Section: Microbiology
Topic: Microbiology, Genetics/Genomics, Evolution

Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum

10.24072/pcjournal.269 - Peer Community Journal, Volume 3 (2023), article no. e41.

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The Coxiellaceae family is composed of five genera showing lifestyles ranging from free-living to symbiosis. Among them, Coxiella burnetii is a well-known pathogen causing Q fever in humans. This bacterium presents both intracellular (parasitic) and environmental (resistant) forms. Recently, several environmental Coxiella genomes have been reported, among which several have come from intracellular mutualistic symbionts of ticks, termed Coxiella-like endosymbionts. We sequenced two new Coxiella-LE genomes from Dermacentor marginatus (CLEDm) and Ornithodoros maritimus (CLEOmar) ticks, the latter belonging to the C. burnetii lineage. Using these newly sequenced Coxiella-LEs and 43 Coxiellaceae genomes, we conducted comparative genomic and phylogenomic analyses to increase our knowledge of C. burnetii pathogenicity and the emergence of Coxiella-LEs. Results highlight the probably parasitic nature of the common ancestor of the Coxiellaceae. Indeed, the virulence factor Dot/Icm T4 Secretion System is present in most, but not all, Coxiellaceae. Whereas it is part of a putative pathogenic island in C. burnetii, it has been entirely lost or inactivated in Coxiella-LEs, suggesting its importance in pathogenesis. Additionally, we found that a Sha/Mrp antiporter was laterally acquired in the C. burnetii lineage. This antiporter might be involved in alkali resistance and the development of the resistant form that is able to persist in the environment for long periods of time. The Sha operon is eroded or absent in Coxiella-LEs. Finally, we found that all Coxiella representatives produce B vitamins and co-factors indicating a pre-adaptation of Coxiella to mutualism with hematophagous arthropods. Accordingly, the ancestor of C. burnetii and Coxiella-LEs was likely a parasitic bacterium able to manipulate its host cell and to produce vitamins and co-factors for its own use.

Published online:
DOI: 10.24072/pcjournal.269
Type: Research article
Keywords: Coxiella; Q fever; endosymbiosis; ticks; pathogenic island; pH homeostasis

Santos-Garcia, Diego 1, 2; Morel, Olivier 1; Henri, Hélène 1; El Filali, Adil 1; Buysse, Marie 3; Noël, Valérie 3; McCoy, Karen D. 3; Gottlieb, Yuval 4; Klasson, Lisa 5; Zenner, Lionel 1; Duron, Olivier 3; Vavre, Fabrice 1

1 University of Lyon, University Lyon 1, CNRS, VetAgro Sup, Laboratory of Biometry and Evolutionary Biology, UMR5558, Villeurbanne, France.
2 Present address: Center for Biology and Management of Populations (CBGP) INRAe UMR1062, Montferrier-sur-Lez, France.
3 MIVEGEC, University of Montpellier, CNRS, IRD, Montpellier, France.
4 Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.
5 Molecular evolution, Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Santos-Garcia, Diego and Morel, Olivier and Henri, H\'el\`ene and El Filali, Adil and Buysse, Marie and No\"el, Val\'erie and McCoy, Karen D. and Gottlieb, Yuval and Klasson, Lisa and Zenner, Lionel and Duron, Olivier and Vavre, Fabrice},
     title = {Genomic changes during the evolution of the {\protect\emph{Coxiella}} genus along the parasitism-mutualism continuum},
     journal = {Peer Community Journal},
     eid = {e41},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.269},
     url = {}
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AU  - Noël, Valérie
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AU  - Gottlieb, Yuval
AU  - Klasson, Lisa
AU  - Zenner, Lionel
AU  - Duron, Olivier
AU  - Vavre, Fabrice
TI  - Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum
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%0 Journal Article
%A Santos-Garcia, Diego
%A Morel, Olivier
%A Henri, Hélène
%A El Filali, Adil
%A Buysse, Marie
%A Noël, Valérie
%A McCoy, Karen D.
%A Gottlieb, Yuval
%A Klasson, Lisa
%A Zenner, Lionel
%A Duron, Olivier
%A Vavre, Fabrice
%T Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum
%J Peer Community Journal
%D 2023
%V 3
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%R 10.24072/pcjournal.269
%F 10_24072_pcjournal_269
Santos-Garcia, Diego; Morel, Olivier; Henri, Hélène; El Filali, Adil; Buysse, Marie; Noël, Valérie; McCoy, Karen D.; Gottlieb, Yuval; Klasson, Lisa; Zenner, Lionel; Duron, Olivier; Vavre, Fabrice. Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum. Peer Community Journal, Volume 3 (2023), article  no. e41. doi : 10.24072/pcjournal.269.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.microbiol.100003

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Anantharaman, K.; Brown, C. T.; Hug, L. A.; Sharon, I.; Castelle, C. J.; Probst, A. J.; Thomas, B. C.; Singh, A.; Wilkins, M. J.; Karaoz, U.; Brodie, E. L.; Williams, K. H.; Hubbard, S. S.; Banfield, J. F. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system, Nature Communications, Volume 7 (2016) no. 1 | DOI

[2] Baker-Austin, C.; Dopson, M. Life in acid: pH homeostasis in acidophiles, Trends in Microbiology, Volume 15 (2007) no. 4, pp. 165-171 | DOI

[3] Bankevich, A.; Nurk, S.; Antipov, D.; Gurevich, A. A.; Dvorkin, M.; Kulikov, A. S.; Lesin, V. M.; Nikolenko, S. I.; Pham, S.; Prjibelski, A. D.; Pyshkin, A. V.; Sirotkin, A. V.; Vyahhi, N.; Tesler, G.; Alekseyev, M. A.; Pevzner, P. A. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing, Journal of Computational Biology, Volume 19 (2012) no. 5, pp. 455-477 | DOI

[4] Ben-Yosef, M.; Rot, A.; Mahagna, M.; Kapri, E.; Behar, A.; Gottlieb, Y. Coxiella-Like Endosymbiont of Rhipicephalus sanguineus Is Required for Physiological Processes During Ontogeny, Frontiers in Microbiology, Volume 11 (2020) | DOI

[5] Bertelli, C.; Laird, M. R.; Williams, K. P.; Lau, B. Y.; Hoad, G.; Winsor, G. L.; Brinkman, F. S. IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets, Nucleic Acids Research, Volume 45 (2017) no. W1 | DOI

[6] Brenner, A. E.; Muñoz-Leal, S.; Sachan, M.; Labruna, M. B.; Raghavan, R. Coxiella burnetii and Related Tick Endosymbionts Evolved from Pathogenic Ancestors, Genome Biology and Evolution, Volume 13 (2021) no. 7 | DOI

[7] Buysse, M.; Duhayon, M.; Cantet, F.; Bonazzi, M.; Duron, O. Vector competence of the African argasid tick Ornithodoros moubata for the Q fever agent Coxiella burnetii, PLOS Neglected Tropical Diseases, Volume 15 (2021) no. 1 | DOI

[8] Buysse, M.; Duron, O. Evidence that microbes identified as tick-borne pathogens are nutritional endosymbionts, Cell, Volume 184 (2021) no. 9, pp. 2259-2260 | DOI

[9] Buysse, M.; Plantard, O.; McCoy, K. D.; Duron, O.; Menard, C. Tissue localization of Coxiella-like endosymbionts in three European tick species through fluorescence in situ hybridization, Ticks and Tick-borne Diseases, Volume 10 (2019) no. 4, pp. 798-804 | DOI

[10] Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T. L. BLAST+: architecture and applications, BMC Bioinformatics, Volume 10 (2009) no. 1 | DOI

[11] Castresana, J. Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis, Molecular Biology and Evolution, Volume 17 (2000) no. 4, pp. 540-552 | DOI

[12] Chakraborty, M.; Mahmud, N. U.; Gupta, D. R.; Tareq, F. S.; Shin, H. J.; Islam, T. Inhibitory Effects of Linear Lipopeptides From a Marine Bacillus subtilis on the Wheat Blast Fungus Magnaporthe oryzae Triticum, Frontiers in Microbiology, Volume 11 (2020) | DOI

[13] Coleman, S. A.; Fischer, E. R.; Cockrell, D. C.; Voth, D. E.; Howe, D.; Mead, D. J.; Samuel, J. E.; Heinzen, R. A. Proteome and Antigen Profiling of Coxiella burnetii Developmental Forms, Infection and Immunity, Volume 75 (2007) no. 1, pp. 290-298 | DOI

[14] Coleman, S. A.; Fischer, E. R.; Howe, D.; Mead, D. J.; Heinzen, R. A. Temporal Analysis of Coxiella burnetii Morphological Differentiation, Journal of Bacteriology, Volume 186 (2004) no. 21, pp. 7344-7352 | DOI

[15] Conway, J. R.; Lex, A.; Gehlenborg, N. UpSetR: an R package for the visualization of intersecting sets and their properties, Bioinformatics, Volume 33 (2017) no. 18, pp. 2938-2940 | DOI

[16] Duron, O.; Binetruy, F.; Noël, V.; Cremaschi, J.; McCoy, K. D.; Arnathau, C.; Plantard, O.; Goolsby, J.; Pérez de León, A. A.; Heylen, D. J. A.; Van Oosten, A. R.; Gottlieb, Y.; Baneth, G.; Guglielmone, A. A.; Estrada‐Peña, A.; Opara, M. N.; Zenner, L.; Vavre, F.; Chevillon, C. Evolutionary changes in symbiont community structure in ticks, Molecular Ecology, Volume 26 (2017) no. 11, pp. 2905-2921 | DOI

[17] Duron, O.; Doublet, P.; Vavre, F.; Bouchon, D. The Importance of Revisiting Legionellales Diversity, Trends in Parasitology, Volume 34 (2018) no. 12, pp. 1027-1037 | DOI

[18] Duron, O.; Gottlieb, Y. Convergence of Nutritional Symbioses in Obligate Blood Feeders, Trends in Parasitology, Volume 36 (2020) no. 10, pp. 816-825 | DOI

[19] Duron, O.; Morel, O.; Noël, V.; Buysse, M.; Binetruy, F.; Lancelot, R.; Loire, E.; Ménard, C.; Bouchez, O.; Vavre, F.; Vial, L. Tick-Bacteria Mutualism Depends on B Vitamin Synthesis Pathways, Current Biology, Volume 28 (2018) no. 12 | DOI

[20] Duron, O.; Noël, V.; McCoy, K. D.; Bonazzi, M.; Sidi-Boumedine, K.; Morel, O.; Vavre, F.; Zenner, L.; Jourdain, E.; Durand, P.; Arnathau, C.; Renaud, F.; Trape, J.-F.; Biguezoton, A. S.; Cremaschi, J.; Dietrich, M.; Léger, E.; Appelgren, A.; Dupraz, M.; Gómez-Díaz, E.; Diatta, G.; Dayo, G.-K.; Adakal, H.; Zoungrana, S.; Vial, L.; Chevillon, C. The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii, PLOS Pathogens, Volume 11 (2015) no. 5 | DOI

[21] Duron, O.; Sidi-Boumedine, K.; Rousset, E.; Moutailler, S.; Jourdain, E. The Importance of Ticks in Q Fever Transmission: What Has (and Has Not) Been Demonstrated?, Trends in Parasitology, Volume 31 (2015) no. 11, pp. 536-552 | DOI

[22] Ellegaard, K. M.; Klasson, L.; Näslund, K.; Bourtzis, K.; Andersson, S. G. E. Comparative Genomics of Wolbachia and the Bacterial Species Concept, PLoS Genetics, Volume 9 (2013) no. 4 | DOI

[23] Emms, D. M.; Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics, Genome Biology, Volume 20 (2019) no. 1 | DOI

[24] Feng, Y.; Napier, B. A.; Manandhar, M.; Henke, S. K.; Weiss, D. S.; Cronan, J. E. AFrancisellavirulence factor catalyses an essential reaction of biotin synthesis, Molecular Microbiology, Volume 91 (2014) no. 2, pp. 300-314 | DOI

[25] Foster, J. W. Escherichia coli acid resistance: tales of an amateur acidophile, Nature Reviews Microbiology, Volume 2 (2004) no. 11, pp. 898-907 | DOI

[26] Gomez-Valero, L.; Chiner-Oms, A.; Comas, I.; Buchrieser, C. Evolutionary Dissection of the Dot/Icm System Based on Comparative Genomics of 58 Legionella Species, Genome Biology and Evolution, Volume 11 (2019) no. 9, pp. 2619-2632 | DOI

[27] Gomez-Valero, L.; Rusniok, C.; Carson, D.; Mondino, S.; Pérez-Cobas, A. E.; Rolando, M.; Pasricha, S.; Reuter, S.; Demirtas, J.; Crumbach, J.; Descorps-Declere, S.; Hartland, E. L.; Jarraud, S.; Dougan, G.; Schroeder, G. N.; Frankel, G.; Buchrieser, C. More than 18,000 effectors in the Legionella genus genome provide multiple, independent combinations for replication in human cells, Proceedings of the National Academy of Sciences, Volume 116 (2019) no. 6, pp. 2265-2273 | DOI

[28] Gottlieb, Y.; Lalzar, I.; Klasson, L. Distinctive Genome Reduction Rates Revealed by Genomic Analyses of Two Coxiella-Like Endosymbionts in Ticks, Genome Biology and Evolution, Volume 7 (2015) no. 6, pp. 1779-1796 | DOI

[29] Guizzo, M. G.; Parizi, L. F.; Nunes, R. D.; Schama, R.; Albano, R. M.; Tirloni, L.; Oldiges, D. P.; Vieira, R. P.; Oliveira, W. H. C.; Leite, M. d. S.; Gonzales, S. A.; Farber, M.; Martins, O.; Vaz, I. d. S.; Oliveira, P. L. A Coxiella mutualist symbiont is essential to the development of Rhipicephalus microplus, Scientific Reports, Volume 7 (2017) no. 1 | DOI

[30] Guy, L.; Roat Kultima, J.; Andersson, S. G. E. genoPlotR: comparative gene and genome visualization in R, Bioinformatics, Volume 26 (2010) no. 18, pp. 2334-2335 | DOI

[31] Hacker, J.; Kaper, J. B. Pathogenicity Islands and the Evolution of Microbes, Annual Review of Microbiology, Volume 54 (2000) no. 1, pp. 641-679 | DOI

[32] Hackstadt, T. Estimation of the cytoplasmic pH of Coxiella burnetii and effect of substrate oxidation on proton motive force, Journal of Bacteriology, Volume 154 (1983) no. 2, pp. 591-597 | DOI

[33] Hackstadt, T.; Williams, J. C. Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii., Proceedings of the National Academy of Sciences, Volume 78 (1981) no. 5, pp. 3240-3244 | DOI

[34] Hackstadt, T.; Williams, J. C. pH dependence of the Coxiella burnetii glutamate transport system, Journal of Bacteriology, Volume 154 (1983) no. 2, pp. 598-603 | DOI

[35] Hyatt, D.; Chen, G.-L.; LoCascio, P. F.; Land, M. L.; Larimer, F. W.; Hauser, L. J. Prodigal: prokaryotic gene recognition and translation initiation site identification, BMC Bioinformatics, Volume 11 (2010) no. 1 | DOI

[36] Ito, M.; Morino, M.; Krulwich, T. A. Mrp Antiporters Have Important Roles in Diverse Bacteria and Archaea, Frontiers in Microbiology, Volume 8 (2017) | DOI

[37] Kalyaanamoorthy, S.; Minh, B. Q.; Wong, T. K. F.; von Haeseler, A.; Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates, Nature Methods, Volume 14 (2017) no. 6, pp. 587-589 | DOI

[38] Kampschreur, L. M.; Delsing, C. E.; Groenwold, R. H. H.; Wegdam-Blans, M. C. A.; Bleeker-Rovers, C. P.; de Jager-Leclercq, M. G. L.; Hoepelman, A. I. M.; van Kasteren, M. E.; Buijs, J.; Renders, N. H. M.; Nabuurs-Franssen, M. H.; Oosterheert, J. J.; Wever, P. C. Chronic Q Fever in the Netherlands 5 Years after the Start of the Q Fever Epidemic: Results from the Dutch Chronic Q Fever Database, Journal of Clinical Microbiology, Volume 52 (2014) no. 5, pp. 1637-1643 | DOI

[39] Katoh, K. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Research, Volume 30 (2002) no. 14, pp. 3059-3066 | DOI

[40] Kelkar, Y. D.; Ochman, H. Genome Reduction Promotes Increase in Protein Functional Complexity in Bacteria, Genetics, Volume 193 (2013) no. 1, pp. 303-307 | DOI

[41] Klyachko, O.; Stein, B. D.; Grindle, N.; Clay, K.; Fuqua, C. Localization and Visualization of a Coxiella -Type Symbiont within the Lone Star Tick, Amblyomma americanum, Applied and Environmental Microbiology, Volume 73 (2007) no. 20, pp. 6584-6594 | DOI

[42] Kosono, S.; Haga, K.; Tomizawa, R.; Kajiyama, Y.; Hatano, K.; Takeda, S.; Wakai, Y.; Hino, M.; Kudo, T. Characterization of a Multigene-Encoded Sodium/Hydrogen Antiporter (Sha) from Pseudomonas aeruginosa : Its Involvement in Pathogenesis, Journal of Bacteriology, Volume 187 (2005) no. 15, pp. 5242-5248 | DOI

[43] Kosono, S.; Ohashi, Y.; Kawamura, F.; Kitada, M.; Kudo, T. Function of a Principal Na+/H+ Antiporter, ShaA, Is Required for Initiation of Sporulation in Bacillus subtilis, Journal of Bacteriology, Volume 182 (2000) no. 4, pp. 898-904 | DOI

[44] Kozlowski, L. P. IPC – Isoelectric Point Calculator, Biology Direct, Volume 11 (2016) no. 1 | DOI

[45] Kozlowski, L. P. IPC 2.0: prediction of isoelectric point and pKa dissociation constants, Nucleic Acids Research, Volume 49 (2021) no. W1 | DOI

[46] Krulwich, T. A.; Sachs, G.; Padan, E. Molecular aspects of bacterial pH sensing and homeostasis, Nature Reviews Microbiology, Volume 9 (2011) no. 5, pp. 330-343 | DOI

[47] La Scola, B.; Raoult, D. Survival of Coxiella burnetii within free-living amoeba Acanthamoeba castellanii, Clinical Microbiology and Infection, Volume 7 (2001) no. 2, pp. 75-79 | DOI

[48] Lagesen, K.; Hallin, P.; Rødland, E. A.; Stærfeldt, H.-H.; Rognes, T.; Ussery, D. W. RNAmmer: consistent and rapid annotation of ribosomal RNA genes, Nucleic Acids Research, Volume 35 (2007) no. 9, pp. 3100-3108 | DOI

[49] Lalzar, I.; Friedmann, Y.; Gottlieb, Y. Tissue tropism and vertical transmission ofCoxiellainRhipicephalus sanguineusandRhipicephalus turanicusticks, Environmental Microbiology, Volume 16 (2014) no. 12, pp. 3657-3668 | DOI

[50] Lalzar, I.; Harrus, S.; Mumcuoglu, K. Y.; Gottlieb, Y. Composition and Seasonal Variation of Rhipicephalus turanicus and Rhipicephalus sanguineus Bacterial Communities, Applied and Environmental Microbiology, Volume 78 (2012) no. 12, pp. 4110-4116 | DOI

[51] Langmead, B.; Salzberg, S. L. Fast gapped-read alignment with Bowtie 2, Nature Methods, Volume 9 (2012) no. 4, pp. 357-359 | DOI

[52] Latorre, A.; Manzano-Marín, A. Dissecting genome reduction and trait loss in insect endosymbionts, Annals of the New York Academy of Sciences, Volume 1389 (2017) no. 1, pp. 52-75 | DOI

[53] Li, L.-H.; Zhang, Y.; Zhu, D. Effects of antibiotic treatment on the fecundity of Rhipicephalus haemaphysaloides ticks, Parasites & Vectors, Volume 11 (2018) no. 1 | DOI

[54] Liu, L.; Li, L.; Liu, J.; Hu, Y.; Liu, Z.; Guo, L.; Liu, J. Coinfection of Dermacentor silvarum Olenev (Acari: Ixodidae) by Coxiella-Like, Arsenophonus-Like, and Rickettsia-Like Symbionts, Applied and Environmental Microbiology, Volume 79 (2013) no. 7, pp. 2450-2454 | DOI

[55] Lowe, T. M.; Eddy, S. R. tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence, Nucleic Acids Research, Volume 25 (1997) no. 5, pp. 955-964 | DOI

[56] Łukasik, P.; van Asch, M.; Guo, H.; Ferrari, J.; Charles J. Godfray, H. Unrelated facultative endosymbionts protect aphids against a fungal pathogen, Ecology Letters, Volume 16 (2012) no. 2, pp. 214-218 | DOI

[57] Lund, P.; Tramonti, A.; De Biase, D. Coping with low pH: molecular strategies in neutralophilic bacteria, FEMS Microbiology Reviews, Volume 38 (2014) no. 6, pp. 1091-1125 | DOI

[58] Madariaga, M. G.; Rezai, K.; Trenholme, G. M.; Weinstein, R. A. Q fever: a biological weapon in your backyard, The Lancet Infectious Diseases, Volume 3 (2003) no. 11, pp. 709-721 | DOI

[59] Manzano-Marín, A.; Lamelas, A.; Moya, A.; Latorre, A. Comparative Genomics of Serratia spp.: Two Paths towards Endosymbiotic Life, PLoS ONE, Volume 7 (2012) no. 10 | DOI

[60] Manzano-Marín, A.; Oceguera-Figueroa, A.; Latorre, A.; Jiménez-García, L. F.; Moya, A. Solving a Bloody Mess: B-Vitamin Independent Metabolic Convergence among Gammaproteobacterial Obligate Endosymbionts from Blood-Feeding Arthropods and the LeechHaementeria officinalis, Genome Biology and Evolution, Volume 7 (2015) no. 10, pp. 2871-2884 | DOI

[61] Manzano-Marín, A.; Simon, J.-C.; Latorre, A. Reinventing the Wheel and Making It Round Again: Evolutionary Convergence inBuchneraSerratiaSymbiotic Consortia between the Distantly Related Lachninae AphidsTuberolachnus salignusandCinara cedri, Genome Biology and Evolution, Volume 8 (2016) no. 5, pp. 1440-1458 | DOI

[62] Mediannikov, O.; Ivanov, L.; Nishikawa, M.; Saito, R.; Sidelnikov, Y. N.; Zdanovskaya, N. I.; Tarasevich, I. V.; Suzuki, H. Molecular Evidence ofCoxiella-like Microorganism Harbored byHaemaphysalis concinnaeTicks in the Russian Far East, Annals of the New York Academy of Sciences, Volume 990 (2003) no. 1, pp. 226-228 | DOI

[63] Mehari, Y. T.; Jason Hayes, B.; Redding, K. S.; Mariappan, P. V. G.; Gunderson, J. H.; Farone, A. L.; Farone, M. B. Description of ‘Candidatus Berkiella aquae’ and ‘Candidatus Berkiella cookevillensis’, two intranuclear bacteria of freshwater amoebae, International Journal of Systematic and Evolutionary Microbiology, Volume 66 (2016) no. 2, pp. 536-541 | DOI

[64] Miele, V.; Penel, S.; Duret, L. Ultra-fast sequence clustering from similarity networks with SiLiX, BMC Bioinformatics, Volume 12 (2011) no. 1 | DOI

[65] Minnick, M. F.; Raghavan, R. Developmental Biology of Coxiella burnetii, Advances in Experimental Medicine and Biology, Springer Netherlands, Dordrecht, 2012, pp. 231-248 | DOI

[66] Modolo, L.; Lerat, E. UrQt: an efficient software for the Unsupervised Quality trimming of NGS data, BMC Bioinformatics, Volume 16 (2015) no. 1 | DOI

[67] Moran, N. A.; Bennett, G. M. The Tiniest Tiny Genomes, Annual Review of Microbiology, Volume 68 (2014) no. 1, pp. 195-215 | DOI

[68] Moriya, Y.; Itoh, M.; Okuda, S.; Yoshizawa, A. C.; Kanehisa, M. KAAS: an automatic genome annotation and pathway reconstruction server, Nucleic Acids Research, Volume 35 (2007) no. Web Server | DOI

[69] Moses, A. S.; Millar, J. A.; Bonazzi, M.; Beare, P. A.; Raghavan, R. Horizontally Acquired Biosynthesis Genes Boost Coxiella burnetii's Physiology, Frontiers in Cellular and Infection Microbiology, Volume 7 (2017) | DOI

[70] Murray, G. G. R.; Charlesworth, J.; Miller, E. L.; Casey, M. J.; Lloyd, C. T.; Gottschalk, M.; Tucker, A. W. (.; Welch, J. J.; Weinert, L. A. Genome reduction is associated with bacterial pathogenicity across different scales of temporal and ecological divergence | DOI

[71] Nguyen, L.-T.; Schmidt, H. A.; von Haeseler, A.; Minh, B. Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies, Molecular Biology and Evolution, Volume 32 (2014) no. 1, pp. 268-274 | DOI

[72] Oakeson, K. F.; Gil, R.; Clayton, A. L.; Dunn, D. M.; von Niederhausern, A. C.; Hamil, C.; Aoyagi, A.; Duval, B.; Baca, A.; Silva, F. J.; Vallier, A.; Jackson, D. G.; Latorre, A.; Weiss, R. B.; Heddi, A.; Moya, A.; Dale, C. Genome Degeneration and Adaptation in a Nascent Stage of Symbiosis, Genome Biology and Evolution, Volume 6 (2014) no. 1, pp. 76-93 | DOI

[73] Okonechnikov, K.; Conesa, A.; García-Alcalde, F. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data, Bioinformatics, Volume 32 (2015) no. 2, pp. 292-294 | DOI

[74] Omsland, A.; Cockrell, D. C.; Fischer, E. R.; Heinzen, R. A. Sustained Axenic Metabolic Activity by the Obligate Intracellular Bacterium Coxiella burnetii, Journal of Bacteriology, Volume 190 (2008) no. 9, pp. 3203-3212 | DOI

[75] Park, S. W.; Klotzsche, M.; Wilson, D. J.; Boshoff, H. I.; Eoh, H.; Manjunatha, U.; Blumenthal, A.; Rhee, K.; Barry, C. E.; Aldrich, C. C.; Ehrt, S.; Schnappinger, D. Evaluating the Sensitivity of Mycobacterium tuberculosis to Biotin Deprivation Using Regulated Gene Expression, PLoS Pathogens, Volume 7 (2011) no. 9 | DOI

[76] Pati, A.; Ivanova, N. N.; Mikhailova, N.; Ovchinnikova, G.; Hooper, S. D.; Lykidis, A.; Kyrpides, N. C. GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes, Nature Methods, Volume 7 (2010) no. 6, pp. 455-457 | DOI

[77] Punta, M.; Coggill, P. C.; Eberhardt, R. Y.; Mistry, J.; Tate, J.; Boursnell, C.; Pang, N.; Forslund, K.; Ceric, G.; Clements, J.; Heger, A.; Holm, L.; Sonnhammer, E. L. L.; Eddy, S. R.; Bateman, A.; Finn, R. D. The Pfam protein families database, Nucleic Acids Research, Volume 40 (2011) no. D1 | DOI

[78] Putnoky, P.; Kereszt, A.; Nakamura, T.; Endre, G.; Grosskopf, E.; Kiss, P.; Kondorosi, A. The pha gene cluster of Rhizobium meliloti involved in pH adaptation and symbiosis encodes a novel type of K+ efflux system, Molecular Microbiology, Volume 28 (1998) no. 6, pp. 1091-1101 | DOI

[79] R Core Team R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Vienna, Austria, 2020 (

[80] Rutherford, K.; Parkhill, J.; Crook, J.; Horsnell, T.; Rice, P.; Rajandream, M.-A.; Barrell, B. Artemis: sequence visualization and annotation, Bioinformatics, Volume 16 (2000) no. 10, pp. 944-945 | DOI

[81] Sandoz, K. M.; Popham, D. L.; Beare, P. A.; Sturdevant, D. E.; Hansen, B.; Nair, V.; Heinzen, R. A. Transcriptional Profiling of Coxiella burnetii Reveals Extensive Cell Wall Remodeling in the Small Cell Variant Developmental Form, PLOS ONE, Volume 11 (2016) no. 2 | DOI

[82] Santos, P.; Pinhal, I.; Rainey, F. A.; Empadinhas, N.; Costa, J.; Fields, B.; Benson, R.; Veríssimo, A.; da Costa, M. S. Gamma-Proteobacteria Aquicella lusitana gen. nov., sp. nov., and Aquicella siphonis sp. nov. Infect Protozoa and Require Activated Charcoal for Growth in Laboratory Media, Applied and Environmental Microbiology, Volume 69 (2003) no. 11, pp. 6533-6540 | DOI

[83] van Schaik, E. J.; Chen, C.; Mertens, K.; Weber, M. M.; Samuel, J. E. Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii, Nature Reviews Microbiology, Volume 11 (2013) no. 8, pp. 561-573 | DOI

[84] Seemann, T. Prokka: rapid prokaryotic genome annotation, Bioinformatics, Volume 30 (2014) no. 14, pp. 2068-2069 | DOI

[85] Seppey, M.; Manni, M.; Zdobnov, E. M. BUSCO: Assessing Genome Assembly and Annotation Completeness, Methods in Molecular Biology, Springer New York, New York, NY, 2019, pp. 227-245 | DOI

[86] Smith, T. A.; Driscoll, T.; Gillespie, J. J.; Raghavan, R. A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick, Genome Biology and Evolution, Volume 7 (2015) no. 3, pp. 831-838 | DOI

[87] Steinegger, M.; Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets, Nature Biotechnology, Volume 35 (2017) no. 11, pp. 1026-1028 | DOI

[88] Stewart, A. C.; Osborne, B.; Read, T. D. DIYA: a bacterial annotation pipeline for any genomics lab, Bioinformatics, Volume 25 (2009) no. 7, pp. 962-963 | DOI

[89] Tatusov, R. L.; Fedorova, N. D.; Jackson, J. D.; Jacobs, A. R.; Kiryutin, B.; Koonin, E. V.; Krylov, D. M.; Mazumder, R.; Mekhedov, S. L.; Nikolskaya, A. N.; Rao, B. S.; Smirnov, S.; Sverdlov, A. V.; Vasudevan, S.; Wolf, Y. I.; Yin, J. J.; Natale, D. A. The COG Database: a Tool for Genome-Scale Analysis of Protein Functions and Evolution, BMC Bioinformatics, Volume 4 (2003) no. 1 | DOI

[90] The UniProt Consortium Reorganizing the protein space at the Universal Protein Resource (UniProt), Nucleic Acids Research, Volume 40 (2012) no. D1 | DOI

[91] Tsuchida, T.; Koga, R.; Horikawa, M.; Tsunoda, T.; Maoka, T.; Matsumoto, S.; Simon, J.-C.; Fukatsu, T. Symbiotic Bacterium Modifies Aphid Body Color, Science, Volume 330 (2010) no. 6007, pp. 1102-1104 | DOI

[92] Varani, A. M.; Siguier, P.; Gourbeyre, E.; Charneau, V.; Chandler, M. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes, Genome Biology, Volume 12 (2011) no. 3 | DOI

[93] Voth, D. E.; Heinzen, R. A. Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii, Cellular Microbiology, Volume 9 (2007) no. 4, pp. 829-840 | DOI

[94] Wick, R. R.; Schultz, M. B.; Zobel, J.; Holt, K. E. Bandage: interactive visualization of de novo genome assemblies, Bioinformatics, Volume 31 (2015) no. 20, pp. 3350-3352 | DOI

[95] Williamson, J.; Brown, G. Purification and properties of L-Aspartate-alpha-decarboxylase, an enzyme that catalyzes the formation of beta-alanine in Escherichia coli., Journal of Biological Chemistry, Volume 254 (1979) no. 16, pp. 8074-8082 | DOI

[96] Yamamura, N. Vertical Transmission and Evolution of Mutualism from Parasitism, Theoretical Population Biology, Volume 44 (1993) no. 1, pp. 95-109 | DOI

[97] Zhong, J.; Jasinskas, A.; Barbour, A. G. Antibiotic Treatment of the Tick Vector Amblyomma americanum Reduced Reproductive Fitness, PLoS ONE, Volume 2 (2007) no. 5 | DOI

[98] Zhu, Q.; Kosoy, M.; Dittmar, K. HGTector: an automated method facilitating genome-wide discovery of putative horizontal gene transfers, BMC Genomics, Volume 15 (2014) no. 1 | DOI

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