The evolution of intramitochondriality in Midichloria bacteria

Author:

Floriano Anna Maria12ORCID,Batisti Biffignandi Gherard13,Castelli Michele1,Olivieri Emanuela14,Clementi Emanuela1,Comandatore Francesco5,Rinaldi Laura6,Opara Maxwell7,Plantard Olivier8,Palomar Ana M.9,Noël Valérie10,Vijay Amrita11,Lo Nathan12,Makepeace Benjamin L.13,Duron Olivier10,Jex Aaron1114,Guy Lionel15,Sassera Davide1

Affiliation:

1. Department of Biology and Biotechnology ‘L. Spallanzani’ University of Pavia Pavia Italy

2. Université de Lyon Université Lyon 1, CNRS, VetAgro Sup, Laboratoire de Biométrie et Biologie Evolutive Villeurbanne France

3. Department of Clinical, Surgical, Diagnostic and Pediatric Sciences University of Pavia Pavia Italy

4. Pavia Department Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia‐Romagna Pavia Italy

5. Department of Biomedical and Clinical Sciences, Pediatric Clinical Research Center ‘Romeo ed Enrica Invernizzi’ University of Milan Milan Italy

6. Department of Veterinary Medicine and Animal Production University of Naples Federico II, CREMOPAR Regione Campania Naples Italy

7. Zoonotic Parasites Research Group, Department of Parasitology and Entomology, Faculty of Veterinary Medicine University of Abuja Abuja Nigeria

8. INRAE Oniris, BIOEPAR Nantes France

9. Center of Rickettsiosis and Arthropod‐Borne Diseases (CRETAV) San Pedro University Hospital, Center of Biomedical Research from La Rioja (CIBIR) Logroño Spain

10. MIVEGEC (Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle) University of Montpellier (UM) Montpellier France

11. Population Health and Immunity Division The Walter and Eliza Hall Institute of Medical Research Parkville Victoria Australia

12. School of Life and Environmental Sciences University of Sydney Sydney New South Wales Australia

13. Institute of Infection, Veterinary & Ecological Sciences University of Liverpool Liverpool UK

14. Faculty of Veterinary and Agricultural Sciences The University of Melbourne Melbourne Victoria Australia

15. Department of Medical Biochemistry and Microbiology, Science for Life Laboratories Uppsala University Uppsala Sweden

Abstract

AbstractMidichloria spp. are intracellular bacterial symbionts of ticks. Representatives of this genus colonise mitochondria in the cells of their hosts. To shed light on this unique interaction we evaluated the presence of an intramitochondrial localization for three Midichloria in the respective tick host species and generated eight high‐quality draft genomes and one closed genome, showing that this trait is non‐monophyletic, either due to losses or multiple acquisitions. Comparative genomics supports the first hypothesis, as the genomes of non‐mitochondrial symbionts are reduced subsets of those capable of colonising the organelles. We detect genomic signatures of mitochondrial tropism, including the differential presence of type IV secretion system and flagellum, which could allow the secretion of unique effectors and/or direct interaction with mitochondria. Other genes, including adhesion molecules, proteins involved in actin polymerisation, cell wall and outer membrane proteins, are only present in mitochondrial symbionts. The bacteria could use these to manipulate host structures, including mitochondrial membranes, to fuse with the organelles or manipulate the mitochondrial network.

Funder

European Molecular Biology Organization

Human Frontier Science Program

Publisher

Wiley

Subject

Ecology, Evolution, Behavior and Systematics,Microbiology

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