ABSTRACT
Many insects depend on obligate mutualistic bacteria for the provisioning of essential nutrients lacking from their food source. Most aphids (Hemiptera: Aphididae), whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera for the supply of essential amino acids and B vitamins. However, in some aphid lineages provision of these nutrients is partitioned between Buchnera and an extra bacterial partner. Little is known about the origin and the evolutionary stability of these di-symbiotic systems. Here, we explore these questions in a group of aphids which harbours both Buchnera and an Erwinia-related symbiont. Using fluorescence in situ hybridisation, we located the Erwinia symbiont in close proximity to Buchnera where it inhabits its own bacteriocytes. Analyses of whole-genome sequences of the endosymbionts of 9 aphid species show that Erwinia genomes are highly reduced, syntenic, and display phylogenetic congruency with Buchnera. Altogether these results depict a scenario for Erwinia that mirrors the evolutionary history of Buchnera: its intracellularisation as an obligate partner is a one time event that has resulted in drastic genome reduction and long-term co-divergence with its host. Additionally, we found that the Erwinia genes that complement Buchnera’s deficiencies, but also a set of genes that carry a new nutritional function, have actually been horizontally acquired from a Sodalis-related bacterium. A subset of these genes have been further transferred to a new Hamiltonella co-obligate symbiont in a specific Cinara lineage. This shows that the establishment and dynamics of multi-partner endosymbioses can be mediated by lateral gene transfers between co-ocurring symbionts.
Footnotes
Expanded the metabolic analyses of the Buchnera-Erwinia pair and the genomic analyses of Hamiltonella symbiont. The introduction and discussion sections have also been reworked.