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Genomic diversity across the Rickettsia and ‘Candidatus Megaira’ genera and proposal of genus status for the Torix group

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 (2022) Genomic diversity across the Rickettsia and ‘Candidatus Megaira’ genera and proposal of genus status for the Torix group. Nature Communications, 13 . Art. No. 2630. ISSN 2041-1723. PMCID PMC9098888. doi:10.1038/s41467-022-30385-6. https://resolver.caltech.edu/CaltechAUTHORS:20211008-224627743

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Abstract

Members of the bacterial genus Rickettsia were originally identified as causative agents of vector-borne diseases in mammals. However, many Rickettsia species are arthropod symbionts and close relatives of ‘Candidatus Megaira’, which are symbiotic associates of microeukaryotes. Here, we clarify the evolutionary relationships between these organisms by assembling 26 genomes of Rickettsia species from understudied groups, including the Torix group, and two genomes of ‘Ca. Megaira’ from various insects and microeukaryotes. Our analyses of the new genomes, in comparison with previously described ones, indicate that the accessory genome diversity and broad host range of Torix Rickettsia are comparable to those of all other Rickettsia combined. Therefore, the Torix clade may play unrecognized roles in invertebrate biology and physiology. We argue this clade should be given its own genus status, for which we propose the name ‘Candidatus Tisiphia’.


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URLURL TypeDescription
https://doi.org/10.1038/s41467-022-30385-6DOIArticle
https://www.ncbi.nlm.nih.gov/bioproject/PRJNA763820Related ItemData
https://www.ncbi.nlm.nih.gov/bioproject/767332Related ItemData
https://doi.org/10.5281/zenodo.6396821DOICode
https://github.com/SioStef/panplotsRelated ItemCode
https://doi.org/10.5281/zenodo.6408803DOICode
https://doi.org/10.6084/m9.figshare.14865576.v3DOICode
https://doi.org/10.6084/m9.figshare.14865567.v5DOICode
https://doi.org/10.6084/m9.figshare.14865570.v4DOICode
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9098888/PubMed CentralArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc9098888/PubMed CentralArticle
https://doi.org/10.1101/2021.10.06.463315DOIDiscussion Paper
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
Alternate Title:Large-scale comparative genomics unravels great genomic diversity across the Rickettsia and Ca. Megaira genera and identifies Torix group as an evolutionarily distinct clade
Additional Information:© The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 18 October 2021; Accepted 29 April 2022; Published 12 May 2022. Grant supporting these works: NE/L002450/1 NERC ACCE Doctoral Training Programme, HRD. Ghent University 01P03420 BOF post-doctoral fellowship and 1513719 N Research Foundation - Flanders (FWO) Research Grant, NW. Funding for tsetse fly genomics were to ACD IP BBSRC projects BB/J017698/1 and BB/K501773/1 FB, the materials from which were provided by Philippe Solano (Institut de Recherche pour le Développement, Montpellier, France) and Jean-Baptiste Rayaisse Centre International de Recherche-Développement sur l’Élevage en zone Subhumide (CIRDES), Bobo Dioulasso, 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. Data availability: The genomes and raw read sets generated in this study have been deposited in the GenBank database under accession code PRJNA763820. The assemblies produced from previously published third party data have been deposited in the GenBank database under accession code PRJNA767332. The genome content data and data for figures generated in this study are provided in the Source Data and Supplementary Data. Accessions and metadata for pre-existing genomic data are listed in the Supplementary Data 1 file. Code availability: All code and bioinformatics pipelines used to extract and construct bacterial genomes from SRA data can be found on Zenodo (https://doi.org/10.5281/zenodo.6396821), and the R script for generating pangenome accumulation curves can be found on GitHub (https://github.com/SioStef/panplots and here 10.5281/zenodo.6408803). The full pangenome Anvi’o database is available on Figshare (https://doi.org/10.6084/m9.figshare.14865576.v3). An interactive html version of Fig. 5 and its associated ‘json’ file is available on Figshare (https://doi.org/10.6084/m9.figshare.14865567.v5). html of bonzai module information for Supplementary Fig. 2 is available on Figshare (https://doi.org/10.6084/m9.figshare.14865570.v4). Contributions: Project concept: H.R.D., S.S., Jack Pilgrim, and G.H. Manuscript written by H.R.D., S.S., J.P., and G.H. All authors commented on the manuscript during development and approved the final version. S.R.A. dive and metagenome assembly carried out by H.R.D. with aid from S.S. Assembly of genome from S.R.A., pangenomics and phylogenomics carried out by H.R.D. with advice from S.S., G.H. Metabolic analysis carried out by H.R.D., Jack Pilgrim and S.S. Sequencing and assembly of bacteria from Cimex lectularius and Culicoides impunctatus genomes by S.S. and Jack Pilgrim. Sequencing and assembly of symbionts from Carteria by S.H.B. and S.S, supervised by P.C. and G.H. Sequencing and construction of RiTSETSE conducted by F.B. as part of thesis work supervised by A.D. J. Parker and S.P. collected and sequenced staphylinid genomes that were released through NCBI by Iridian Genomes. N.W. collected and sequenced the Bryobia Moomin strain and performed preliminary metagenomic analyses. The authors declare no competing interests. Peer review information: Nature Communications thanks Joseph Gillespie and the other, anonymous, reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.
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
Subject Keywords:Bacterial genomics; Metagenomics; Phylogenetics; Symbiosis; Taxonomy
PubMed Central ID:PMC9098888
DOI:10.1038/s41467-022-30385-6
Record Number:CaltechAUTHORS:20211008-224627743
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211008-224627743
Official Citation:Davison, H.R., Pilgrim, J., Wybouw, N. et al. Genomic diversity across the Rickettsia and ‘Candidatus Megaira’ genera and proposal of genus status for the Torix group. Nat Commun 13, 2630 (2022). https://doi.org/10.1038/s41467-022-30385-6
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:17 May 2022 15:58

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