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Large-scale comparative genomics unravels great genomic diversity across the Rickettsia and Ca. Megaira genera and identifies Torix group as an evolutionarily distinct clade

Davison, Helen R. and Pilgrim, Jack and Wybouw, Nicky and Parker, Joseph and Pirro, Stacy and Hunter-Barnett, Simon and Campbell, Paul M. and Blow, Frances and Darby, Alistair C. and Hurst, Gregory D. D. and Siozios, Stefanos (2021) Large-scale comparative genomics unravels great genomic diversity across the Rickettsia and Ca. Megaira genera and identifies Torix group as an evolutionarily distinct clade. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20211008-224627743

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Abstract

Rickettsia are intracellular bacteria originally described as arthropod borne pathogens that are emerging as a diverse group of often biologically important, non-pathogenic symbionts of invertebrates and microeukaryotes. However, sparse genomic resources for symbiotic strains and for the sister genus (Candidatus Megaira) inhibit our understanding of Rickettsia evolution and biology. Here, we present the first closed genomes of Ca. Megaira from an alga (Mesostigma viride), and Torix Rickettsia from midge (Culicoides impunctatus) and bed bug (Cimex lectularius) hosts. Additionally, we sequenced and constructed draft genomes for Ca. Megaira from another alga (Carteria cerasiformis), Transitional group Rickettsia from tsetse fly (Glossina morsitans submorsitans), and Torix Rickettsia from a spider mite (Bryobia graminum). We further extract 22 draft genomes from arthropod genome sequencing projects, including 1 Adalia, 4 Transitional, 1 Spotted Fever, 7 Torix, 7 Belli and the first Rhyzobius and Meloidae Rickettsia group genomes. We used new and existing Rickettsia genomes to estimate the phylogeny and metabolic potential across groups and reveal transitions in genomic properties. These data reveal Torix as unique amongst currently described Rickettsia, with highly distinct and diverse accessory genomes. We confirm the presence of a third subclade of Torix, previously only known from gene marker sequences. Further, Torix share an intact pentose phosphate pathway with Ca. Megaira, not observed in other Rickettsia. Considering the distinctness and diversity of Torix, we propose that the group be named Candidatus Tisiphia. The wide host range of Ca. Tisiphia symbionts necessitates onward research to understand the biological and physiological bases of Ca. Tisiphia-host interactions.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.10.06.463315DOIDiscussion Paper
https://doi.org/10.6084/m9.figshare.c.5518182.v1DOISupplementary data and full resolution figures
ORCID:
AuthorORCID
Davison, Helen R.0000-0002-4302-5756
Pilgrim, Jack0000-0002-2941-1482
Wybouw, Nicky0000-0001-7874-9765
Parker, Joseph0000-0001-9598-2454
Pirro, Stacy0000-0002-5642-4203
Hunter-Barnett, Simon0000-0003-3283-0933
Campbell, Paul M.0000-0001-5912-6095
Blow, Frances0000-0003-3064-5160
Darby, Alistair C.0000-0002-3786-6209
Hurst, Gregory D. D.0000-0002-7163-7784
Siozios, Stefanos0000-0002-1104-7061
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. Version 1 - October 6, 2021; Version 2 - October 18, 2021. HRD was supported by the NERC ACCE Doctoral Training Programme. Grant code: NE/L002450/1 and NW was supported by a BOF post-doctoral fellowship (Ghent University, 01P03420) and by a Research Foundation - Flanders (FWO) Research Grant (1513719N). Funding for tsetse fly genomics were to ACD IP BBSRC projects BB/J017698/1 and BB/K501773/1, the materials from which were provided by P. Solano (Institut de Recherche pour le Développement, Unité Mixte de Recherche Interactions Hôtes-Vecteurs-Parasites-Environnement dans les Maladies Tropicales Négligées Dues aux Trypanosomatides, 34398, Montpellier, France) and J.-B. Rayaisse (Centre International de Recherche-Développement sur l’Élevage en zone Subhumide (CIRDES), N°559, Rue 5-31 Avenue du Gouverneur Louveau, 01 BP 454, Bobo Dioulasso 01, Burkina Faso). Jean-Baptiste died a few years ago but he was a fantastic person to work with and a great field entomologist. We also wish to thank Dr David Montagnes for teaching skills associated with algal culture. We wish to thank Dr Débora Pires Paula (Embrapa) for granting permission to use SRA data for sample number SRR5651504, Iridian Genomes for allowing use of their SRA data, and the Microbial Culture Collection at the National Institute for Environmental Studies, Japan for use of the sample Carteria cerasiformis NIES-425. Supporting information: All original genomes and raw readsets produced in this study can be accessed at Bioproject accession PRJNA763820 and all assemblies produced from previously published third party data can be accessed at Bioproject PRJNA767332. Author Contributions: Project concept: HRD, SS, JP and GH. Manuscript written by HRD, SS, JP and GDDH. SRA dive and metagenome assembly carried out by HRD with aid from SS. Assembly of genome from SRA, pangenomics and phylogenomics carried out by HRD with advice from SS, GH. Metabolic analysis carried out by HRD, JP and SS. Sequencing and assembly of bacteria from Cimex lecticularius and Culicoides impunctatus genomes by SS and JP. Sequencing and assembly of symbionts from Carteria by SHB and SS, supervised by PC and GH. Sequencing and construction of RiTSETSE carried out by FB as part of thesis work supervised by AD. SP collected and sequenced staphylinid genomes that were released through NCBI by iridian genomics. NW collected and sequenced the Bryobia Moomin strain and performed preliminary metagenomic analyses. The authors have declared no competing interest.
Funders:
Funding AgencyGrant Number
Natural Environment Research Council (NERC)NE/L002450/1
Ghent University01P03420
Fonds Wetenschappelijk Onderzoek (FWO)1513719N
Biotechnology and Biological Sciences Research Council (BBSRC)BB/J017698/1
Biotechnology and Biological Sciences Research Council (BBSRC)BB/K501773/1
DOI:10.1101/2021.10.06.463315
Record Number:CaltechAUTHORS:20211008-224627743
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211008-224627743
Official Citation:Large-scale comparative genomics unravels great genomic diversity across the Rickettsia and Ca. Megaira genera and identifies Torix group as an evolutionarily distinct clade. Helen R Davison, Jack Pilgrim, Nicky Wybouw, Joseph Parker, Stacy Pirro, Simon Hunter-Barnett, Paul M Campbell, Frances Blow, Alistair C Darby, Gregory D D Hurst, Stefanos Siozios. bioRxiv 2021.10.06.463315; doi: https://doi.org/10.1101/2021.10.06.463315
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:111332
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:11 Oct 2021 22:30
Last Modified:26 Oct 2021 16:12

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