An obligatory symbiosis with Buchnera aphidicola

Many insects live in symbiosis with micro-organisms that allow them to better exploit the resources of their habitats or to better protect themselves from environmental stresses. Aphids have established symbiotic relationships with the bacterium Buchnera aphidicola for more than 150 million years, which provides them with essential amino acids and vitamins absent or in small quantities in the sap of the plants from which they feed. Without this obligatory symbiont, aphids cannot survive and vice versa for Buchnera, which creates an interdependence between the two organisms.

A consortium of facultative or secondary symbionts

However, Buchnera is not the only microbial symbiont harbored by aphids and since the early 2000s, discoveries of new partners and their effects on their hosts have followed one another. These symbionts, mostly bacterial, are generally found at intermediate frequencies in populations: not all individuals are infected unlike the symbiosis with Buchnera and we therefore speak of facultative or secondary symbionts. In certain aphid species such as the Lachninae, tripartite symbionts may have evolved where Buchnera and another symbiotic bacterium complement each other to provide the aphid with the nutrients essential for its development and reproduction

Localization of symbionts in specialized organs

Most of the symbiotic bacteria reside in specialized organs of the host, called bacteriocytes, located on either side of the digestive tract. An adult female of the pea aphid Acyrthosiphon pisum thus comprises approximately 90 bacteriocytes harboring in total more than 10 million Buchnera cells. The facultative symbionts can reside in different internal organs of the host: they can for example co-exist in the same bacteriocytes as Buchnera or reside in secondary bacteriocytes, in cells on the periphery of the bacteriocytes and in the hemolymph.

Mother-to-daughter transmission with occasional horizontal transfers

The symbionts are mainly transmitted vertically: Buchnera and other facultative symbionts are transferred at a very early stage in the embryonic development of aphids. The embryos therefore receive the symbionts from their mother in utero. The vertical transmission of Buchnera is reflected in phylogenetic analyzes which reveal a perfect co-diversification of the two partners since the establishment of this symbiosis. This is not always the case with facultative symbionts, which show occasional horizontal transfer events between unrelated hosts. The horizontal transfer routes are unknown but could involve contacts between congeners, attacks by natural enemies or acquisition via host plants.

A wide range of effects of symbionts on their hosts

While Buchnera's role for aphids is well known and strictly nutritional in nature, that of optional symbionts is very varied and not always well understood. The facultative symbionts can thus influence the response to biotic or abiotic stresses, reproduction, development, immunity, behavior and even color. The pea aphid is certainly the species for which the effects of symbionts have been best studied. It has thus been shown that the bacterium Hamiltonella defensa could protect aphids against attacks by parasitoid wasps, that Regiella insecticola made its hosts more resistant to pathogenic fungi, that Rickettsiella viridis modified aphid body color, that Spiroplasma selectively eliminated the male embryos in the offspring, that Serratia symbiotica conferred better tolerance to heat. However, these beneficial effects are very often accompanied by physiological or ecological costs, which translate into reduced fecundity or behavioral defenses for aphids carrying facultative symbionts.

Aphid symbioses: a very dynamic field of research

Many research teams are currently working on aphid symbioses. They study in particular the molecular interactions between aphids and their symbionts to better understand the effects of the latter on their hosts and how the aphids regulate their populations of symbionts. They are also interested in the dynamics of symbiotic associations to identify the factors involved in the acquisition, evolution, loss of symbionts in aphid lineages. Finally, they explore the influence of symbionts in ecological networks, notably by questioning the consequences of protective symbiosis on communities of natural enemies.

Section of an embryo of the aphid Acyrthosiphon pisum with labeling of bacteriocytes containing Buchnera aphidicola (in green). Photographer: Karen Gaget and Federica Calevro.

Microscopic image obtained by fluorescence in situ hybridization (FISH) showing the location and morphology of the symbionts of the aphid Tuberolachnus salignus (Buchnera aphidicola in green and Serratia symbiotica in red). Photographer: Alejandro Manzano-Marin.