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Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development

An important contributing factor to the evolutionary success of insects is nutritional association with microbial symbionts, which provide the host insects with nutrients lacking in their unbalanced diets. These symbionts are often compartmentalized in specialized cells of the host, the bacteriocyte...

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Autores principales: Ribeiro Lopes, Mélanie, Gaget, Karen, Renoz, François, Duport, Gabrielle, Balmand, Séverine, Charles, Hubert, Callaerts, Patrick, Calevro, Federica
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9685537/
https://www.ncbi.nlm.nih.gov/pubmed/36439244
http://dx.doi.org/10.3389/fphys.2022.982920
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author Ribeiro Lopes, Mélanie
Gaget, Karen
Renoz, François
Duport, Gabrielle
Balmand, Séverine
Charles, Hubert
Callaerts, Patrick
Calevro, Federica
author_facet Ribeiro Lopes, Mélanie
Gaget, Karen
Renoz, François
Duport, Gabrielle
Balmand, Séverine
Charles, Hubert
Callaerts, Patrick
Calevro, Federica
author_sort Ribeiro Lopes, Mélanie
collection PubMed
description An important contributing factor to the evolutionary success of insects is nutritional association with microbial symbionts, which provide the host insects with nutrients lacking in their unbalanced diets. These symbionts are often compartmentalized in specialized cells of the host, the bacteriocytes. Even though bacteriocytes were first described more than a century ago, few studies have explored their dynamics throughout the insect life cycle and in response to environmental stressors. Here, we use the Buchnera aphidicola/pea aphid symbiotic system to study how bacteriocytes are regulated in response to nutritional stress throughout aphid development. Using artificial diets, we analyzed the effects of depletion or excess of phenylalanine or leucine, two amino acids essential for aphid growth and whose biosynthetic pathways are shared between the host and the symbiont. Bacteriocytes responded dynamically to those treatments, while other tissues showed no obvious morphological change. Amino acid depletion resulted in an increase in bacteriocyte numbers, with the extent of the increase depending on the amino acid, while excess either caused a decrease (for leucine) or an increase (for phenylalanine). Only a limited impact on survival and fecundity was observed, suggesting that the adjustment in bacteriocyte (and symbiont) numbers is sufficient to withstand these nutritional challenges. We also studied the impact of more extreme conditions by exposing aphids to a 24 h starvation period at the beginning of nymphal development. This led to a dramatic drop in aphid survival and fecundity and a significant developmental delay. Again, bacteriocytes responded dynamically, with a considerable decrease in number and size, correlated with a decrease in the number of symbionts, which were prematurely degraded by the lysosomal system. This study shows how bacteriocyte dynamics is integrated in the physiology of insects and highlights the high plasticity of these cells.
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spelling pubmed-96855372022-11-25 Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development Ribeiro Lopes, Mélanie Gaget, Karen Renoz, François Duport, Gabrielle Balmand, Séverine Charles, Hubert Callaerts, Patrick Calevro, Federica Front Physiol Physiology An important contributing factor to the evolutionary success of insects is nutritional association with microbial symbionts, which provide the host insects with nutrients lacking in their unbalanced diets. These symbionts are often compartmentalized in specialized cells of the host, the bacteriocytes. Even though bacteriocytes were first described more than a century ago, few studies have explored their dynamics throughout the insect life cycle and in response to environmental stressors. Here, we use the Buchnera aphidicola/pea aphid symbiotic system to study how bacteriocytes are regulated in response to nutritional stress throughout aphid development. Using artificial diets, we analyzed the effects of depletion or excess of phenylalanine or leucine, two amino acids essential for aphid growth and whose biosynthetic pathways are shared between the host and the symbiont. Bacteriocytes responded dynamically to those treatments, while other tissues showed no obvious morphological change. Amino acid depletion resulted in an increase in bacteriocyte numbers, with the extent of the increase depending on the amino acid, while excess either caused a decrease (for leucine) or an increase (for phenylalanine). Only a limited impact on survival and fecundity was observed, suggesting that the adjustment in bacteriocyte (and symbiont) numbers is sufficient to withstand these nutritional challenges. We also studied the impact of more extreme conditions by exposing aphids to a 24 h starvation period at the beginning of nymphal development. This led to a dramatic drop in aphid survival and fecundity and a significant developmental delay. Again, bacteriocytes responded dynamically, with a considerable decrease in number and size, correlated with a decrease in the number of symbionts, which were prematurely degraded by the lysosomal system. This study shows how bacteriocyte dynamics is integrated in the physiology of insects and highlights the high plasticity of these cells. Frontiers Media S.A. 2022-11-10 /pmc/articles/PMC9685537/ /pubmed/36439244 http://dx.doi.org/10.3389/fphys.2022.982920 Text en Copyright © 2022 Ribeiro Lopes, Gaget, Renoz, Duport, Balmand, Charles, Callaerts and Calevro. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Ribeiro Lopes, Mélanie
Gaget, Karen
Renoz, François
Duport, Gabrielle
Balmand, Séverine
Charles, Hubert
Callaerts, Patrick
Calevro, Federica
Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development
title Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development
title_full Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development
title_fullStr Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development
title_full_unstemmed Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development
title_short Bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development
title_sort bacteriocyte plasticity in pea aphids facing amino acid stress or starvation during development
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9685537/
https://www.ncbi.nlm.nih.gov/pubmed/36439244
http://dx.doi.org/10.3389/fphys.2022.982920
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