New Insights into the Nature of Symbiotic Associations in Aphids: Initial Steps Involved in Aphid Gut Infection by Serratia symbiotica Bacteria

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 mechanisms behind these symbiotic associations. The recent discovery of cultivable S. symbiotica strains having the possibility of 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 dynamic of cultivable S. symbiotica strains during the hosts lifetime using qPCR 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. Usually, S. symbiotica are considered as maternally-transmitted bacteria living within aphid body cavity and bringing some benefits to their hosts despite their costs. Otherwise, our study revealed that cultivable S. symbiotica are predisposed to establish a symbiotic association with new aphid host, settling in its gut. We showed that cultivable S. symbiotica colonized the entire aphid digestive tract following infection, after which the bacterium multiplied exponentially during aphid development. Our results further revealed that gut colonization by the bacteria induce a fitness cost to their hosts. Nevertheless, it appeared that they also offer an immediate protection against parasitoids. Interestingly, cultivable S. symbiotica seem to be extracellularly transmitted, possibly through the honeydew. These findings provide new insights into the nature of symbiosis in aphids and the mechanisms underpinning these interactions.\n\nImportanceFor the first time, our study provides experimental data that highlight a new kind of symbiotic associations in aphids. By successfully isolating microbial symbiont from aphids and by cultivating it in vitro in our laboratory, we established artificial association by simulating new bacterial acquisitions involved in aphid gut infection. Our results showed the early stages involved in this route of infection. Until now, Serratia symbiotica is considered as a maternally-transmitted aphid endosymbiont. Nevertheless, here, we showed that our cultivable strains having an intermediate status between a strict free-living bacterium and a facultative endosymbiont, occupy and replicate in aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, they are both parasites and mutualists given the context, as many of the endosymbionts in aphids. Our findings give new perception of associations involved in aphids symbiosis.