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.
Highlights
Animals and plants live in symbiosis with a complex microbiota
To enable optimal utilization of diet, sap-feeding Hemipterans exist in a state of endosymbiosis with microbial symbionts [4, 7, 12]
A paradigm has evolved where the insect is considered to supply the symbiont with nonessential amino acids (NEAAs) and, in return, the symbiont provides the insect with essential amino acids (EAAs), or critical biosynthetic pathway components (Fig. 1B)
Summary
Animals and plants live in symbiosis with a complex microbiota. Such symbioses are ubiquitous and impact the biology of all multicellular organisms [1,2,3]. Phloem sap is a poor source of EAAs. Plant sap-feeding insects thrive despite feeding exclusively on a diet lacking in essential amino acids. Plant sap-feeding insects thrive despite feeding exclusively on a diet lacking in essential amino acids This nutritional deficit is countered through endosymbiotic relationships with microbial symbionts. Nonessential amino acids, vital for microbial symbionts, are utilized by symbiont metabolic pathways and yield essential amino acids required by their eukaryotic hosts. We identify a transport system that mediates a crucial step in this metabolic complementarity: a transporter capable of transporting nonessential amino acids across the symbiosomal membrane of the pea aphid Acyrthosiphon pisum. The relationship is complex and integrated with key biosynthetic steps in single pathways being encoded by a combination of endosymbiont and host genomes [13,14,15,16, 20,21,22,23,24,25,26,27] (Fig. 1C)
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