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Trading amino acids at the aphid-Buchnera symbiotic interface

  • 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 immuno-localized 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.

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Metadaten
Document Type:Article
Language:English
Author:Honglin Feng, Noel Edwards, Catriona M. H. Anderson, Mike Althaus, Rebecca P. Duncan, Yu-Ching Hsu, Charles W. Luetje, Daniel R. G. Price, Alex C. C. Wilson, David T. Thwaites
Parent Title (English):Proceedings of the National Academy of Sciences of the United States of America
Volume:116
Issue:32
Number of pages:9
First Page:16003
Last Page:16011
ISSN:0027-8424
DOI:https://doi.org/10.1073/pnas.1906223116
PMID:https://pubmed.ncbi.nlm.nih.gov/31337682
Publisher:National Academy of Sciences
Date of first publication:2019/07/23
Funding:H.F. was supported by a University of Miami Maytag Fellowship. This work was supported by National Science Foundation Awards 1121847 (to A.C.C.W. and D.R.G.P.) and 1354154 (to A.C.C.W. and C.W.L.). N.E. was supported by a PhD studentship from the Biotechnology and Biological Sciences Research Council
Keyword:amino acid transport; metabolic integration; symbiosis
Departments, institutes and facilities:Institut für funktionale Gen-Analytik (IFGA)
Dewey Decimal Classification (DDC):5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Entry in this database:2023/03/22
Licence (German):License LogoCreative Commons - CC BY - Namensnennung 4.0 International