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The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids

Dependence on multiple nutritional bacterial symbionts forming a metabolic unit has repeatedly evolved in many insect species that feed on nutritionally unbalanced diets such as plant sap. This is the case for aphids of the subfamilies Lachninae and Chaitophorinae, which have evolved di-symbiotic sy...

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Autores principales: Renoz, François, Ambroise, Jérôme, Bearzatto, Bertrand, Fakhour, Samir, Parisot, Nicolas, Ribeiro Lopes, Mélanie, Gala, Jean-Luc, Calevro, Federica, Hance, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9317480/
https://www.ncbi.nlm.nih.gov/pubmed/35889078
http://dx.doi.org/10.3390/microorganisms10071360
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author Renoz, François
Ambroise, Jérôme
Bearzatto, Bertrand
Fakhour, Samir
Parisot, Nicolas
Ribeiro Lopes, Mélanie
Gala, Jean-Luc
Calevro, Federica
Hance, Thierry
author_facet Renoz, François
Ambroise, Jérôme
Bearzatto, Bertrand
Fakhour, Samir
Parisot, Nicolas
Ribeiro Lopes, Mélanie
Gala, Jean-Luc
Calevro, Federica
Hance, Thierry
author_sort Renoz, François
collection PubMed
description Dependence on multiple nutritional bacterial symbionts forming a metabolic unit has repeatedly evolved in many insect species that feed on nutritionally unbalanced diets such as plant sap. This is the case for aphids of the subfamilies Lachninae and Chaitophorinae, which have evolved di-symbiotic systems in which the ancient obligate nutritional symbiont Buchnera aphidicola is metabolically complemented by an additional nutritional symbiont acquired more recently. Deciphering how different symbionts integrate both metabolically and anatomically in such systems is crucial to understanding how complex nutritional symbiotic systems function and evolve. In this study, we sequenced and analyzed the genomes of the symbionts B. aphidicola and Serratia symbiotica associated with the Chaitophorinae aphids Sipha maydis and Periphyllus lyropictus. Our results show that, in these two species, B. aphidicola and S. symbiotica complement each other metabolically (and their hosts) for the biosynthesis of essential amino acids and vitamins, but with distinct metabolic reactions supported by each symbiont depending on the host species. Furthermore, the S. symbiotica symbiont associated with S. maydis appears to be strictly compartmentalized into the specialized host cells housing symbionts in aphids, the bacteriocytes, whereas the S. symbiotica symbiont associated with P. lyropictus exhibits a highly invasive phenotype, presumably because it is capable of expressing a larger set of virulence factors, including a complete flagellum for bacterial motility. Such contrasting levels of metabolic and anatomical integration for two S. symbiotica symbionts that were recently acquired as nutritional co-obligate partners reflect distinct coevolutionary processes specific to each association.
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spelling pubmed-93174802022-07-27 The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids Renoz, François Ambroise, Jérôme Bearzatto, Bertrand Fakhour, Samir Parisot, Nicolas Ribeiro Lopes, Mélanie Gala, Jean-Luc Calevro, Federica Hance, Thierry Microorganisms Article Dependence on multiple nutritional bacterial symbionts forming a metabolic unit has repeatedly evolved in many insect species that feed on nutritionally unbalanced diets such as plant sap. This is the case for aphids of the subfamilies Lachninae and Chaitophorinae, which have evolved di-symbiotic systems in which the ancient obligate nutritional symbiont Buchnera aphidicola is metabolically complemented by an additional nutritional symbiont acquired more recently. Deciphering how different symbionts integrate both metabolically and anatomically in such systems is crucial to understanding how complex nutritional symbiotic systems function and evolve. In this study, we sequenced and analyzed the genomes of the symbionts B. aphidicola and Serratia symbiotica associated with the Chaitophorinae aphids Sipha maydis and Periphyllus lyropictus. Our results show that, in these two species, B. aphidicola and S. symbiotica complement each other metabolically (and their hosts) for the biosynthesis of essential amino acids and vitamins, but with distinct metabolic reactions supported by each symbiont depending on the host species. Furthermore, the S. symbiotica symbiont associated with S. maydis appears to be strictly compartmentalized into the specialized host cells housing symbionts in aphids, the bacteriocytes, whereas the S. symbiotica symbiont associated with P. lyropictus exhibits a highly invasive phenotype, presumably because it is capable of expressing a larger set of virulence factors, including a complete flagellum for bacterial motility. Such contrasting levels of metabolic and anatomical integration for two S. symbiotica symbionts that were recently acquired as nutritional co-obligate partners reflect distinct coevolutionary processes specific to each association. MDPI 2022-07-06 /pmc/articles/PMC9317480/ /pubmed/35889078 http://dx.doi.org/10.3390/microorganisms10071360 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Renoz, François
Ambroise, Jérôme
Bearzatto, Bertrand
Fakhour, Samir
Parisot, Nicolas
Ribeiro Lopes, Mélanie
Gala, Jean-Luc
Calevro, Federica
Hance, Thierry
The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids
title The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids
title_full The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids
title_fullStr The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids
title_full_unstemmed The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids
title_short The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids
title_sort di-symbiotic systems in the aphids sipha maydis and periphyllus lyropictus provide a contrasting picture of recent co-obligate nutritional endosymbiosis in aphids
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9317480/
https://www.ncbi.nlm.nih.gov/pubmed/35889078
http://dx.doi.org/10.3390/microorganisms10071360
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