New Insights into the Nature of Symbiotic Associations in Aphids: Infection Process, Biological Effects, and Transmission Mode of Cultivable Serratia symbiotica Bacteria

S. symbiotica is one of the most common symbionts among aphid populations and includes a wide variety of strains whose degree of interdependence on the host may vary considerably. S. symbiotica strains with a free-living capacity have recently been isolated from aphids. By using these strains, we established artificial associations by simulating new bacterial acquisitions involved in aphid gut infections to decipher their infection processes and biological effects on their new hosts. Our results showed the early stages involved in this route of infection. So far, S. symbiotica has been considered a maternally transmitted aphid endosymbiont. Nevertheless, we show that our cultivable S. symbiotica strains occupy and replicate in the aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, cultivable S. symbiotica bacteria are both parasites and mutualists given the context, as are many aphid endosymbionts. Our findings give new perception of the associations involved in bacterial mutualism in aphids. ABSTRACT Symbiotic microorganisms are widespread in nature and can play a major role in the ecology and evolution of animals. The aphid-Serratia symbiotica bacterium interaction provides a valuable model to study the mechanisms behind these symbiotic associations. The recent discovery of cultivable S. symbiotica strains with a free-living lifestyle allowed us to simulate their environmental acquisition by aphids to examine the mechanisms involved in this infection pathway. Here, after oral ingestion, we analyzed the infection dynamics of cultivable S. symbiotica during the host’s lifetime using quantitative PCR and fluorescence techniques and determined the immediate fitness consequences of these bacteria on their new host. We further examined the transmission behavior and phylogenetic position of cultivable strains. Our study revealed that cultivable S. symbiotica bacteria are predisposed to establish a symbiotic association with a new aphid host, settling in its gut. We show that cultivable S. symbiotica bacteria colonize the entire aphid digestive tract following infection, after which the bacteria multiply exponentially during aphid development. Our results further reveal that gut colonization by the bacteria induces a fitness cost to their hosts. Nevertheless, it appeared that the bacteria also offer an immediate protection against parasitoids. Interestingly, cultivable S. symbiotica strains seem to be extracellularly transmitted, possibly through the honeydew, while S. symbiotica is generally considered a maternally transmitted bacterium living within the aphid body cavity and bringing some benefits to its hosts, despite its costs. These findings provide new insights into the nature of symbiosis in aphids and the mechanisms underpinning these interactions. IMPORTANCE S. symbiotica is one of the most common symbionts among aphid populations and includes a wide variety of strains whose degree of interdependence on the host may vary considerably. S. symbiotica strains with a free-living capacity have recently been isolated from aphids. By using these strains, we established artificial associations by simulating new bacterial acquisitions involved in aphid gut infections to decipher their infection processes and biological effects on their new hosts. Our results showed the early stages involved in this route of infection. So far, S. symbiotica has been considered a maternally transmitted aphid endosymbiont. Nevertheless, we show that our cultivable S. symbiotica strains occupy and replicate in the aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, cultivable S. symbiotica bacteria are both parasites and mutualists given the context, as are many aphid endosymbionts. Our findings give new perception of the associations involved in bacterial mutualism in aphids.