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Evidence for Gut-Associated Serratia symbiotica in Wild Aphids and Ants Provides New Perspectives on the Evolution of Bacterial Mutualism in Insects

  • François Renoz
  • Inès Pons
  • Alain Vanderpoorten
  • Gwennaël Bataille
  • Christine Noël
  • Vincent Foray
  • Valentin Pierson
  • Thierry Hance
Invertebrate Microbiology

Abstract

Many insects engage in symbiotic associations with diverse assemblages of bacterial symbionts that can deeply impact on their ecology and evolution. The intraspecific variation of symbionts remains poorly assessed while phenotypic effects and transmission behaviors, which are key processes for the persistence and evolution of symbioses, may differ widely depending on the symbiont strains. Serratia symbiotica is one of the most frequent symbiont species in aphids and a valuable model to assess this intraspecific variation since it includes both facultative and obligate symbiotic strains. Despite evidence that some facultative S. symbiotica strains exhibit a free-living capacity, the presence of these strains in wild aphid populations, as well as in insects with which they maintain regular contact, has never been demonstrated. Here, we examined the prevalence, diversity, and tissue tropism of S. symbiotica in wild aphids and associated ants. We found a high occurrence of S. symbiotica infection in ant populations, especially when having tended infected aphid colonies. We also found that the S. symbiotica diversity includes strains found located within the gut of aphids and ants. In the latter, this tissue tropism was found restricted to the proventriculus. Altogether, these findings highlight the extraordinary diversity and versatility of an insect symbiont and suggest the existence of novel routes for symbiont acquisition in insects.

Keywords

Ant Aphid Bacterial mutualism Gut symbiont Horizontal transmission Serratia symbiotica 

Notes

Acknowledgments

The authors thank deeply Abdelmounaim Errachid and Charles Hachez for technical support regarding confocal microscopy and Florence Hecq and Marianne Renoz for their helpful comments on the earlier version of the manuscript. This paper is publication BRC394 of the Biodiversity Research center (Université catholique de Louvain).

Authors’ Contributions

FR conceived and designed the research; FR, IP, VP, and CN performed the research; FR, IP, GB, AV, CN, VF, and VP analyzed the data; FR wrote the paper; VF, IP, AV, and TH made manuscript revisions. All authors gave final approval for publication.

Funding

This work was supported by the Fonds de la Recherche Scientifique (FNRS) through a Fonds pour la Recherche en Industrie et en Agronomie (FRIA) (FRIA grant no. 1.E074.14). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Compliance with Ethical Standards

Competing Interests

The authors declare that they have no conflict of interest.

Supplementary material

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Authors and Affiliations

  1. 1.Biodiversity Research Centre, Earth and Life InstituteUniversité catholique de LouvainLouvain-la-NeuveBelgium
  2. 2.Department of Biology, Institute of BotanyUniversity of LiègeLiegeBelgium
  3. 3.Centre de Recherche de Biologie cellulaire de Montpellier, UMR CNRS 5237MontpellierFrance

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