{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T16:19:10Z","timestamp":1790785150358,"version":"4.1.0"},"reference-count":62,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,1,8]],"date-time":"2021-01-08T00:00:00Z","timestamp":1610064000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,1,8]],"date-time":"2021-01-08T00:00:00Z","timestamp":1610064000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Commun Biol"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Copper is both essential and toxic to living beings, which tightly controls its intracellular concentration. At the host\u2013pathogen interface, copper is used by phagocytic cells to kill invading microorganisms. We investigated copper homeostasis in <jats:italic>Bordetella pertussis<\/jats:italic>, which lives in the human respiratory mucosa and has no environmental reservoir. <jats:italic>B. pertussis<\/jats:italic> has considerably streamlined copper homeostasis mechanisms relative to other Gram-negative bacteria. Its single remaining defense line consists of a metallochaperone diverted for copper passivation, CopZ, and two peroxide detoxification enzymes, PrxGrx and GorB, which together fight stresses encountered in phagocytic cells. Those proteins are encoded by an original, composite operon assembled in an environmental ancestor, which is under sensitive control by copper. This system appears to contribute to persistent infection in the nasal cavity of <jats:italic>B. pertussis<\/jats:italic>-infected mice. Combining responses to co-occurring stresses in a tailored operon reveals a strategy adopted by a host-restricted pathogen to optimize survival at minimal energy expenditure.<\/jats:p>","DOI":"10.1038\/s42003-020-01580-2","type":"journal-article","created":{"date-parts":[[2021,1,8]],"date-time":"2021-01-08T11:19:34Z","timestamp":1610104774000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Streamlined copper defenses make Bordetella pertussis reliant on custom-made operon"],"prefix":"10.1038","volume":"4","author":[{"given":"Alex","family":"Rivera-Millot","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"St\u00e9phanie","family":"Slupek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan","family":"Chatagnon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gauthier","family":"Roy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0105-5196","authenticated-orcid":false,"given":"Jean-Michel","family":"Saliou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriel","family":"Billon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"V\u00e9ronique","family":"Alaimo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2361-0616","authenticated-orcid":false,"given":"David","family":"Hot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophie","family":"Salom\u00e9-Desnoulez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Camille","family":"Locht","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rudy","family":"Antoine","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5102-1704","authenticated-orcid":false,"given":"Fran\u00e7oise","family":"Jacob-Dubuisson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,1,8]]},"reference":[{"key":"1580_CR1","doi-asserted-by":"crossref","unstructured":"Solioz, M. Copper and Bacteria. Evolution, homeostasis and toxicity, Springer Nature Switzerland AG, Cham, Switzerland (2018).","DOI":"10.1007\/978-3-319-94439-5"},{"key":"1580_CR2","doi-asserted-by":"publisher","first-page":"2512","DOI":"10.1128\/JB.00058-10","volume":"192","author":"S Chillappagari","year":"2010","unstructured":"Chillappagari, S. et al. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J. Bacteriol. 192, 2512\u20132524 (2010).","journal-title":"J. Bacteriol."},{"key":"1580_CR3","doi-asserted-by":"publisher","first-page":"8344","DOI":"10.1073\/pnas.0812808106","volume":"106","author":"L Macomber","year":"2009","unstructured":"Macomber, L. & Imlay, J. A. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl Acad. Sci. USA 106, 8344\u20138349 (2009).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1580_CR4","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/bs.ampbs.2017.01.007","volume":"70","author":"AG Dalecki","year":"2017","unstructured":"Dalecki, A. G., Crawford, C. L. & Wolschendorf, F. Copper and antibiotics: discovery, modes of action, and opportunities for medicinal applications. Adv. Micro. Physiol. 70, 193\u2013260 (2017).","journal-title":"Adv. Micro. Physiol."},{"key":"1580_CR5","doi-asserted-by":"publisher","first-page":"13549","DOI":"10.1074\/jbc.R111.316406","volume":"287","author":"V Hodgkinson","year":"2012","unstructured":"Hodgkinson, V. & Petris, M. J. Copper homeostasis at the host-pathogen interface. J. Biol. Chem. 287, 13549\u201313555 (2012).","journal-title":"J. Biol. Chem."},{"key":"1580_CR6","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1002\/iub.1437","volume":"67","author":"M Migocka","year":"2015","unstructured":"Migocka, M. Copper-transporting ATPases: The evolutionarily conserved machineries for balancing copper in living systems. IUBMB Life 67, 737\u2013745 (2015).","journal-title":"IUBMB Life"},{"key":"1580_CR7","doi-asserted-by":"publisher","first-page":"25057","DOI":"10.1074\/jbc.R000006200","volume":"275","author":"TV O\u2019Halloran","year":"2000","unstructured":"O\u2019Halloran, T. V. & Culotta, V. C. Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275, 25057\u201325060 (2000).","journal-title":"J. Biol. Chem."},{"key":"1580_CR8","doi-asserted-by":"crossref","unstructured":"Stafford, S. L. et al. Metal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper. Biosci Rep. 33, e00049 (2013).","DOI":"10.1042\/BSR20130014"},{"key":"1580_CR9","doi-asserted-by":"publisher","first-page":"33949","DOI":"10.1074\/jbc.M109.070201","volume":"284","author":"C White","year":"2009","unstructured":"White, C., Lee, J., Kambe, T., Fritsche, K. & Petris, M. J. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284, 33949\u201333956 (2009).","journal-title":"J. Biol. Chem."},{"key":"1580_CR10","doi-asserted-by":"publisher","first-page":"628","DOI":"10.1111\/mmi.13483","volume":"102","author":"X Hao","year":"2016","unstructured":"Hao, X. et al. A role for copper in protozoan grazing - two billion years selecting for bacterial copper resistance. Mol. Microbiol 102, 628\u2013641 (2016).","journal-title":"Mol. Microbiol"},{"key":"1580_CR11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.coi.2019.04.002","volume":"60","author":"JR Sheldon","year":"2019","unstructured":"Sheldon, J. R. & Skaar, E. P. Metals as phagocyte antimicrobial effectors. Curr. Opin. Immunol. 60, 1\u20139 (2019).","journal-title":"Curr. Opin. Immunol."},{"key":"1580_CR12","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1038\/nrmicro.2017.15","volume":"15","author":"P Chandrangsu","year":"2017","unstructured":"Chandrangsu, P., Rensing, C. & Helmann, J. D. Metal homeostasis and resistance in bacteria. Nat. Rev. Microbiol 15, 338\u2013350 (2017).","journal-title":"Nat. Rev. Microbiol"},{"key":"1580_CR13","doi-asserted-by":"publisher","first-page":"957","DOI":"10.1039\/C4MT00327F","volume":"7","author":"E Ladomersky","year":"2015","unstructured":"Ladomersky, E. & Petris, M. J. Copper tolerance and virulence in bacteria. Metallomics 7, 957\u2013964 (2015).","journal-title":"Metallomics"},{"key":"1580_CR14","doi-asserted-by":"publisher","first-page":"73","DOI":"10.3389\/fcimb.2013.00073","volume":"3","author":"JM Arguello","year":"2013","unstructured":"Arguello, J. M., Raimunda, D. & Padilla-Benavides, T. Mechanisms of copper homeostasis in bacteria. Front Cell Infect. Microbiol 3, 73 (2013).","journal-title":"Front Cell Infect. Microbiol"},{"key":"1580_CR15","doi-asserted-by":"publisher","first-page":"7815","DOI":"10.1128\/JB.186.22.7815-7817.2004","volume":"186","author":"SK Singh","year":"2004","unstructured":"Singh, S. K., Grass, G., Rensing, C. & Montfort, W. R. Cuprous oxidase activity of CueO from Escherichia coli. J. Bacteriol. 186, 7815\u20137817 (2004).","journal-title":"J. Bacteriol."},{"key":"1580_CR16","doi-asserted-by":"publisher","first-page":"e01007","DOI":"10.1128\/mBio.01007-15","volume":"6","author":"A Durand","year":"2015","unstructured":"Durand, A. et al. c-Type cytochrome assembly is a key target of copper toxicity within the bacterial periplasm. mBio 6, e01007\u2013e01015 (2015).","journal-title":"mBio"},{"key":"1580_CR17","doi-asserted-by":"publisher","first-page":"4934","DOI":"10.1074\/jbc.RA118.006316","volume":"294","author":"L Novoa-Aponte","year":"2019","unstructured":"Novoa-Aponte, L., Ramirez, D. & Arguello, J. M. The interplay of the metallosensor CueR with two distinct CopZ chaperones defines copper homeostasis in Pseudomonas aeruginosa. J. Biol. Chem. 294, 4934\u20134945 (2019).","journal-title":"J. Biol. Chem."},{"key":"1580_CR18","doi-asserted-by":"publisher","first-page":"2217","DOI":"10.3389\/fmicb.2019.02217","volume":"10","author":"R Antoine","year":"2019","unstructured":"Antoine, R., Rivera-Millot, A., Roy, G. & Jacob-Dubuisson, F. Relationships between copper-related proteomes and lifestyles in beta proteobacteria. Front Microbiol 10, 2217 (2019).","journal-title":"Front Microbiol"},{"key":"1580_CR19","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1038\/nrmicro3235","volume":"12","author":"JA Melvin","year":"2014","unstructured":"Melvin, J. A., Scheller, E. V., Miller, J. F. & Cotter, P. A. Bordetella pertussis pathogenesis: current and future challenges. Nat. Rev. Microbiol. 12, 274\u2013288 (2014).","journal-title":"Nat. Rev. Microbiol."},{"key":"1580_CR20","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1042\/EBC20160076","volume":"61","author":"DA Capdevila","year":"2017","unstructured":"Capdevila, D. A., Edmonds, K. A. & Giedroc, D. P. Metallochaperones and metalloregulation in bacteria. Essays Biochem. 61, 177\u2013200 (2017).","journal-title":"Essays Biochem."},{"key":"1580_CR21","doi-asserted-by":"publisher","first-page":"2451","DOI":"10.1099\/mic.0.058487-0","volume":"158","author":"C Rademacher","year":"2012","unstructured":"Rademacher, C. & Masepohl, B. Copper-responsive gene regulation in bacteria. Microbiology 158, 2451\u20132464 (2012).","journal-title":"Microbiology"},{"key":"1580_CR22","doi-asserted-by":"publisher","first-page":"697","DOI":"10.1016\/S0006-291X(03)00249-3","volume":"302","author":"SP Kidd","year":"2003","unstructured":"Kidd, S. P. & Brown, N. L. ZccR\u2013a MerR-like regulator from Bordetella pertussis which responds to zinc, cadmium, and cobalt. Biochem Biophys. Res Commun. 302, 697\u2013702 (2003).","journal-title":"Biochem Biophys. Res Commun."},{"key":"1580_CR23","doi-asserted-by":"publisher","first-page":"5431","DOI":"10.1128\/JB.00271-08","volume":"190","author":"K Helbig","year":"2008","unstructured":"Helbig, K., Bleuel, C., Krauss, G. J. & Nies, D. H. Glutathione and transition-metal homeostasis in Escherichia coli. J. Bacteriol. 190, 5431\u20135438 (2008).","journal-title":"J. Bacteriol."},{"key":"1580_CR24","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/S0378-1097(03)00095-8","volume":"220","author":"DS Radford","year":"2003","unstructured":"Radford, D. S. et al. CopZ from Bacillus subtilis interacts in vivo with a copper exporting CPx-type ATPase CopA. FEMS Microbiol Lett. 220, 105\u2013112 (2003).","journal-title":"FEMS Microbiol Lett."},{"key":"1580_CR25","doi-asserted-by":"publisher","first-page":"9324","DOI":"10.1021\/bi9011995","volume":"48","author":"S Hearnshaw","year":"2009","unstructured":"Hearnshaw, S. et al. A tetranuclear Cu(I) cluster in the metallochaperone protein CopZ. Biochemistry 48, 9324\u20139326 (2009).","journal-title":"Biochemistry"},{"key":"1580_CR26","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/S0014-5793(03)01156-6","volume":"554","author":"N Rouhier","year":"2003","unstructured":"Rouhier, N. & Jacquot, J. P. Molecular and catalytic properties of a peroxiredoxin-glutaredoxin hybrid from Neisseria meningitidis. FEBS Lett. 554, 149\u2013153 (2003).","journal-title":"FEBS Lett."},{"key":"1580_CR27","doi-asserted-by":"publisher","first-page":"20890","DOI":"10.1074\/jbc.M102026200","volume":"276","author":"B Vergauwen","year":"2001","unstructured":"Vergauwen, B. et al. Characterization of glutathione amide reductase from Chromatium gracile. Identification of a novel thiol peroxidase (Prx\/Grx) fueled by glutathione amide redox cycling. J. Biol. Chem. 276, 20890\u201320897 (2001).","journal-title":"J. Biol. Chem."},{"key":"1580_CR28","doi-asserted-by":"publisher","first-page":"16658","DOI":"10.1074\/jbc.M300157200","volume":"278","author":"F Pauwels","year":"2003","unstructured":"Pauwels, F., Vergauwen, B., Vanrobaeys, F., Devreese, B. & Van Beeumen, J. J. Purification and characterization of a chimeric enzyme from Haemophilus influenzae Rd that exhibits glutathione-dependent peroxidase activity. J. Biol. Chem. 278, 16658\u201316666 (2003).","journal-title":"J. Biol. Chem."},{"key":"1580_CR29","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1111\/j.1574-6968.2008.01181.x","volume":"284","author":"A Omsland","year":"2008","unstructured":"Omsland, A., Miranda, K. M., Friedman, R. L. & Boitano, S. Bordetella bronchiseptica responses to physiological reactive nitrogen and oxygen stresses. FEMS Microbiol Lett. 284, 92\u2013101 (2008).","journal-title":"FEMS Microbiol Lett."},{"key":"1580_CR30","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1111\/j.1365-2958.2005.04532.x","volume":"56","author":"K Yamamoto","year":"2005","unstructured":"Yamamoto, K. & Ishihama, A. Transcriptional response of Escherichia coli to external copper. Mol. Microbiol. 56, 215\u2013227 (2005).","journal-title":"Mol. Microbiol."},{"key":"1580_CR31","doi-asserted-by":"publisher","first-page":"954","DOI":"10.1038\/nrmicro1022","volume":"2","author":"J Green","year":"2004","unstructured":"Green, J. & Paget, M. S. Bacterial redox sensors. Nat. Rev. Microbiol 2, 954\u2013966 (2004).","journal-title":"Nat. Rev. Microbiol"},{"key":"1580_CR32","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1515\/hsz-2015-0102","volume":"396","author":"M Hillion","year":"2015","unstructured":"Hillion, M. & Antelmann, H. Thiol-based redox switches in prokaryotes. Biol. Chem. 396, 415\u2013444 (2015).","journal-title":"Biol. Chem."},{"key":"1580_CR33","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1111\/1462-2920.14445","volume":"21","author":"JA Imlay","year":"2019","unstructured":"Imlay, J. A. Where in the world do bacteria experience oxidative stress? Environ. Microbiol 21, 521\u2013530 (2019).","journal-title":"Environ. Microbiol"},{"key":"1580_CR34","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1016\/j.chom.2012.01.009","volume":"11","author":"MI Samanovic","year":"2012","unstructured":"Samanovic, M. I., Ding, C., Thiele, D. J. & Darwin, K. H. Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 11, 106\u2013115 (2012).","journal-title":"Cell Host Microbe"},{"key":"1580_CR35","doi-asserted-by":"publisher","first-page":"15691","DOI":"10.1074\/jbc.M117.804492","volume":"292","author":"J Quintana","year":"2017","unstructured":"Quintana, J., Novoa-Aponte, L. & Arguello, J. M. Copper homeostasis networks in the bacterium Pseudomonas aeruginosa. J. Biol. Chem. 292, 15691\u201315704 (2017).","journal-title":"J. Biol. Chem."},{"key":"1580_CR36","doi-asserted-by":"publisher","first-page":"e2000420","DOI":"10.1371\/journal.pbio.2000420","volume":"15","author":"DL Taylor-Mulneix","year":"2017","unstructured":"Taylor-Mulneix, D. L. et al. Bordetella bronchiseptica exploits the complex life cycle of Dictyostelium discoideum as an amplifying transmission vector. PLoS Biol. 15, e2000420 (2017).","journal-title":"PLoS Biol."},{"key":"1580_CR37","doi-asserted-by":"publisher","first-page":"5139","DOI":"10.1128\/IAI.00895-08","volume":"76","author":"C Andreasen","year":"2008","unstructured":"Andreasen, C. & Carbonetti, N. H. Pertussis toxin inhibits early chemokine production to delay neutrophil recruitment in response to Bordetella pertussisrespiratory tract infection in mice. Infect. Immun. 76, 5139\u20135148 (2008).","journal-title":"Infect. Immun."},{"key":"1580_CR38","doi-asserted-by":"publisher","first-page":"01743","DOI":"10.1128\/mBio.01743-19","volume":"10","author":"JN Ahmad","year":"2019","unstructured":"Ahmad, J. N. et al. Bordetella adenylate cyclase toxin inhibits monocyte-to-macrophage transition and dedifferentiates human alveolar macrophages into monocyte-like cells. mBio 10, 01743\u201319 (2019).","journal-title":"mBio"},{"key":"1580_CR39","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1128\/IAI.01031-09","volume":"78","author":"YA Lamberti","year":"2010","unstructured":"Lamberti, Y. A., Hayes, J. A., Perez Vidakovics, M. L., Harvill, E. T. & Rodriguez, M. E. Intracellular trafficking of Bordetella pertussis in human macrophages. Infect. Immun. 78, 907\u2013913 (2010).","journal-title":"Infect. Immun."},{"key":"1580_CR40","doi-asserted-by":"publisher","first-page":"e0203204","DOI":"10.1371\/journal.pone.0203204","volume":"13","author":"JH Cafiero","year":"2018","unstructured":"Cafiero, J. H., Lamberti, Y. A., Surmann, K., Vecerek, B. & Rodriguez, M. E. A Bordetella pertussis MgtC homolog plays a role in the intracellular survival. PLoS One 13, e0203204 (2018).","journal-title":"PLoS One"},{"key":"1580_CR41","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1016\/j.micpath.2008.01.002","volume":"44","author":"Y Lamberti","year":"2008","unstructured":"Lamberti, Y., Perez Vidakovics, M. L., van der Pol, L. W. & Rodriguez, M. E. Cholesterol-rich domains are involved in Bordetella pertussis phagocytosis and intracellular survival in neutrophils. Micro. Pathog. 44, 501\u2013511 (2008).","journal-title":"Micro. Pathog."},{"key":"1580_CR42","doi-asserted-by":"publisher","first-page":"730","DOI":"10.4049\/jimmunol.175.2.730","volume":"175","author":"AP Boyd","year":"2005","unstructured":"Boyd, A. P. et al. Bordetella pertussis adenylate cyclase toxin modulates innate and adaptive immune responses: distinct roles for acylation and enzymatic activity in immunomodulation and cell death. J. Immunol. 175, 730\u2013738 (2005).","journal-title":"J. Immunol."},{"key":"1580_CR43","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1016\/j.coph.2006.12.004","volume":"7","author":"NH Carbonetti","year":"2007","unstructured":"Carbonetti, N. H. Immunomodulation in the pathogenesis of Bordetella pertussis infection and disease. Curr. Opin. Pharm. 7, 272\u2013278 (2007).","journal-title":"Curr. Opin. Pharm."},{"key":"1580_CR44","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1007\/s00005-013-0242-1","volume":"61","author":"G Fedele","year":"2013","unstructured":"Fedele, G., Bianco, M. & Ausiello, C. M. The virulence factors of Bordetella pertussis: talented modulators of host immune response. Arch. Immunol. Ther. Exp. (Warsz.) 61, 445\u2013457 (2013).","journal-title":"Arch. Immunol. Ther. Exp. (Warsz.)"},{"key":"1580_CR45","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1111\/j.1574-6976.2010.00257.x","volume":"35","author":"D de Gouw","year":"2011","unstructured":"de Gouw, D., Diavatopoulos, D. A., Bootsma, H. J., Hermans, P. W. & Mooi, F. R. Pertussis: a matter of immune modulation. FEMS Microbiol Rev. 35, 441\u2013474 (2011).","journal-title":"FEMS Microbiol Rev."},{"key":"1580_CR46","doi-asserted-by":"publisher","first-page":"764","DOI":"10.1111\/mmi.14190","volume":"111","author":"M Utz","year":"2019","unstructured":"Utz, M. et al. The Cu chaperone CopZ is required for Cu homeostasis in Rhodobacter capsulatus and influences cytochrome cbb3 oxidase assembly. Mol. Microbiol 111, 764\u2013783 (2019).","journal-title":"Mol. Microbiol"},{"key":"1580_CR47","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1039\/C4MT00020J","volume":"6","author":"J Brose","year":"2014","unstructured":"Brose, J., La Fontaine, S., Wedd, A. G. & Xiao, Z. Redox sulfur chemistry of the copper chaperone Atox1 is regulated by the enzyme glutaredoxin 1, the reduction potential of the glutathione couple GSSG\/2GSH and the availability of Cu(I). Metallomics 6, 793\u2013808 (2014).","journal-title":"Metallomics"},{"key":"1580_CR48","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1089\/ars.2012.5086","volume":"19","author":"Y Hatori","year":"2013","unstructured":"Hatori, Y. & Lutsenko, S. An expanding range of functions for the copper chaperone\/antioxidant protein Atox1. Antioxid. Redox Signal 19, 945\u2013957 (2013).","journal-title":"Antioxid. Redox Signal"},{"key":"1580_CR49","doi-asserted-by":"publisher","first-page":"28","DOI":"10.3389\/fmicb.2017.00028","volume":"8","author":"I Hamidou Soumana","year":"2017","unstructured":"Hamidou Soumana, I., Linz, B. & Harvill, E. T. Environmental origin of the genus Bordetella. Front Microbiol 8, 28 (2017).","journal-title":"Front Microbiol"},{"key":"1580_CR50","doi-asserted-by":"publisher","first-page":"2839","DOI":"10.3389\/fmicb.2019.02839","volume":"10","author":"I Rivera","year":"2019","unstructured":"Rivera, I. et al. Conservation of ancient genetic pathways for intracellular persistence among animal pathogenic bordetellae. Front Microbiol. 10, 2839 (2019).","journal-title":"Front Microbiol."},{"key":"1580_CR51","doi-asserted-by":"publisher","first-page":"1016","DOI":"10.1038\/nchembio.2441","volume":"13","author":"EI Koh","year":"2017","unstructured":"Koh, E. I., Robinson, A. E., Bandara, N., Rogers, B. E. & Henderson, J. P. Copper import in Escherichia coli by the yersiniabactin metallophore system. Nat. Chem. Biol. 13, 1016\u20131021 (2017).","journal-title":"Nat. Chem. Biol."},{"key":"1580_CR52","doi-asserted-by":"publisher","first-page":"e0176396","DOI":"10.1371\/journal.pone.0176396","volume":"12","author":"A Rivera-Millot","year":"2017","unstructured":"Rivera-Millot, A. et al. Characterization of a Bvg-regulated fatty acid methyl-transferase in Bordetella pertussis. PLoS ONE 12, e0176396 (2017).","journal-title":"PLoS ONE"},{"key":"1580_CR53","doi-asserted-by":"publisher","first-page":"5902","DOI":"10.1128\/JB.182.20.5902-5905.2000","volume":"182","author":"R Antoine","year":"2000","unstructured":"Antoine, R. et al. New virulence-activated and virulence-repressed genes identified by systematic gene inactivation and generation of transcriptional fusions in Bordetella pertussis. J. Bacteriol. 182, 5902\u20135905 (2000).","journal-title":"J. Bacteriol."},{"key":"1580_CR54","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/0378-1119(95)00584-1","volume":"166","author":"ME Kovach","year":"1995","unstructured":"Kovach, M. E. et al. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166, 175\u2013176 (1995).","journal-title":"Gene"},{"key":"1580_CR55","doi-asserted-by":"publisher","first-page":"e0204861","DOI":"10.1371\/journal.pone.0204861","volume":"13","author":"E Lesne","year":"2018","unstructured":"Lesne, E. et al. Distinct virulence ranges for infection of mice by Bordetella pertussis revealed by engineering of the sensor-kinase BvgS. PLoS ONE 13, e0204861 (2018).","journal-title":"PLoS ONE"},{"key":"1580_CR56","doi-asserted-by":"publisher","first-page":"1673","DOI":"10.3390\/ijms19061673","volume":"19","author":"R Veyron-Churlet","year":"2018","unstructured":"Veyron-Churlet, R. et al. Rv0613c\/MSMEG_1285 Interacts with HBHA and mediates its proper cell-surface exposure in Mycobacteria. Int. J. Mol. Sci. 19, 1673 (2018).","journal-title":"Int. J. Mol. Sci."},{"key":"1580_CR57","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1016\/S0166-4328(01)00297-2","volume":"125","author":"Y Benjamini","year":"2001","unstructured":"Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N. & Golani, I. Controlling the false discovery rate in behavior genetics research. Behav. Brain Res 125, 279\u2013284 (2001).","journal-title":"Behav. Brain Res"},{"key":"1580_CR58","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","volume":"9","author":"J Schindelin","year":"2012","unstructured":"Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676\u2013682 (2012).","journal-title":"Nat. Methods"},{"key":"1580_CR59","doi-asserted-by":"publisher","first-page":"1753","DOI":"10.1038\/s41385-018-0073-9","volume":"11","author":"L Solans","year":"2018","unstructured":"Solans, L. et al. IL-17-dependent SIgA-mediated protection against nasal Bordetella pertussis infection by live attenuated BPZE1 vaccine. Mucosal Immunol. 11, 1753\u20131762 (2018).","journal-title":"Mucosal Immunol"},{"key":"1580_CR60","doi-asserted-by":"crossref","unstructured":"Frith, M. C., Saunders, N. F. W., Kobe, B. & Bailey, T. L. Discovering sequence motifs with arbitrary insertions and deletions. PLoS Comput. Biol. 4, e1000071 (2008).","DOI":"10.1371\/journal.pcbi.1000071"},{"key":"1580_CR61","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-11-431","volume":"11","author":"LS Johnson","year":"2010","unstructured":"Johnson, L. S., Eddy, S. R. & Portugaly, E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinform. 11, 431 (2010).","journal-title":"BMC Bioinform"},{"issue":"D1","key":"1580_CR62","doi-asserted-by":"publisher","first-page":"D442","DOI":"10.1093\/nar\/gky1106","volume":"47","author":"Y Perez-Riverol","year":"2019","unstructured":"Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res 47(D1), D442\u2013D450 (2019).","journal-title":"Nucleic Acids Res"}],"container-title":["Communications Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s42003-020-01580-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-020-01580-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-020-01580-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,27]],"date-time":"2023-01-27T11:47:30Z","timestamp":1674820050000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s42003-020-01580-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,8]]},"references-count":62,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["1580"],"URL":"https:\/\/doi.org\/10.1038\/s42003-020-01580-2","relation":{},"ISSN":["2399-3642"],"issn-type":[{"value":"2399-3642","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,8]]},"assertion":[{"value":"11 February 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 December 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 January 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"46"}}