionts. The diversity of these heritable bacterial associates is now well known, and some of the ecologically important traits associated with them have been well documented. Some twenty years ago, it was suggested that facultative symbionts could play an important role in aphid nutrition, notably by improving feeding performance on specific host plants, thus influencing the adaptation of these insects to host plants. However, the underlying mechanisms have never been elucidated, and the nutritional role that facultative symbionts might perform in aphids remains enigmatic. In this opinion piece, I put forward a series of arguments in support of the hypothesis that facultative symbionts play a central role in aphid nutrition and emphasize methodological considerations for testing this hypothesis in future work. In particular, I hypothesize that the metabolic capacities of B. aphidicola alone may not always be able to counterbalance the nutritional deficiencies of phloem sap. The association with one or several facultative symbionts with extensive metabolic capabilities would then be necessary to buffer the insect from host plant-derived nutrient deficiencies, thus enabling it to gain access to certain host plants