New insights into the nature of symbiotic associations in aphids: Infection process, biological effects, and transmission mode of cultivable 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 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.