The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> 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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| Format: | Article |
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MDPI AG
2022-07-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/10/7/1360 |
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| author | François Renoz Jérôme Ambroise Bertrand Bearzatto Samir Fakhour Nicolas Parisot Mélanie Ribeiro Lopes Jean-Luc Gala Federica Calevro Thierry Hance |
| author_facet | François Renoz Jérôme Ambroise Bertrand Bearzatto Samir Fakhour Nicolas Parisot Mélanie Ribeiro Lopes Jean-Luc Gala Federica Calevro Thierry Hance |
| author_sort | François Renoz |
| collection | DOAJ |
| 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 <i>Buchnera aphidicola</i> 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 <i>B. aphidicola</i> and <i>Serratia symbiotica</i> associated with the Chaitophorinae aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i>. Our results show that, in these two species, <i>B. aphidicola</i> and <i>S. symbiotica</i> 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 <i>S. symbiotica</i> symbiont associated with <i>S. maydis</i> appears to be strictly compartmentalized into the specialized host cells housing symbionts in aphids, the bacteriocytes, whereas the <i>S. symbiotica</i> symbiont associated with <i>P. lyropictus</i> 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 <i>S. symbiotica</i> symbionts that were recently acquired as nutritional co-obligate partners reflect distinct coevolutionary processes specific to each association. |
| first_indexed | 2024-03-09T13:20:31Z |
| format | Article |
| id | doaj.art-8237040c1a904d299c251d33d8095b4a |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T13:20:31Z |
| publishDate | 2022-07-01 |
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| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-8237040c1a904d299c251d33d8095b4a2023-11-30T21:30:29ZengMDPI AGMicroorganisms2076-26072022-07-01107136010.3390/microorganisms10071360The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in AphidsFrançois Renoz0Jérôme Ambroise1Bertrand Bearzatto2Samir Fakhour3Nicolas Parisot4Mélanie Ribeiro Lopes5Jean-Luc Gala6Federica Calevro7Thierry Hance8Biodiversity Research Centre, Earth and Life Institute, Université Catholique de Louvain (UCLouvain), 1348 Louvain-la-Neuve, BelgiumCenter for Applied Molecular Technologies, Institute of Experimental and Clinical Research, Université Catholique de Louvain (UCLouvain), 1200 Woluwe-Saint-Lambert, BelgiumCenter for Applied Molecular Technologies, Institute of Experimental and Clinical Research, Université Catholique de Louvain (UCLouvain), 1200 Woluwe-Saint-Lambert, BelgiumDepartment of Plant Protection, National Institute of Agricultural Research, Avenue Ennasr, BP 415 Rabat Principale, Rabat 10090, MoroccoUniv Lyon, INSA Lyon, INRAE, BF2I, UMR203, F-69621 Villeurbanne, FranceUniv Lyon, INSA Lyon, INRAE, BF2I, UMR203, F-69621 Villeurbanne, FranceCenter for Applied Molecular Technologies, Institute of Experimental and Clinical Research, Université Catholique de Louvain (UCLouvain), 1200 Woluwe-Saint-Lambert, BelgiumUniv Lyon, INSA Lyon, INRAE, BF2I, UMR203, F-69621 Villeurbanne, FranceBiodiversity Research Centre, Earth and Life Institute, Université Catholique de Louvain (UCLouvain), 1348 Louvain-la-Neuve, BelgiumDependence 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 <i>Buchnera aphidicola</i> 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 <i>B. aphidicola</i> and <i>Serratia symbiotica</i> associated with the Chaitophorinae aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i>. Our results show that, in these two species, <i>B. aphidicola</i> and <i>S. symbiotica</i> 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 <i>S. symbiotica</i> symbiont associated with <i>S. maydis</i> appears to be strictly compartmentalized into the specialized host cells housing symbionts in aphids, the bacteriocytes, whereas the <i>S. symbiotica</i> symbiont associated with <i>P. lyropictus</i> 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 <i>S. symbiotica</i> symbionts that were recently acquired as nutritional co-obligate partners reflect distinct coevolutionary processes specific to each association.https://www.mdpi.com/2076-2607/10/7/1360aphidsbacterial symbiont<i>Buchnera aphidicola</i>co-obligate <i>Serratia symbiotica</i>nutritional mutualismvirulence factors |
| spellingShingle | François Renoz Jérôme Ambroise Bertrand Bearzatto Samir Fakhour Nicolas Parisot Mélanie Ribeiro Lopes Jean-Luc Gala Federica Calevro Thierry Hance The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids Microorganisms aphids bacterial symbiont <i>Buchnera aphidicola</i> co-obligate <i>Serratia symbiotica</i> nutritional mutualism virulence factors |
| title | The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids |
| title_full | The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids |
| title_fullStr | The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids |
| title_full_unstemmed | The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids |
| title_short | The Di-Symbiotic Systems in the Aphids <i>Sipha maydis</i> and <i>Periphyllus lyropictus</i> Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids |
| title_sort | di symbiotic systems in the aphids i sipha maydis i and i periphyllus lyropictus i provide a contrasting picture of recent co obligate nutritional endosymbiosis in aphids |
| topic | aphids bacterial symbiont <i>Buchnera aphidicola</i> co-obligate <i>Serratia symbiotica</i> nutritional mutualism virulence factors |
| url | https://www.mdpi.com/2076-2607/10/7/1360 |
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