Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome

Abstract Background Host/symbiont integration is a signature of evolutionarily ancient, obligate endosymbioses. However, little is known about the cellular and developmental mechanisms of host/symbiont integration at the molecular level. Many insects possess obligate bacterial endosymbionts that pro...

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Main Authors: Celeste R. Banfill, Alex C. C. Wilson, Hsiao-ling Lu
Format: Article
Language:English
Published: BMC 2020-11-01
Series:EvoDevo
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13227-020-00168-5
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spelling doaj-b1f51396f0824b9a97bf80dac848dd672020-11-25T04:08:24ZengBMCEvoDevo2041-91392020-11-0111111410.1186/s13227-020-00168-5Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriomeCeleste R. Banfill0Alex C. C. Wilson1Hsiao-ling Lu2Department of Biology, University of MiamiDepartment of Biology, University of MiamiDepartment of Biotechnology, National Formosa UniversityAbstract Background Host/symbiont integration is a signature of evolutionarily ancient, obligate endosymbioses. However, little is known about the cellular and developmental mechanisms of host/symbiont integration at the molecular level. Many insects possess obligate bacterial endosymbionts that provide essential nutrients. To advance understanding of the developmental and metabolic integration of hosts and endosymbionts, we track the localization of a non-essential amino acid transporter, ApNEAAT1, across asexual embryogenesis in the aphid, Acyrthosiphon pisum. Previous work in adult bacteriomes revealed that ApNEAAT1 functions to exchange non-essential amino acids at the A. pisum/Buchnera aphidicola symbiotic interface. Driven by amino acid concentration gradients, ApNEAAT1 moves proline, serine, and alanine from A. pisum to Buchnera and cysteine from Buchnera to A. pisum. Here, we test the hypothesis that ApNEAAT1 is localized to the symbiotic interface during asexual embryogenesis. Results During A. pisum asexual embryogenesis, ApNEAAT1 does not localize to the symbiotic interface. We observed ApNEAAT1 localization to the maternal follicular epithelium, the germline, and, in late-stage embryos, to anterior neural structures and insect immune cells (hemocytes). We predict that ApNEAAT1 provisions non-essential amino acids to developing oocytes and embryos, as well as to the brain and related neural structures. Additionally, ApNEAAT1 may perform roles related to host immunity. Conclusions Our work provides further evidence that the embryonic and adult bacteriomes of asexual A. pisum are not equivalent. Future research is needed to elucidate the developmental time point at which the bacteriome reaches maturity.http://link.springer.com/article/10.1186/s13227-020-00168-5Host/symbiont developmental integrationEndosymbiosisBacteriomeAmino acid transporterCoevolution
collection DOAJ
language English
format Article
sources DOAJ
author Celeste R. Banfill
Alex C. C. Wilson
Hsiao-ling Lu
spellingShingle Celeste R. Banfill
Alex C. C. Wilson
Hsiao-ling Lu
Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome
EvoDevo
Host/symbiont developmental integration
Endosymbiosis
Bacteriome
Amino acid transporter
Coevolution
author_facet Celeste R. Banfill
Alex C. C. Wilson
Hsiao-ling Lu
author_sort Celeste R. Banfill
title Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome
title_short Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome
title_full Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome
title_fullStr Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome
title_full_unstemmed Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome
title_sort further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic acyrthosiphon pisum bacteriome
publisher BMC
series EvoDevo
issn 2041-9139
publishDate 2020-11-01
description Abstract Background Host/symbiont integration is a signature of evolutionarily ancient, obligate endosymbioses. However, little is known about the cellular and developmental mechanisms of host/symbiont integration at the molecular level. Many insects possess obligate bacterial endosymbionts that provide essential nutrients. To advance understanding of the developmental and metabolic integration of hosts and endosymbionts, we track the localization of a non-essential amino acid transporter, ApNEAAT1, across asexual embryogenesis in the aphid, Acyrthosiphon pisum. Previous work in adult bacteriomes revealed that ApNEAAT1 functions to exchange non-essential amino acids at the A. pisum/Buchnera aphidicola symbiotic interface. Driven by amino acid concentration gradients, ApNEAAT1 moves proline, serine, and alanine from A. pisum to Buchnera and cysteine from Buchnera to A. pisum. Here, we test the hypothesis that ApNEAAT1 is localized to the symbiotic interface during asexual embryogenesis. Results During A. pisum asexual embryogenesis, ApNEAAT1 does not localize to the symbiotic interface. We observed ApNEAAT1 localization to the maternal follicular epithelium, the germline, and, in late-stage embryos, to anterior neural structures and insect immune cells (hemocytes). We predict that ApNEAAT1 provisions non-essential amino acids to developing oocytes and embryos, as well as to the brain and related neural structures. Additionally, ApNEAAT1 may perform roles related to host immunity. Conclusions Our work provides further evidence that the embryonic and adult bacteriomes of asexual A. pisum are not equivalent. Future research is needed to elucidate the developmental time point at which the bacteriome reaches maturity.
topic Host/symbiont developmental integration
Endosymbiosis
Bacteriome
Amino acid transporter
Coevolution
url http://link.springer.com/article/10.1186/s13227-020-00168-5
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