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Experimental Sodalis infection eliminates ancient insect symbiont

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Abstract

Many insects benefit from ancient nutrient-supplementing endosymbionts. While symbiont losses and replacements occur on evolutionary timescales, their dynamics remain enigmatic due to the lack of experimentally tractable systems. Here, we report on the experimental establishment of the culturable bacterium Sodalis praecaptivus in a grain pest beetle (Oryzaephilus surinamensis) and its effect on the native symbiont Shikimatogenerans silvanidophilus, which produces the tyrosine precursor prephenate. Injection of Sodalis into female beetles led to systemic intracellular infection and efficient transovarial vertical transmission but reduced host survival and reproduction. Interestingly, Sodalis also invaded the host’s bacteriomes, causing irregular morphology and rapid loss of Shikimatogenerans within three beetle generations. Transcriptomics revealed a strong upregulation of host immune effectors upon Sodalis infection, but little reaction from Shikimatogenerans, indicating that the ancient symbiont is incapable of responding adaptively to the introduced competitor. The rapid elimination of the native symbiont in O. surinamensis showcases the fragility of ancient beneficial symbioses and experimentally recapitulates a crucial step towards a functional symbiont replacement.

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Data availability

The annotated beetle and symbiont genomes and RNAseq data are available in the Edmond open data repository of the Max Planck Society under https://doi.org/10.17617/3.MUV1MF. RNAseq data generated in this study has also been deposited in the NCBI Sequence Read Archive under accession number PRJNA1423255 [http://www.ncbi.nlm.nih.gov/bioproject/1423255]. The bacterial genomes used in this study were obtained from NCBI using accession numbers GCF_018200315.1 [https://www.ncbi.nlm.nih.gov/datasets/genome/GCF_018200315.1/] (Shikimatogenerans silvanidophilus) and GCA_000517425.1 [https://www.ncbi.nlm.nih.gov/datasets/genome/GCF_000517425.1/] (Sodalis praecaptivus). Single-molecule long reads for assembling the Oryzaephilus surinamensis genome were obtained from the NCBI Sequence Read Archive under accession numbers [SRR12881567]-[SRR12881568]. RNAseq data used for annotation of the Oryzaephilus surinamensis genome is available in the NCBI Sequence Read Archive under accession number PRJNA1423469 [http://www.ncbi.nlm.nih.gov/bioproject/1423469]. Source data are provided with this paper.

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Acknowledgements

We thank Freya Weituschat for assistance with beetle rearing and Bruno Hüttel and the Max Planck-Genome-Centre Cologne (http://mpgc.mpipz.mpg.de/home/) for performing library preparation and sequencing. We gratefully acknowledge financial support from the Max Planck Society, the European Research Council through an ERC Consolidator Grant (ERC CoG 819585 “SYMBeetle” to M.K.), and the U.S. National Science Foundation (DEB1926738 to C.D.).

Funding

Open Access funding enabled and organized by Projekt DEAL.

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Authors and Affiliations

  1. Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany

    Ronja Krüsemer, Ana S. P. Carvalho, Jean Keller, Heiko Vogel, Tobias Engl & Martin Kaltenpoth

  2. Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, Toulouse INP, Castanet-Tolosan, France

    Jean Keller

  3. School of Biological Sciences, University of Utah, Salt Lake City, UT, USA

    Colin Dale

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  1. Ronja Krüsemer
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Contributions

R.K. and M.K. conceived the study and designed the experiments. C.D and T.E. provided conceptual support. C.D. provided Sodalis praecaptivus strain MC1. R.K. performed the fitness experiments, microscopy and µCT analysis as well as respective data acquisition and analysis. For the triple RNASeq analysis, R.K. dissected bacteriomes and extracted RNA. H.V. and J.K. assembled and annotated the O. surinamensis genome. A.S.P.C. and J.K. performed the gene expression analyses. M.K. and T.E. provided supervision. R.K. and M.K. drafted the original manuscript. All authors reviewed and edited the final manuscript version.

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Martin Kaltenpoth.

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Krüsemer, R., Carvalho, A.S.P., Keller, J. et al. Experimental Sodalis infection eliminates ancient insect symbiont.
Nat Commun (2026). https://doi.org/10.1038/s41467-026-71143-2

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