Trading amino acids at the aphid– Buchnera symbiotic interface

Abstract

Plant sap-feeding insects are widespread, having evolved to occupy diverse environmental niches despite exclusive feeding on an impoverished diet lacking in essential amino acids and vitamins. Success depends exquisitely on their symbiotic relationships with microbial symbionts housed within specialized eukaryotic bacteriocyte cells. Each bacteriocyte is packed with symbionts that are individually surrounded by a host-derived symbiosomal membrane representing the absolute host–symbiont interface. The symbiosomal membrane must be a dynamic and selectively permeable structure to enable bidirectional and differential movement of essential nutrients, metabolites, and biosynthetic intermediates, vital for growth and survival of host and symbiont. However, despite this crucial role, the molecular basis of membrane transport across the symbiosomal membrane remains unresolved in all bacteriocyte-containing insects. A transport protein was immunolocalized to the symbiosomal membrane separating the pea aphid Acyrthosiphon pisum from its intracellular symbiont Buchnera aphidicola. The transporter, A. pisum nonessential amino acid transporter 1, or ApNEAAT1 (gene: ACYPI008971), was characterized functionally following heterologous expression in Xenopus oocytes, and mediates both inward and outward transport of small dipolar amino acids (serine, proline, cysteine, alanine, glycine). Electroneutral ApNEAAT1 transport is driven by amino acid concentration gradients and is not coupled to transmembrane ion gradients. Previous metabolite profiling of hemolymph and bacteriocyte, alongside metabolic pathway analysis in host and symbiont, enable prediction of a physiological role for ApNEAAT1 in bidirectional host–symbiont amino acid transfer, supplying both host and symbiont with indispensable nutrients and biosynthetic precursors to facilitate metabolic complementarity.

RETRACTED: Amino acid synthesis loss in parasitoid wasps and other hymenopterans

“…For example, bees feed on amino acid rich pollen and ants have a wide range of food sources ( Rabie et al, 1983 ; Nicolson and Human, 2013 ). Another possibility is that symbiotic bacteria can provide essential nutrients to host insects, as reported in Cephalotes ants by Hu et al, 2018 and as well known in other insects such as aphids ( Wilson et al, 2010 ; Feng et al, 2019 ).…”

Dynamics of Insect–Microbiome Interaction Influence Host and Microbial Symbiont

“…They supplement the nutritional requirement of their host by synthesizing essential amino acids and rare vitamins especially for the hemimetabolous sap-sucking insects that feed on nutrient-poor diets. For instance, in Buchnera aphidicola, an obligate symbiont of aphids, and probably the most studied model, it has been shown that the bacteria fulfills the nutritional requirement of the insect host to an extent that its removal dramatically affects aphid survival and fecundity (Feng et al, 2019). Similarly, symbiosis between the sap-feeding insect Megacopta cribraria and its primary bacterial symbiont, Candidatus Ishikawaella capsulate, is essential for host survival to adulthood (Couret et al, 2019).…”

Trends in symbiont-induced host cellular differentiation

“…However, there may be striking differences between patterns of symbiont-induced host post-transcriptional modifications between mutualists and pathogens. For example, in regards to ubiquitination, amino acid economies are vastly different between pathogenic infections that usurp them from the host (Zhang and Rubin 2013) and mutualistic infections that synthesize them for the host (Feng et al 2019). Thus, if mutualists are capable of altering host ubiquitination, they may be more likely to use it to control host signalling cascades than to obtain amino acids.…”