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Single-cell Microbiomics Unveils Distribution and Patterns of Microbial Symbioses in the Natural Environment

  • Host Microbe Interactions
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Abstract

Protist-bacteria associations are extremely common. Among them, those involving ciliates of the genus Euplotes are emerging as models for symbioses between prokaryotes and eukaryotes, and a great deal of information is available from cultured representatives of this system. Even so, as for most known microbial symbioses, data on natural populations is lacking, and their ecology remains largely unexplored; how well lab cultures represent actual diversity is untested. Here, we describe a survey on natural populations of Euplotes based on a single-cell microbiomic approach, focusing on taxa that include known endosymbionts of this ciliate. The results reveal an unexpected variability in symbiotic communities, with individual hosts of the same population harboring different sets of bacterial endosymbionts. Co-occurring Euplotes individuals of the same population can even have different essential symbionts, Polynucleobacter and “Candidatus Protistobacter,” which might suggest that replacement events could be more frequent in nature than previously hypothesized. Accessory symbionts are even more variable: some showed a strong affinity for one host species, some for a sampling site, and two (“Candidatus Cyrtobacter” and “Candidatus Anadelfobacter”) displayed an unusual pattern of competitive exclusion. These data represent the first insight into the prevalence and patterns of bacterial symbionts in natural populations of free-living protists.

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Data availability

Sanger nucleotide sequences and metabarcoding raw reads have been deposited in the European Nucleotide Archive (ENA) database under accession numbers OU070010-OU070076 and project number PRJEB44318, respectively.

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Not applicable.

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Acknowledgements

The authors wish to thank Simone Gabrielli and Davide Stano for support in sampling and for help with graphic artworks. The authors are grateful to the Migliarino San Rossore Massaciuccoli Regional Park for giving permission for sampling and to Francesca Logli in particular for her assistance.

Funding

This work was supported by the University of Pisa (565–60% 2018, 565–60% 2019, 565–60% 2020, PRA_2018_63) and by the Gordon and Betty Moore Foundation (https://doi.org/10.37807/GBMF9201).

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Authors and Affiliations

  1. Department of Botany, University of British Columbia, Vancouver, Canada

    Vittorio Boscaro & Patrick J. Keeling

  2. Department of Biology, University of Pisa, 56126, Pisa, Italy

    Vittoria Manassero & Claudia Vannini

Authors
  1. Vittorio Boscaro
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  2. Vittoria Manassero
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  3. Patrick J. Keeling
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  4. Claudia Vannini
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Contributions

Vittorio Boscaro and Claudia Vannini conceived and designed the project, analyzed the data, and wrote the first draft of the paper. Field and lab work were performed by Vittoria Manassero and Claudia Vannini. Patrick Keeling and Claudia Vannini supervised the work. All authors contributed to the final draft.

Corresponding author

Correspondence to Claudia Vannini.

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The authors declare no competing interests.

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Boscaro, V., Manassero, V., Keeling, P.J. et al. Single-cell Microbiomics Unveils Distribution and Patterns of Microbial Symbioses in the Natural Environment. Microb Ecol 85, 307–316 (2023). https://doi.org/10.1007/s00248-021-01938-x

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