TY - JOUR
T1 - Trading amino acids at the aphid–Buchnera symbiotic interface
AU - Feng, Honglin
AU - Edwards, Noel
AU - Anderson, Catriona M.H.
AU - Althaus, Mike
AU - Duncan, Rebecca P.
AU - Hsu, Yu Ching
AU - Luetje, Charles W.
AU - Price, Daniel R.G.
AU - Wilson, Alex C.C.
AU - Thwaites, David T.
N1 - Funding Information:
ACKNOWLEDGMENTS. 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.
Funding Information:
. 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.
PY - 2019/8/6
Y1 - 2019/8/6
N2 - 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.
AB - 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.
KW - Amino acid transport
KW - Metabolic integration
KW - Symbiosis
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U2 - 10.1073/pnas.1906223116
DO - 10.1073/pnas.1906223116
M3 - Article
C2 - 31337682
AN - SCOPUS:85070221590
VL - 116
SP - 16003
EP - 16011
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 32
ER -