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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 special...

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Autores principales: Feng, Honglin, Edwards, Noel, Anderson, Catriona M. H., Althaus, Mike, Duncan, Rebecca P., Hsu, Yu-Ching, Luetje, Charles W., Price, Daniel R. G., Wilson, Alex C. C., Thwaites, David T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6690024/
https://www.ncbi.nlm.nih.gov/pubmed/31337682
http://dx.doi.org/10.1073/pnas.1906223116
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author Feng, Honglin
Edwards, Noel
Anderson, Catriona M. H.
Althaus, Mike
Duncan, Rebecca P.
Hsu, Yu-Ching
Luetje, Charles W.
Price, Daniel R. G.
Wilson, Alex C. C.
Thwaites, David T.
author_facet Feng, Honglin
Edwards, Noel
Anderson, Catriona M. H.
Althaus, Mike
Duncan, Rebecca P.
Hsu, Yu-Ching
Luetje, Charles W.
Price, Daniel R. G.
Wilson, Alex C. C.
Thwaites, David T.
author_sort Feng, Honglin
collection PubMed
description 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.
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spelling pubmed-66900242019-08-14 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, Alex C. C. Thwaites, David T. Proc Natl Acad Sci U S A PNAS Plus 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. National Academy of Sciences 2019-08-06 2019-07-23 /pmc/articles/PMC6690024/ /pubmed/31337682 http://dx.doi.org/10.1073/pnas.1906223116 Text en Copyright © 2019 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle PNAS Plus
Feng, Honglin
Edwards, Noel
Anderson, Catriona M. H.
Althaus, Mike
Duncan, Rebecca P.
Hsu, Yu-Ching
Luetje, Charles W.
Price, Daniel R. G.
Wilson, Alex C. C.
Thwaites, David T.
Trading amino acids at the aphid–Buchnera symbiotic interface
title Trading amino acids at the aphid–Buchnera symbiotic interface
title_full Trading amino acids at the aphid–Buchnera symbiotic interface
title_fullStr Trading amino acids at the aphid–Buchnera symbiotic interface
title_full_unstemmed Trading amino acids at the aphid–Buchnera symbiotic interface
title_short Trading amino acids at the aphid–Buchnera symbiotic interface
title_sort trading amino acids at the aphid–buchnera symbiotic interface
topic PNAS Plus
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6690024/
https://www.ncbi.nlm.nih.gov/pubmed/31337682
http://dx.doi.org/10.1073/pnas.1906223116
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