Trading amino acids at the aphid–Buchnera symbiotic interface

Honglin Feng, Noel Edwards, Catriona M.H. Anderson, Mike Althaus, Rebecca P. Duncan, Yu Ching Hsu, Charles W. Luetje, Daniel R.G. Price, Alexandra Wilson, David T. Thwaites

Research output: Contribution to journalArticle

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 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.

Original languageEnglish (US)
Pages (from-to)16003-16011
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number32
DOIs
StatePublished - Aug 6 2019
Externally publishedYes

Fingerprint

Amino Acids
Membranes
Insects
Buchnera
Amino Acid Transport Systems
Food
Aphids
Essential Amino Acids
Hemolymph
Peas
Eukaryotic Cells
Xenopus
Metabolic Networks and Pathways
Proline
Vitamins
Alanine
Glycine
Serine
Oocytes
Cysteine

Keywords

  • Amino acid transport
  • Metabolic integration
  • Symbiosis

ASJC Scopus subject areas

  • General

Cite this

Feng, H., Edwards, N., Anderson, C. M. H., Althaus, M., Duncan, R. P., Hsu, Y. C., ... Thwaites, D. T. (2019). Trading amino acids at the aphid–Buchnera symbiotic interface. Proceedings of the National Academy of Sciences of the United States of America, 116(32), 16003-16011. https://doi.org/10.1073/pnas.1906223116

Trading amino acids at the aphid–Buchnera symbiotic interface. / Feng, Honglin; Edwards, Noel; Anderson, Catriona M.H.; Althaus, Mike; Duncan, Rebecca P.; Hsu, Yu Ching; Luetje, Charles W.; Price, Daniel R.G.; Wilson, Alexandra; Thwaites, David T.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 32, 06.08.2019, p. 16003-16011.

Research output: Contribution to journalArticle

Feng, H, Edwards, N, Anderson, CMH, Althaus, M, Duncan, RP, Hsu, YC, Luetje, CW, Price, DRG, Wilson, A & Thwaites, DT 2019, 'Trading amino acids at the aphid–Buchnera symbiotic interface', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 32, pp. 16003-16011. https://doi.org/10.1073/pnas.1906223116
Feng, Honglin ; Edwards, Noel ; Anderson, Catriona M.H. ; Althaus, Mike ; Duncan, Rebecca P. ; Hsu, Yu Ching ; Luetje, Charles W. ; Price, Daniel R.G. ; Wilson, Alexandra ; Thwaites, David T. / Trading amino acids at the aphid–Buchnera symbiotic interface. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 32. pp. 16003-16011.
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