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A New Species of the γ-Proteobacterium Francisella, F. adeliensis Sp. Nov., Endocytobiont in an Antarctic Marine Ciliate and Potential Evolutionary Forerunner of Pathogenic Species

  • Microbiology of Aquatic Systems
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Abstract

The study of the draft genome of an Antarctic marine ciliate, Euplotes petzi, revealed foreign sequences of bacterial origin belonging to the γ-proteobacterium Francisella that includes pathogenic and environmental species. TEM and FISH analyses confirmed the presence of a Francisella endocytobiont in E. petzi. This endocytobiont was isolated and found to be a new species, named F. adeliensis sp. nov.. F. adeliensis grows well at wide ranges of temperature, salinity, and carbon dioxide concentrations implying that it may colonize new organisms living in deeply diversified habitats. The F. adeliensis genome includes the igl and pdp gene sets (pdpC and pdpE excepted) of the Francisella pathogenicity island needed for intracellular growth. Consistently with an F. adeliensis ancient symbiotic lifestyle, it also contains a single insertion-sequence element. Instead, it lacks genes for the biosynthesis of essential amino acids such as cysteine, lysine, methionine, and tyrosine. In a genome-based phylogenetic tree, F. adeliensis forms a new early branching clade, basal to the evolution of pathogenic species. The correlations of this clade with the other clades raise doubts about a genuine free-living nature of the environmental Francisella species isolated from natural and man-made environments, and suggest to look at F. adeliensis as a pioneer in the Francisella colonization of eukaryotic organisms.

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Acknowledgments

E.V. was supported by the Universidad de Sevilla (Movilidad Docente ERASMUS). We acknowledge the National Genomics Infrastructure (NGI)/Uppsala Genome Center and UPPMAX for providing assistance in massive parallel sequencing and computational infrastructure..

Funding

This work was financially supported by the PNRA (Programma Nazionale di Ricerca in Antartide) from the Italian Ministry of Research (MIUR), FAR (Fondo Ateneo Ricerca) from the University of Camerino, by the Swedish Ministry of Defence (A4040), and the Swedish Civil Contingencies Agency (B4010). The work performed at NGI/Uppsala Genome Center was funded by RFI/VR and Science for Life Laboratory, Sweden.

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Authors and Affiliations

  1. School of Biosciences and Veterinary Medicine, University of Camerino, 62032, Camerino, MC, Italy

    Adriana Vallesi, Dezemona Petrelli & Pierangelo Luporini

  2. Department of Chemistry, Computational Life Science Cluster (CLiC), Umeå University, Umeå, Sweden

    Andreas Sjödin

  3. Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, Umeå, Sweden

    Andreas Sjödin, Johanna Thelaus, Caroline Öhrman & Elin Nilsson

  4. Center of Large Equipment-section of Electron Microscopy, University of Tuscia, Largo dell’Università, snc, Viterbo, Italy

    Anna Rita Taddei

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

    Graziano Di Giuseppe

  6. Departamento de Genética, Universidad de Sevilla, Av Reina Mercedes 6, 41012, Seville, Spain

    Gabriel Gutiérrez

  7. Departamento de Microbiología, Universidad de Sevilla, Av Reina Mercedes 6, 41012, Seville, Spain

    Eduardo Villalobo

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  1. Adriana Vallesi
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Correspondence to Adriana Vallesi or Eduardo Villalobo.

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Vallesi, A., Sjödin, A., Petrelli, D. et al. A New Species of the γ-Proteobacterium Francisella, F. adeliensis Sp. Nov., Endocytobiont in an Antarctic Marine Ciliate and Potential Evolutionary Forerunner of Pathogenic Species. Microb Ecol 77, 587–596 (2019). https://doi.org/10.1007/s00248-018-1256-3

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