{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T04:32:20Z","timestamp":1779251540361,"version":"3.51.4"},"reference-count":107,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2023,1,1]],"date-time":"2023-01-01T00:00:00Z","timestamp":1672531200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R03AI149144"],"award-info":[{"award-number":["R03AI149144"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009452","name":"EIS","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100009452","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,1,17]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Coxiella burnetii (Cb) is an obligate intracellular pathogen in nature and the causative agent of acute Q fever as well as chronic diseases. In an effort to identify genes and proteins crucial to their normal intracellular growth lifestyle, we applied a \u2018reverse evolution\u2019 approach where the avirulent Nine Mile Phase II strain of Cb was grown for 67 passages in chemically defined ACCM-D media and gene expression patterns and genome integrity from various passages was compared to passage number one following intracellular growth. Transcriptomic analysis identified a marked downregulation of the structural components of the type 4B secretion system (T4BSS), the general secretory (Sec) pathway, as well as 14 out of 118 previously identified genes encoding effector proteins. Additional downregulated pathogenicity determinants genes included several chaperones, LPS, and peptidoglycan biosynthesis. A general marked downregulation of central metabolic pathways was also observed, which was balanced by a marked upregulation of genes encoding transporters. This pattern reflected the richness of the media and diminishing anabolic, and ATP-generation needs. Finally, genomic sequencing and comparative genomic analysis demonstrated an extremely low level of mutation across passages, despite the observed Cb gene expression changes following acclimation to axenic media.<\/jats:p>","DOI":"10.1093\/femspd\/ftad009","type":"journal-article","created":{"date-parts":[[2023,5,17]],"date-time":"2023-05-17T02:37:21Z","timestamp":1684291041000},"source":"Crossref","is-referenced-by-count":2,"title":["Comparative transcriptomics and genomics from continuous axenic media growth identifies<i>Coxiella burnetii<\/i>intracellular survival strategies"],"prefix":"10.1093","volume":"81","author":[{"given":"Archana","family":"Yadav","sequence":"first","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, Oklahoma State University, , 74078 Stillwater, OK , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Melissa N","family":"Brewer","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, Oklahoma State University, , 74078 Stillwater, OK , United States"},{"name":"Biological Sciences, Southeastern Oklahoma State University , 74078 Durant, OK , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1067-1647","authenticated-orcid":false,"given":"Mostafa S","family":"Elshahed","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, Oklahoma State University, , 74078 Stillwater, OK , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Edward I","family":"Shaw","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, Oklahoma State University, , 74078 Stillwater, OK , United States"},{"name":"Department of Biomedical Sciences, Philadelphia College of Osteopathic Medicine , 74078 Moultrie, GA , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2023,5,16]]},"reference":[{"key":"2023060216323044100_bib1","doi-asserted-by":"crossref","first-page":"1E.13.1","DOI":"10.1002\/cpmc.37","article-title":"Using KBase to assemble and annotate prokaryotic genomes","volume":"46","author":"Allen","year":"2017","journal-title":"Curr Protoc Microbiol"},{"key":"2023060216323044100_bib2","doi-asserted-by":"crossref","first-page":"982","DOI":"10.1128\/jb.160.3.982-988.1984","article-title":"Biochemical and immunological properties of Coxiella burnetii cell wall and peptidoglycan-protein complex fractions","volume":"160","author":"Amano","year":"1984","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib3","doi-asserted-by":"crossref","first-page":"4740","DOI":"10.1016\/S0021-9258(18)61258-X","article-title":"Structure and biological relationships of Coxiella burnetii lipopolysaccharides","volume":"262","author":"Amano","year":"1987","journal-title":"J Biol Chem"},{"key":"2023060216323044100_bib4","doi-asserted-by":"crossref","first-page":"R106","DOI":"10.1186\/gb-2010-11-10-r106","article-title":"Differential expression analysis for sequence count data","volume":"11","author":"Anders","year":"2010","journal-title":"Genome Biol"},{"key":"2023060216323044100_bib5","article-title":"FastQC: a quality control tool for high throughput sequence data","author":"Andrews","year":"2010"},{"key":"2023060216323044100_bib6","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.tig.2007.03.017","article-title":"Evolution of microbial virulence: the benefits of stress","volume":"23","author":"Arnold","year":"2007","journal-title":"Trends Genet"},{"key":"2023060216323044100_bib7","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1051\/vetres:2005010","article-title":"Is Q fever an emerging or re-emerging zoonosis?","volume":"36","author":"Arricau-Bouvery","year":"2005","journal-title":"Vet Res"},{"key":"2023060216323044100_bib8","first-page":"395","article-title":"Ankyrin: structure, properties, and functions","volume":"65","author":"Batrukova","year":"2000","journal-title":"Biochemistry (Mosc)"},{"key":"2023060216323044100_bib9","doi-asserted-by":"crossref","first-page":"1771","DOI":"10.1128\/CVI.00300-08","article-title":"Candidate antigens for Q fever serodiagnosis revealed by immunoscreening of a Coxiella burnetii protein microarray","volume":"15","author":"Beare","year":"2008","journal-title":"Clin Vaccine Immunol"},{"key":"2023060216323044100_bib10","doi-asserted-by":"crossref","first-page":"e00175","DOI":"10.1128\/mBio.00175-11","article-title":"Dot\/Icm type IVB secretion system requirements for Coxiella burnetii growth in human macrophages","volume":"2","author":"Beare","year":"2011","journal-title":"Mbio"},{"key":"2023060216323044100_bib11","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1007\/978-1-4939-1261-2_19","article-title":"Gene inactivation in Coxiella burnetii","volume-title":"Host\u2013Bacteria Interactions","author":"Beare","year":"2014"},{"key":"2023060216323044100_bib12","doi-asserted-by":"crossref","first-page":"e1006922","DOI":"10.1371\/journal.ppat.1006922","article-title":"Genetic mechanisms of Coxiella burnetii lipopolysaccharide phase variation","volume":"14","author":"Beare","year":"2018","journal-title":"PLoS Pathogens"},{"key":"2023060216323044100_bib13","doi-asserted-by":"crossref","first-page":"4580","DOI":"10.1128\/AEM.00881-12","article-title":"Two systems for targeted gene deletion in Coxiella burnetii","volume":"78","author":"Beare","year":"2012","journal-title":"Appl Environ Microbiol"},{"key":"2023060216323044100_bib14","doi-asserted-by":"crossref","first-page":"1925","DOI":"10.1128\/JB.01532-14","article-title":"Essential role for the response regulator PmrA in Coxiella burnetii type 4B secretion and colonization of mammalian host cells","volume":"196","author":"Beare","year":"2014","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib15","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1128\/IAI.01141-08","article-title":"Comparative genomics reveal extensive transposon-mediated genomic plasticity and diversity among potential effector proteins within the genus Coxiella","volume":"77","author":"Beare","year":"2009","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib16","first-page":"230","volume-title":"The identification of immune-reactive proteins recognised in response to Coxiella burnetii infection","author":"Bewley","year":"2015"},{"key":"2023060216323044100_bib17","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"2023060216323044100_bib18","doi-asserted-by":"crossref","first-page":"6666","DOI":"10.1128\/IAI.72.11.6666-6675.2004","article-title":"Both inducible nitric oxide synthase and NADPH oxidase contribute to the control of virulent phase I Coxiella burnetii infections","volume":"72","author":"Brennan","year":"2004","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib19","doi-asserted-by":"crossref","first-page":"1869","DOI":"10.1128\/JCM.41.5.1869-1874.2003","article-title":"Evaluation of Coxiella burnetii antibiotic susceptibilities by real-time PCR assay","volume":"41","author":"Brennan","year":"2003","journal-title":"J Clin Microbiol"},{"key":"2023060216323044100_bib20","doi-asserted-by":"crossref","first-page":"e1002056","DOI":"10.1371\/journal.ppat.1002056","article-title":"The Coxiella burnetii Dot\/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication","volume":"7","author":"Carey","year":"2011","journal-title":"PLoS Pathog"},{"key":"2023060216323044100_bib21","doi-asserted-by":"crossref","first-page":"21755","DOI":"10.1073\/pnas.1010485107","article-title":"Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii","volume":"107","author":"Chen","year":"2010","journal-title":"Proc Natl Acad Sci USA"},{"key":"2023060216323044100_bib22","doi-asserted-by":"crossref","first-page":"7344","DOI":"10.1128\/JB.186.21.7344-7352.2004","article-title":"Temporal analysis of Coxiella burnetii morphological differentiation","volume":"186","author":"Coleman","year":"2004","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib23","doi-asserted-by":"crossref","first-page":"e1010266","DOI":"10.1371\/journal.ppat.1010266","article-title":"The Coxiella burnetii T4SS effector protein AnkG hijacks the 7SK small nuclear ribonucleoprotein complex for reprogramming host cell transcription","volume":"18","author":"Cordsmeier","year":"2022","journal-title":"PLOS Pathogens"},{"key":"2023060216323044100_bib24","doi-asserted-by":"crossref","first-page":"6333","DOI":"10.1128\/jb.172.11.6333-6338.1990","article-title":"Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product","volume":"172","author":"Cotter","year":"1990","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib25","doi-asserted-by":"crossref","first-page":"e00758","DOI":"10.1128\/IAI.00758-17","article-title":"Dot\/Icm-translocated proteins important for biogenesis of the Coxiella burnetii-containing vacuole identified by screening of an effector mutant sublibrary","volume":"86","author":"Crabill","year":"2018","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib26","first-page":"D606","article-title":"The PATRIC Bioinformatics Resource Center: expanding data and analysis capabilities","volume":"48","author":"Davis","year":"2020","journal-title":"Nucleic Acids Res"},{"key":"2023060216323044100_bib27","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/978-1-4939-0554-6_12","article-title":"Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq","volume":"1151","author":"Deatherage","year":"2014","journal-title":"Methods Mol Biol"},{"key":"2023060216323044100_bib28","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1111\/j.1574-6968.2006.00544.x","article-title":"Analysis of the O-antigen biosynthesis regions of phase II isolates of Coxiella burnetii","volume":"267","author":"Denison","year":"2007","journal-title":"FEMS Microbiol Lett"},{"key":"2023060216323044100_bib29","doi-asserted-by":"crossref","first-page":"2763","DOI":"10.1128\/IAI.01204-13","article-title":"Antiapoptotic activity of Coxiella burnetii effector protein AnkG is controlled by p32-dependent trafficking","volume":"82","author":"Eckart","year":"2014","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib30","first-page":"339","article-title":"Immunogenicity of Coxiella burnetii whole cells and their outer membrane components","volume":"38","author":"Gajdosova","year":"1994","journal-title":"Acta Virologica"},{"key":"2023060216323044100_bib31","doi-asserted-by":"crossref","first-page":"D274","DOI":"10.1093\/nar\/gkaa1018","article-title":"COG database update: focus on microbial diversity, model organisms, and widespread pathogens","volume":"49","author":"Galperin","year":"2021","journal-title":"Nucleic Acids Res"},{"key":"2023060216323044100_bib32","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1111\/j.1365-2958.2007.05961.x","article-title":"The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions","volume":"66","author":"Genevaux","year":"2007","journal-title":"Mol Microbiol"},{"key":"2023060216323044100_bib33","doi-asserted-by":"crossref","DOI":"10.1128\/microbiolspec.VMBF-0012-2015","article-title":"Bacterial secretion systems: an overview","volume":"4","author":"Green","year":"2016","journal-title":"Microbiol Spectr"},{"key":"2023060216323044100_bib34","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1093\/bioinformatics\/btt086","article-title":"QUAST: quality assessment tool for genome assemblies","volume":"29","author":"Gurevich","year":"2013","journal-title":"Bioinformatics"},{"key":"2023060216323044100_bib35","doi-asserted-by":"crossref","first-page":"1460","DOI":"10.1111\/j.1462-2920.2007.01560.x","article-title":"Role for the Ankyrin eukaryotic-like genes of Legionella pneumophila in parasitism of protozoan hosts and human macrophages","volume":"10","author":"Habyarimana","year":"2008","journal-title":"Environ Microbiol"},{"key":"2023060216323044100_bib36","doi-asserted-by":"crossref","first-page":"3240","DOI":"10.1073\/pnas.78.5.3240","article-title":"Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii","volume":"78","author":"Hackstadt","year":"1981","journal-title":"Proc Natl Acad Sci USA"},{"key":"2023060216323044100_bib37","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/S0966-842X(99)01475-4","article-title":"Developmental biology of Coxiella burnettii","volume":"7","author":"Heinzen","year":"1999","journal-title":"Trends Microbiol"},{"key":"2023060216323044100_bib38","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1111\/j.1749-6632.2003.tb07426.x","article-title":"Fusogenicity of the coxiella burnetii parasitophorous vacuole","volume":"990","author":"Howe","year":"2003","journal-title":"Ann NY Acad Sci"},{"key":"2023060216323044100_bib39","first-page":"173","article-title":"Isolation and evaluation of Coxiella burnetii O-polysaccharide antigen as an immunodiagnostic reagent","volume":"45","author":"Hussein","year":"2001","journal-title":"Acta Virologica"},{"key":"2023060216323044100_bib40","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.3389\/fmicb.2017.02325","article-title":"Mrp antiporters have important roles in diverse bacteria and archaea","volume":"8","author":"Ito","year":"2017","journal-title":"Front Microbiol"},{"key":"2023060216323044100_bib42","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1016\/j.jmb.2015.11.006","article-title":"BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences","volume":"428","author":"Kanehisa","year":"2016","journal-title":"J Mol Biol"},{"key":"2023060216323044100_bib41","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1002\/pro.3711","article-title":"KEGG Mapper for inferring cellular functions from protein sequences","volume":"29","author":"Kanehisa","year":"2020","journal-title":"Protein Sci"},{"key":"2023060216323044100_bib43","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","article-title":"Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype","volume":"37","author":"Kim","year":"2019","journal-title":"Nat Biotechnol"},{"key":"2023060216323044100_bib44","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1186\/s13059-019-1910-1","article-title":"Transcriptome assembly from long-read RNA-seq alignments with StringTie2","volume":"20","author":"Kovaka","year":"2019","journal-title":"Genome Biol"},{"key":"2023060216323044100_bib45","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1186\/s12864-015-2143-7","article-title":"Major differential gene regulation in Coxiella burnetii between in vivo and in vitro cultivation models","volume":"16","author":"Kuley","year":"2015","journal-title":"BMC Genomics"},{"key":"2023060216323044100_bib46","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1128\/IAI.02763-14","article-title":"Coxiella burnetii effector proteins that localize to the parasitophorous vacuole membrane promote intracellular replication","volume":"83","author":"Larson","year":"2015","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib47","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3389\/fcimb.2017.00048","article-title":"High-content imaging reveals expansion of the endosomal compartment during Coxiella burnetii parasitophorous vacuole maturation","volume":"7","author":"Larson","year":"2017","journal-title":"Front Cell Infect Microbiol"},{"key":"2023060216323044100_bib48","doi-asserted-by":"crossref","first-page":"919","DOI":"10.2217\/fmb-2016-0044","article-title":"Right on Q: genetics begin to unravel Coxiella burnetii host cell interactions","volume":"11","author":"Larson","year":"2016","journal-title":"Future Microbiol"},{"key":"2023060216323044100_bib49","doi-asserted-by":"crossref","first-page":"E707","DOI":"10.1073\/pnas.1215278110","article-title":"Computational modeling and experimental validation of the Legionella and Coxiella virulence-related type-IVB secretion signal","volume":"110","author":"Lifshitz","year":"2013","journal-title":"Proc Natl Acad Sci USA"},{"key":"2023060216323044100_bib50","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol"},{"key":"2023060216323044100_bib51","doi-asserted-by":"crossref","first-page":"ftx047","DOI":"10.1093\/femspd\/ftx047","article-title":"The Coxiella Burnetii type IVB secretion system (T4BSS) component DotA is released\/secreted during infection of host cells and during in vitro growth in a T4BSS-dependent manner","volume":"75","author":"Luedtke","year":"2017","journal-title":"Pathog Dis"},{"key":"2023060216323044100_bib52","doi-asserted-by":"crossref","first-page":"5882","DOI":"10.1128\/IAI.66.12.5882-5888.1998","article-title":"Identification of a 71-kilodalton surface-associated Hsp70 homologue in Coxiella burnetii","volume":"66","author":"Macellaro","year":"1998","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib53","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1093\/femsre\/fuw007","article-title":"Lipopolysaccharide modification in gram-negative bacteria during chronic infection","volume":"40","author":"Maldonado","year":"2016","journal-title":"FEMS Microbiol Rev"},{"key":"2023060216323044100_bib54","first-page":"e52851","article-title":"Generation and multi-phenotypic high-content screening of Coxiella burnetii&nbsp;transposon mutants","volume":"99","author":"Martinez","year":"2015","journal-title":"J Vis Exp"},{"key":"2023060216323044100_bib55","doi-asserted-by":"crossref","first-page":"e1004013","DOI":"10.1371\/journal.ppat.1004013","article-title":"Identification of OmpA, a Coxiella burnetii protein involved in host cell invasion, by multi-phenotypic high-content screening","volume":"10","author":"Martinez","year":"2014","journal-title":"PLoS Pathog"},{"key":"2023060216323044100_bib56","doi-asserted-by":"crossref","first-page":"3269","DOI":"10.1128\/JB.00180-13","article-title":"Refining the plasmid-encoded type IV secretion system substrate repertoire of Coxiella burnetii","volume":"195","author":"Maturana","year":"2013","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib57","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1128\/CMR.12.4.518","article-title":"Q fever","volume":"12","author":"Maurin","year":"1999","journal-title":"Clin Microbiol Rev"},{"key":"2023060216323044100_bib58","doi-asserted-by":"crossref","first-page":"796","DOI":"10.2460\/javma.2002.221.796","article-title":"Q fever","volume":"221","author":"McQuiston","year":"2002","journal-title":"J Am Vet Med Assoc"},{"key":"2023060216323044100_bib59","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1007\/0-387-28159-2_10","article-title":"Fever and bioterrorism","volume-title":"Microorganisms and Bioterrorism","author":"Miller","year":"2006"},{"key":"2023060216323044100_bib60","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1007\/978-94-007-4315-1_12","article-title":"Developmental biology of Coxiella burnetii","volume":"984","author":"Minnick","year":"2012","journal-title":"Adv Exp Med Biol"},{"key":"2023060216323044100_bib61","doi-asserted-by":"crossref","first-page":"D412","DOI":"10.1093\/nar\/gkaa913","article-title":"Pfam: the protein families database in 2021","volume":"49","author":"Mistry","year":"2020","journal-title":"Nucleic Acids Res"},{"key":"2023060216323044100_bib62","doi-asserted-by":"crossref","first-page":"e00009","DOI":"10.1128\/JB.00009-19","article-title":"Coxiella burnetii RpoS regulates genes involved in morphological differentiation and intracellular growth","volume":"201","author":"Moormeier","year":"2019","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib63","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1111\/j.1574-6968.2010.01926.x","article-title":"Polar localization of the Coxiella burnetii type IVB secretion system","volume":"305","author":"Morgan","year":"2010","journal-title":"FEMS Microbiol Lett"},{"key":"2023060216323044100_bib64","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1016\/S0966-842X(01)02174-6","article-title":"The Sec protein-translocation pathway","volume":"9","author":"Mori","year":"2001","journal-title":"Trends Microbiol"},{"key":"2023060216323044100_bib65","doi-asserted-by":"crossref","first-page":"136","DOI":"10.3389\/fmicb.2011.00136","article-title":"Type IVB secretion systems of Legionella and other gram-negative bacteria","volume":"2","author":"Nagai","year":"2011","journal-title":"Front Microbiol"},{"key":"2023060216323044100_bib66","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/j.chom.2008.10.011","article-title":"Molecular chaperones in pathogen virulence: emerging new targets for therapy","volume":"4","author":"Neckers","year":"2008","journal-title":"Cell Host Microbe"},{"key":"2023060216323044100_bib67","doi-asserted-by":"crossref","first-page":"e1004286","DOI":"10.1371\/journal.ppat.1004286","article-title":"A screen of Coxiella burnetii mutants reveals important roles for Dot\/Icm effectors and host autophagy in vacuole biogenesis","volume":"10","author":"Newton","year":"2014","journal-title":"PLoS Pathog"},{"key":"2023060216323044100_bib68","doi-asserted-by":"crossref","first-page":"e54566","DOI":"10.1371\/journal.pone.0054566","article-title":"Effector protein translocation by the Coxiella burnetii Dot\/Icm type IV secretion system requires endocytic maturation of the pathogen-occupied vacuole","volume":"8","author":"Newton","year":"2013","journal-title":"PLoS One"},{"key":"2023060216323044100_bib69","doi-asserted-by":"crossref","first-page":"3720","DOI":"10.1128\/AEM.02826-10","article-title":"Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium","volume":"77","author":"Omsland","year":"2011","journal-title":"Appl Environ Microbiol"},{"key":"2023060216323044100_bib70","doi-asserted-by":"crossref","first-page":"4430","DOI":"10.1073\/pnas.0812074106","article-title":"Host cell-free growth of the Q fever bacterium Coxiella burnetii","volume":"106","author":"Omsland","year":"2009","journal-title":"Proc Natl Acad Sci USA"},{"key":"2023060216323044100_bib71","doi-asserted-by":"crossref","first-page":"1651","DOI":"10.1126\/science.1158160","article-title":"Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors","volume":"320","author":"Pan","year":"2008","journal-title":"Science"},{"key":"2023060216323044100_bib72","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1101\/gr.186072.114","article-title":"CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes","volume":"25","author":"Parks","year":"2015","journal-title":"Genome Res"},{"key":"2023060216323044100_bib73","doi-asserted-by":"crossref","first-page":"559915","DOI":"10.3389\/fcimb.2020.559915","article-title":"The Coxiella burnetii T4SS effector AnkF is important for intracellular replication","volume":"10","author":"Pechstein","year":"2020","journal-title":"Front Cell Infect Microbiol"},{"key":"2023060216323044100_bib74","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/S1473-3099(05)70052-9","article-title":"Natural history and pathophysiology of Q fever","volume":"5","author":"Raoult","year":"2005","journal-title":"Lancet Infect Dis"},{"key":"2023060216323044100_bib75","volume-title":"Coxiella Burnetii: Recent Advances and New Perspectives in Research of the Q Fever Bacterium. Advances in Experimental Medicine and Biology","author":"Rudolf\u00a0Toman","year":"2012"},{"key":"2023060216323044100_bib76","doi-asserted-by":"crossref","first-page":"2503","DOI":"10.1016\/j.carres.2003.07.009","article-title":"Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly","volume":"338","author":"Samuel","year":"2003","journal-title":"Carbohydr Res"},{"key":"2023060216323044100_bib77","doi-asserted-by":"crossref","first-page":"e52","DOI":"10.1002\/cpmc.52","article-title":"Use of axenic culture tools to study Coxiella burnetii","volume":"50","author":"Sanchez","year":"2018","journal-title":"Curr Protoc Microbiol"},{"key":"2023060216323044100_bib78","doi-asserted-by":"crossref","first-page":"3042","DOI":"10.1128\/AEM.00261-16","article-title":"Complementation of arginine auxotrophy for genetic transformation of Coxiella burnetii by use of a defined axenic medium","volume":"82","author":"Sandoz","year":"2016","journal-title":"Appl Environ Microbiol"},{"key":"2023060216323044100_bib79","doi-asserted-by":"crossref","first-page":"e0149957","DOI":"10.1371\/journal.pone.0149957","article-title":"Transcriptional profiling of Coxiella burnetii reveals extensive cell wall remodeling in the small cell variant developmental form","volume":"11","author":"Sandoz","year":"2016","journal-title":"PLoS One"},{"key":"2023060216323044100_bib80","doi-asserted-by":"crossref","DOI":"10.1111\/cmi.12634","article-title":"Nuclear trafficking of the anti-apoptotic Coxiella burnetii effector protein AnkG requires binding to p32 and importin-\u03b11","volume":"19","author":"Sch\u00e4fer","year":"2017","journal-title":"Cell Microbiol"},{"key":"2023060216323044100_bib81","doi-asserted-by":"crossref","first-page":"15396","DOI":"10.1038\/s41598-020-72340-9","article-title":"The anti-apoptotic Coxiella burnetii effector protein AnkG is a strain specific virulence factor","volume":"10","author":"Sch\u00e4fer","year":"2020","journal-title":"Sci Rep"},{"key":"2023060216323044100_bib82","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.femsre.2004.07.001","article-title":"The Icm\/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii","volume":"29","author":"Segal","year":"2005","journal-title":"FEMS Microbiol Rev"},{"key":"2023060216323044100_bib83","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1046\/j.1365-2958.1999.01511.x","article-title":"Possible origin of the Legionella pneumophila virulence genes and their relation to Coxiella burnetii","volume":"33","author":"Segal","year":"1999","journal-title":"Mol Microbiol"},{"key":"2023060216323044100_bib84","doi-asserted-by":"crossref","first-page":"5455","DOI":"10.1073\/pnas.0931379100","article-title":"Complete genome sequence of the Q-fever pathogen Coxiella burnetii","volume":"100","author":"Seshadri","year":"2003","journal-title":"Proc Natl Acad Sci USA"},{"key":"2023060216323044100_bib85","doi-asserted-by":"crossref","first-page":"5983","DOI":"10.1128\/IAI.72.10.5983-5992.2004","article-title":"Legionella pneumophila DotU and IcmF are required for stability of the Dot\/Icm complex","volume":"72","author":"Sexton","year":"2004","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib86","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1034\/j.1600-0854.2002.030303.x","article-title":"Type IVB secretion by intracellular pathogens","volume":"3","author":"Sexton","year":"2002","journal-title":"Traffic"},{"key":"2023060216323044100_bib107_1684904126882","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1186\/1471-2180-13-222","article-title":"Sec-mediated secretion by Coxiella burnetii","volume":"13","author":"Stead","year":"2013","journal-title":"BMC Microbiology"},{"key":"2023060216323044100_bib87","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1128\/IAI.72.3.1364-1373.2004","article-title":"The DnaK\/DnaJ chaperone machinery of Salmonella enterica serovar Typhimurium is essential for invasion of epithelial cells and survival within macrophages, leading to systemic infection","volume":"72","author":"Takaya","year":"2004","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib88","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/nrmicro.2016.161","article-title":"Protein export through the bacterial Sec pathway","volume":"15","author":"Tsirigotaki","year":"2017","journal-title":"Nat Rev Microbiol"},{"key":"2023060216323044100_bib90","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1038\/nrmicro3049","article-title":"Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii","volume":"11","author":"van\u00a0Schaik","year":"2013","journal-title":"Nat Rev Microbiol"},{"key":"2023060216323044100_bib89","doi-asserted-by":"crossref","first-page":"5972","DOI":"10.1128\/IAI.72.10.5972-5982.2004","article-title":"IcmF and DotU are required for optimal effector translocation and trafficking of the Legionella pneumophila vacuole","volume":"72","author":"VanRheenen","year":"2004","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib91","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.1111\/j.1365-2958.2006.05446.x","article-title":"Identification of the core transmembrane complex of the Legionella Dot\/Icm type IV secretion system","volume":"62","author":"Vincent","year":"2006","journal-title":"Mol Microbiol"},{"key":"2023060216323044100_bib92","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1111\/j.1365-2958.2012.08118.x","article-title":"Identification of the DotL coupling protein subcomplex of the Legionella Dot\/Icm type IV secretion system","volume":"85","author":"Vincent","year":"2012","journal-title":"Mol Microbiol"},{"key":"2023060216323044100_bib93","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.tim.2004.01.008","article-title":"Turning a tiger into a house cat: using Legionella pneumophila to study Coxiella burnetii","volume":"12","author":"Vogel","year":"2004","journal-title":"Trends Microbiol"},{"key":"2023060216323044100_bib94","doi-asserted-by":"crossref","first-page":"1493","DOI":"10.1128\/JB.01359-10","article-title":"The Coxiella burnetii cryptic plasmid is enriched in genes encoding type IV secretion system substrates","volume":"193","author":"Voth","year":"2011","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib96","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.mib.2008.11.005","article-title":"Coxiella type IV secretion and cellular microbiology","volume":"12","author":"Voth","year":"2009","journal-title":"Curr Opin Microbiol"},{"key":"2023060216323044100_bib95","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1111\/j.1462-5822.2007.00901.x","article-title":"Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii","volume":"9","author":"Voth","year":"2007","journal-title":"Cell Microbiol"},{"key":"2023060216323044100_bib97","doi-asserted-by":"crossref","first-page":"4232","DOI":"10.1128\/JB.01656-08","article-title":"The Coxiella burnetii ankyrin repeat domain-containing protein family is heterogeneous, with C-terminal truncations that influence Dot\/Icm-mediated secretion","volume":"191","author":"Voth","year":"2009","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib98","doi-asserted-by":"crossref","first-page":"2368","DOI":"10.3390\/app8122368","article-title":"Advances in the assembly model of bacterial type IVB secretion systems","volume":"8","author":"Wang","year":"2018","journal-title":"Appl Sci"},{"key":"2023060216323044100_bib100","doi-asserted-by":"crossref","first-page":"3914","DOI":"10.1128\/JB.00071-13","article-title":"Identification of Coxiella burnetii type IV secretion substrates required for intracellular replication and Coxiella-containing vacuole formation","volume":"195","author":"Weber","year":"2013","journal-title":"J Bacteriol"},{"key":"2023060216323044100_bib99","first-page":"126","volume-title":"Identification of C. burnetii type IV secretion substrates required for intracellular replication and Coxiella-containing vacuole formation","author":"Weber","year":"2014"},{"key":"2023060216323044100_bib101","first-page":"175","article-title":"Antigens, virulence factors, and biological response modifiers of coxiella burnetii: strategies for vaccine development","volume-title":"Q Fever: the Biology of Coxiella Burnetii","author":"Williams","year":"1991"},{"key":"2023060216323044100_bib102","doi-asserted-by":"crossref","first-page":"1608","DOI":"10.1093\/bioinformatics\/btq249","article-title":"PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes","volume":"26","author":"Yu","year":"2010","journal-title":"Bioinformatics"},{"key":"2023060216323044100_bib103","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1046\/j.1365-2958.2003.03626.x","article-title":"Coxiella burnetii express type IV secretion system proteins that function similarly to components of the Legionella pneumophila Dot\/Icm system","volume":"49","author":"Zamboni","year":"2003","journal-title":"Mol Microbiol"},{"key":"2023060216323044100_bib104","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1111\/j.1365-2958.2007.05604.x","article-title":"The response regulator PmrA is a major regulator of the Icm\/Dot type IV secretion system in Legionella pneumophila and Coxiella burnetii","volume":"63","author":"Zusman","year":"2007","journal-title":"Mol Microbiol"},{"key":"2023060216323044100_bib105","doi-asserted-by":"crossref","first-page":"3398","DOI":"10.1128\/IAI.72.6.3398-3409.2004","article-title":"Characterization of the icmH and icmF genes required for Legionella pneumophila intracellular growth, genes that are present in many bacteria associated with eukaryotic cells","volume":"72","author":"Zusman","year":"2004","journal-title":"Infect Immun"},{"key":"2023060216323044100_bib106","doi-asserted-by":"crossref","first-page":"3714","DOI":"10.1128\/IAI.71.7.3714-3723.2003","article-title":"Functional similarities between the Icm\/Dot pathogenesis systems of Coxiella burnetii and Legionella pneumophila","volume":"71","author":"Zusman","year":"2003","journal-title":"Infect Immun"}],"container-title":["Pathogens and Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/femspd\/advance-article-pdf\/doi\/10.1093\/femspd\/ftad009\/50356021\/ftad009.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/femspd\/article-pdf\/doi\/10.1093\/femspd\/ftad009\/50513021\/ftad009.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/femspd\/article-pdf\/doi\/10.1093\/femspd\/ftad009\/50513021\/ftad009.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,13]],"date-time":"2023-12-13T04:03:52Z","timestamp":1702440232000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/femspd\/article\/doi\/10.1093\/femspd\/ftad009\/7165752"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023]]},"references-count":107,"URL":"https:\/\/doi.org\/10.1093\/femspd\/ftad009","relation":{},"ISSN":["2049-632X"],"issn-type":[{"value":"2049-632X","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023]]},"published":{"date-parts":[[2023]]},"article-number":"ftad009"}}