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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Main Authors: Inès Pons, François Renoz, Christine Noël, Thierry Hance
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.00764/full
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author Inès Pons
François Renoz
Christine Noël
Thierry Hance
author_facet Inès Pons
François Renoz
Christine Noël
Thierry Hance
author_sort Inès Pons
collection DOAJ
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 doaj.art-08e5c374e3984dda9f5983a53f6c02b92022-12-22T03:37:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-04-011010.3389/fmicb.2019.00764447431Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by PlantsInès PonsFrançois RenozChristine NoëlThierry HanceSymbiosis 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.00764/fullhorizontal transfersenvironmental acquisitionplant-mediated transmissioninsect-microbe associationstrophic networks
spellingShingle Inès Pons
François Renoz
Christine Noël
Thierry Hance
Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants
Frontiers in Microbiology
horizontal transfers
environmental acquisition
plant-mediated transmission
insect-microbe associations
trophic networks
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 horizontal transfers
environmental acquisition
plant-mediated transmission
insect-microbe associations
trophic networks
url https://www.frontiersin.org/article/10.3389/fmicb.2019.00764/full
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AT francoisrenoz circulationofthecultivablesymbiontserratiasymbioticainaphidsismediatedbyplants
AT christinenoel circulationofthecultivablesymbiontserratiasymbioticainaphidsismediatedbyplants
AT thierryhance circulationofthecultivablesymbiontserratiasymbioticainaphidsismediatedbyplants