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Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants

Symbiosis is a common phenomenon in nature that substantially affects organismal ecology and evolution. Fundamental questions regarding how mutualistic associations arise and evolve in nature remain, however, poorly studied. The aphid-Serratia symbiotica bacterium interaction represents a valuable m...

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Autores principales: Pons, Inès, Renoz, François, Noël, Christine, Hance, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6476230/
https://www.ncbi.nlm.nih.gov/pubmed/31037067
http://dx.doi.org/10.3389/fmicb.2019.00764
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author Pons, Inès
Renoz, François
Noël, Christine
Hance, Thierry
author_facet Pons, Inès
Renoz, François
Noël, Christine
Hance, Thierry
author_sort Pons, Inès
collection PubMed
description Symbiosis is a common phenomenon in nature that substantially affects organismal ecology and evolution. Fundamental questions regarding how mutualistic associations arise and evolve in nature remain, however, poorly studied. The aphid-Serratia symbiotica bacterium interaction represents a valuable model to study mechanisms shaping these symbiotic interspecific interactions. S. symbiotica strains capable of living independently of aphid hosts have recently been isolated. These strains probably resulted from horizontal transfers and could be an evolutionary link to an intra-organismal symbiosis. In this context, we used the tripartite interaction between the aphid Aphis fabae, a cultivable S. symbiotica bacterium, and the host plant Vicia faba to evaluate the bacterium ability to circulate in this system, exploring its environmental acquisition by aphids and horizontal transmission between aphids via the host plant. Using molecular analyses and fluorescence techniques, we showed that the cultivable S. symbiotica can enter the plants and induce new bacterial infections in aphids feeding on these new infected plants. Remarkably, we also found that the bacterium can have positive effects on the host plant, mainly at the root level. Furthermore, our results demonstrated that cultivable S. symbiotica can be horizontally transferred from infected to uninfected aphids sharing the same plant, providing first direct evidence that plants can mediate horizontal transmission of certain strains of this symbiont species. These findings highlight the importance of considering symbiotic associations in complex systems where microorganisms can circulate between different compartments. Our study can thus have major implications for understanding the multifaceted interactions between microbes, insects and plants.
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spelling pubmed-64762302019-04-29 Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants Pons, Inès Renoz, François Noël, Christine Hance, Thierry Front Microbiol Microbiology Symbiosis is a common phenomenon in nature that substantially affects organismal ecology and evolution. Fundamental questions regarding how mutualistic associations arise and evolve in nature remain, however, poorly studied. The aphid-Serratia symbiotica bacterium interaction represents a valuable model to study mechanisms shaping these symbiotic interspecific interactions. S. symbiotica strains capable of living independently of aphid hosts have recently been isolated. These strains probably resulted from horizontal transfers and could be an evolutionary link to an intra-organismal symbiosis. In this context, we used the tripartite interaction between the aphid Aphis fabae, a cultivable S. symbiotica bacterium, and the host plant Vicia faba to evaluate the bacterium ability to circulate in this system, exploring its environmental acquisition by aphids and horizontal transmission between aphids via the host plant. Using molecular analyses and fluorescence techniques, we showed that the cultivable S. symbiotica can enter the plants and induce new bacterial infections in aphids feeding on these new infected plants. Remarkably, we also found that the bacterium can have positive effects on the host plant, mainly at the root level. Furthermore, our results demonstrated that cultivable S. symbiotica can be horizontally transferred from infected to uninfected aphids sharing the same plant, providing first direct evidence that plants can mediate horizontal transmission of certain strains of this symbiont species. These findings highlight the importance of considering symbiotic associations in complex systems where microorganisms can circulate between different compartments. Our study can thus have major implications for understanding the multifaceted interactions between microbes, insects and plants. Frontiers Media S.A. 2019-04-15 /pmc/articles/PMC6476230/ /pubmed/31037067 http://dx.doi.org/10.3389/fmicb.2019.00764 Text en Copyright © 2019 Pons, Renoz, Noël and Hance. http://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 Microbiology
Pons, Inès
Renoz, François
Noël, Christine
Hance, Thierry
Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants
title Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants
title_full Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants
title_fullStr Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants
title_full_unstemmed Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants
title_short Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants
title_sort circulation of the cultivable symbiont serratia symbiotica in aphids is mediated by plants
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6476230/
https://www.ncbi.nlm.nih.gov/pubmed/31037067
http://dx.doi.org/10.3389/fmicb.2019.00764
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