At the Gate of Mutualism: Identification of Genomic Traits Predisposing to Insect-Bacterial Symbiosis in Pathogenic Strains of the Aphid Symbiont Serratia symbiotica

Renoz, F.; Foray, V.; Ambroise, J.; Baa-Puyoulet, P.; Bearzatto, B.; Mendez, G. L.; Grigorescu, Alina; Mahillon, J.; Mardulyn, P.; Gala, J.-L.; Calevro, F.; Hance, T.

doi:10.3389/fcimb.2021.660007

Article (Scientific journals)

At the Gate of Mutualism: Identification of Genomic Traits Predisposing to Insect-Bacterial Symbiosis in Pathogenic Strains of the Aphid Symbiont Serratia symbiotica

Renoz, F.; Foray, V.; Ambroise, J. et al.

2021 • In Frontiers in Cellular and Infection Microbiology, 11

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https://hdl.handle.net/2268/262385

DOI
10.3389/fcimb.2021.660007

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34268133

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Keywords :

Serratia symbiotica

Abstract :

[en] Mutualistic associations between insects and heritable bacterial symbionts are ubiquitous in nature. The aphid symbiont Serratia symbiotica is a valuable candidate for studying the evolution of bacterial symbiosis in insects because it includes a wide diversity of strains that reflect the diverse relationships in which bacteria can be engaged with insects, from pathogenic interactions to obligate intracellular mutualism. The recent discovery of culturable strains, which are hypothesized to resemble the ancestors of intracellular strains, provide an opportunity to study the mechanisms underlying bacterial symbiosis in its early stages. In this study, we analyzed the genomes of three of these culturable strains that are pathogenic to aphid hosts, and performed comparative genomic analyses including mutualistic host-dependent strains. All three genomes are larger than those of the host-restricted S. symbiotica strains described so far, and show significant enrichment in pseudogenes and mobile elements, suggesting that these three pathogenic strains are in the early stages of the adaptation to their host. Compared to their intracellular mutualistic relatives, the three strains harbor a greater diversity of genes coding for virulence factors and metabolic pathways, suggesting that they are likely adapted to infect new hosts and are a potential source of metabolic innovation for insects. The presence in their genomes of secondary metabolism gene clusters associated with the production of antimicrobial compounds and phytotoxins supports the hypothesis that S. symbiotia symbionts evolved from plant-associated strains and that plants may serve as intermediate hosts. Mutualistic associations between insects and bacteria are the result of independent transitions to endosymbiosis initiated by the acquisition of environmental progenitors. In this context, the genomes of free-living S. symbiotica strains provide a rare opportunity to study the inventory of genes held by bacterial associates of insects that are at the gateway to a host-dependent lifestyle. © Copyright © 2021 Renoz, Foray, Ambroise, Baa-Puyoulet, Bearzatto, Mendez, Grigorescu, Mahillon, Mardulyn, Gala, Calevro and Hance.

Disciplines :

Microbiology

Author, co-author :

Renoz, F.; Biodiversity Research Centre, Earth and Life Institute, Université catholique de Louvain (UCLouvain), Louvain-la-Neuve, Belgium

Foray, V.; Biodiversity Research Centre, Earth and Life Institute, Université catholique de Louvain (UCLouvain), Louvain-la-Neuve, Belgium, Institut de Recherche sur la Biologie de l’insecte, UMR 7261, CNRS, Université de Tours, Tours, France

Ambroise, J.; Center for Applied Molecular Technologies, Institute of Experimental and Clinical Research, Université catholique de Louvain (UCLouvain), Woluwe-Saint-Lambert, Belgium

Baa-Puyoulet, P.; Univ Lyon, INSA-Lyon, INRAE, BF2i, UMR203, Villeurbanne, F-69621, France

Bearzatto, B.; Center for Applied Molecular Technologies, Institute of Experimental and Clinical Research, Université catholique de Louvain (UCLouvain), Woluwe-Saint-Lambert, Belgium

Mendez, G. L.; Louvain Institute of Biomolecular Science and Technology (LIBST), Université catholique de Louvain (UCLouvain), Louvain-la-Neuve, Belgium

Grigorescu, Alina ; Université de Liège - ULg

Mahillon, J.; Laboratory of Food and Environmental Microbiology, Earth and Life Institute, Université catholique de Louvain (UCLouvain), Louvain-la-Neuve, Belgium

Mardulyn, P.; Evolutionary Biology and Ecology, Université Libre de Bruxelles, Brussels, Belgium

Gala, J.-L.; Center for Applied Molecular Technologies, Institute of Experimental and Clinical Research, Université catholique de Louvain (UCLouvain), Woluwe-Saint-Lambert, Belgium

Calevro, F.; Univ Lyon, INSA-Lyon, INRAE, BF2i, UMR203, Villeurbanne, F-69621, France

Hance, T.; Biodiversity Research Centre, Earth and Life Institute, Université catholique de Louvain (UCLouvain), Louvain-la-Neuve, Belgium

Language :

English

Title :

At the Gate of Mutualism: Identification of Genomic Traits Predisposing to Insect-Bacterial Symbiosis in Pathogenic Strains of the Aphid Symbiont Serratia symbiotica

Publication date :

2021

Journal title :

Frontiers in Cellular and Infection Microbiology

eISSN :

2235-2988

Publisher :

Frontiers Media SA

Volume :

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Fonds De La Recherche Scientifique - FNRS, FNRSFonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture, FRIA: E074.14

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