{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T04:53:29Z","timestamp":1791089609962,"version":"4.1.0"},"reference-count":70,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T00:00:00Z","timestamp":1790899200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>The zinc import system ZnuABC is essential for the virulence of smooth (bearing O-polysaccharide chains) zoonotic Brucella species but remains uncharacterized in the non-zoonotic rough (lacking O-chains) species Brucella ovis, the causative agent of a type of ovine brucellosis of veterinary and economic importance. In this study, we constructed a panel of B. ovis mutants for genes of the znuACB locus that were characterized by evaluating growth, gene expression, protein abundance, metal content, and virulence in mice. We identified a ZigA ortholog (uncharacterized in the genus Brucella but linked to zinc homeostasis and histidine metabolism in other bacteria) that belongs to the Zur regulon and is transcriptionally modulated in a zinc-dependent manner as the ZnuABC system. A potential link of B. ovis ZigA with histidine catabolism and a crosstalk between the homeostasis of zinc and other metals have been identified as areas for further exploration. Remarkably, the znuA, zigAznuA and znuACB mutants of B. ovis displayed wild-type virulence in mice, which contrasts with the reported attenuation for the znuA mutant of smooth zoonotic Brucella species sharing a high degree of DNA homology. These results significantly enlarge the knowledge about the metallobiology of the genus Brucella, providing new perspectives for related research.<\/jats:p>","DOI":"10.3390\/biology15191753","type":"journal-article","created":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T10:14:56Z","timestamp":1790936096000},"page":"1753","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Zinc Homeostasis in Brucella ovis Under Zinc Scarcity: Characterization of the ZnuABC Zinc Import System and of a Newly Identified Gene of the Zur Regulon"],"prefix":"10.3390","volume":"15","author":[{"given":"Beatriz","family":"Tartil\u00e1n-Choya","sequence":"first","affiliation":[{"name":"Departamento de Microbiolog\u00eda y Gen\u00e9tica, Universidad de Salamanca, 37007 Salamanca, Spain"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0461-0522","authenticated-orcid":false,"given":"Ian S.","family":"Barton","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, NC 27834, USA"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"}]},{"suffix":"II","given":"R. Martin","family":"Roop","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, NC 27834, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1687-1559","authenticated-orcid":false,"given":"Nieves","family":"Vizca\u00edno","sequence":"additional","affiliation":[{"name":"Departamento de Microbiolog\u00eda y Gen\u00e9tica, Universidad de Salamanca, 37007 Salamanca, Spain"},{"name":"Instituto de Investigaci\u00f3n Biom\u00e9dica de Salamanca (IBSAL), 37007 Salamanca, Spain"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,10,2]]},"reference":[{"key":"ref_1","unstructured":"OIE (2021). Chapter 3.8.7. Ovine epididymitis (Brucella ovis). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2021, OIE. Available online: https:\/\/www.oie.int\/fileadmin\/Home\/eng\/Health_standards\/tahm\/3.08.07_OVINE_EPID.pdf."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Picard-Hagen, N., Berthelot, X., Champion, J.L., Eon, L., Lyazrhi, F., Marois, M., Peglion, M., Schuster, A., Trouche, C., and Garin-Bastuji, B. (2015). Contagious epididymitis due to Brucella ovis: Relationship between sexual function, serology and bacterial shedding in semen. BMC Vet. Res., 11.","DOI":"10.1186\/s12917-015-0440-7"},{"key":"ref_3","unstructured":"OIE (2021). Chapter 3.1.4. Brucellosis (infection with B. abortus, B. melitensis and B. suis). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2021, OIE. Available online: https:\/\/www.oie.int\/fileadmin\/Home\/eng\/Health_standards\/tahm\/3.01.04_BRUCELLOSIS.pdf."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e00021-19","DOI":"10.1128\/MMBR.00021-19","article-title":"Uncovering the Hidden Credentials of Brucella Virulence","volume":"85","author":"Roop","year":"2021","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1186\/s13567-014-0072-0","article-title":"Mutants in the lipopolysaccharide of Brucella ovis are attenuated and protect against B. ovis infection in mice","volume":"45","author":"Iriarte","year":"2014","journal-title":"Vet. Res."},{"key":"ref_6","unstructured":"Mar\u00edn, C.M., Mainar, R.C., de Miguel, M.J., Andr\u00e9s, S., Alvarez, J.J., Blasco, J.M., and Mu\u00f1oz, P.M. (2019, January 2\u20133). Re-emergence of Brucella ovis infection in Aragon (Spain) after the ban of Rev 1 vaccination. Proceedings of the 72nd Annual Brucellosis Research Conference, Chicago, IL, USA."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1007\/s00430-009-0123-8","article-title":"Survival of the fittest: How Brucella strains adapt to their intracellular niche in the host","volume":"198","author":"Roop","year":"2009","journal-title":"Med. Microbiol. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1042\/BST20180275","article-title":"The role of metal ions in the virulence and viability of bacterial pathogens","volume":"47","author":"Begg","year":"2019","journal-title":"Biochem. Soc. Trans."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1038\/nrmicro.2017.15","article-title":"Metal homeostasis and resistance in bacteria","volume":"15","author":"Chandrangsu","year":"2017","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/s41579-022-00745-6","article-title":"Nutritional immunity: The battle for nutrient metals at the host-pathogen interface","volume":"20","author":"Murdoch","year":"2022","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1146\/annurev-genet-120215-035146","article-title":"Transition Metals and Virulence in Bacteria","volume":"50","author":"Palmer","year":"2016","journal-title":"Annu. Rev. Genet."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1016\/j.tibs.2019.06.010","article-title":"Nutrient Zinc at the Host-Pathogen Interface","volume":"44","author":"Lonergan","year":"2019","journal-title":"Trends Biochem. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"20858","DOI":"10.1074\/jbc.R116.742023","article-title":"Bacterial Strategies to Maintain Zinc Metallostasis at the Host-Pathogen Interface","volume":"291","author":"Capdevila","year":"2016","journal-title":"J. Biol. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.cbpa.2013.12.021","article-title":"Recent developments in copper and zinc homeostasis in bacterial pathogens","volume":"19","author":"Braymer","year":"2014","journal-title":"Curr. Opin. Chem. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1042\/EBC20160076","article-title":"Metallochaperones and metalloregulation in bacteria","volume":"61","author":"Capdevila","year":"2017","journal-title":"Essays Biochem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1017\/S1466252312000047","article-title":"Metal acquisition and virulence in Brucella","volume":"13","author":"Roop","year":"2012","journal-title":"Anim. Health Res. Rev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2452","DOI":"10.1099\/mic.0.082446-0","article-title":"Control of zinc homeostasis in Agrobacterium tumefaciens via zur and the zinc uptake genes znuABC and zinT","volume":"160","author":"Bhubhanil","year":"2014","journal-title":"Microbiology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1747","DOI":"10.1007\/s10534-026-00828-4","article-title":"The genes zntA and zntR encoding a P-type ATPase and its activator confer zinc and cadmium resistance in Chromobacterium violaceum","volume":"39","author":"Schuindt","year":"2026","journal-title":"BioMetals"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2327377","DOI":"10.1080\/19490976.2024.2327377","article-title":"ZntA maintains zinc and cadmium homeostasis and promotes oxidative stress resistance and virulence in Vibrio parahaemolyticus","volume":"16","author":"Zheng","year":"2024","journal-title":"Gut Microbes"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1582","DOI":"10.1128\/JB.02543-14","article-title":"Coordinated zinc homeostasis is essential for the wild-type virulence of Brucella abortus","volume":"197","author":"Sheehan","year":"2015","journal-title":"J. Bacteriol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Tartil\u00e1n-Choya, B., Tejedor, C., Conde-\u00c1lvarez, R., Mu\u00f1oz, M.P., and Vizca\u00edno, N. (2024). Characterization of three predicted zinc exporters in Brucella ovis identifies ZntR-ZntA as a powerful zinc and cadmium efflux system not required for virulence and unveils pathogenic Brucellae heterogeneity in zinc homeostasis. Front. Vet. Sci., 10.","DOI":"10.3389\/fvets.2023.1323500"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1730","DOI":"10.1099\/mic.0.000135","article-title":"Roles of Agrobacterium tumefaciens C58 ZntA and ZntB and the transcriptional regulator ZntR in controlling Cd2+\/Zn2+\/Co2+ resistance and the peroxide stress response","volume":"161","author":"Chaoprasid","year":"2015","journal-title":"Microbiology"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1292\/jvms.66.1059","article-title":"Zinc uptake system (znuA locus) of Brucella abortus is essential for intracellular survival and virulence in mice","volume":"66","author":"Kim","year":"2004","journal-title":"J. Vet. Med. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4165","DOI":"10.1128\/IAI.05080-11","article-title":"Protective live oral brucellosis vaccines stimulate Th1 and th17 cell responses","volume":"79","author":"Clapp","year":"2011","journal-title":"Infect. Immun."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3874","DOI":"10.1128\/IAI.01957-05","article-title":"Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge","volume":"74","author":"Yang","year":"2006","journal-title":"Infect. Immun."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/j.chom.2016.05.007","article-title":"The Response of Acinetobacter baumannii to Zinc Starvation","volume":"19","author":"Nairn","year":"2016","journal-title":"Cell Host Microbe"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1783","DOI":"10.1128\/IAI.06257-11","article-title":"Quorum-sensing and BvrR\/BvrS regulation, the type IV secretion system, cyclic glucans, and BacA in the virulence of Brucella ovis: Similarities to and differences from smooth brucellae","volume":"80","author":"Sancho","year":"2012","journal-title":"Infect. Immun."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/0378-1119(95)00584-1","article-title":"Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes","volume":"166","author":"Kovach","year":"1995","journal-title":"Gene"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"13139","DOI":"10.1038\/srep13139","article-title":"ZnuA and zinc homeostasis in Pseudomonas aeruginosa","volume":"5","author":"Pederick","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"6594","DOI":"10.1128\/JB.01091-12","article-title":"The zinc-responsive regulon of Neisseria meningitidis comprises 17 genes under control of a Zur element","volume":"194","author":"Pawlik","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Tsolis, R.M., Seshadri, R., Santos, R.L., Sangari, F.J., Garc\u00eda Lobo, J.M., de Jong, M.F., Ren, Q., Myers, G., Brinkac, L.M., and Nelson, W.C. (2009). Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0005519"},{"key":"ref_32","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":"ref_33","doi-asserted-by":"crossref","first-page":"D523","DOI":"10.1093\/nar\/gkac1052","article-title":"UniProt: The Universal Protein Knowledgebase in 2023","volume":"51","author":"UniProt","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Sidhu-Mu\u00f1oz, R.S., Tejedor, C., and Vizca\u00edno, N. (2020). The Three Flagellar Loci of Brucella ovis PA Are Dispensable for Virulence in Cellular Models and Mice. Front. Vet. Sci., 7.","DOI":"10.3389\/fvets.2020.00441"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Tartil\u00e1n-Choya, B., Sidhu-Mu\u00f1oz, R.S., and Vizca\u00edno, N. (2022). The Transcriptional Regulator MucR, but Not Its Controlled Acid-Activated Chaperone HdeA, Is Essential for Virulence and Modulates Surface Architecture and Properties in Brucella ovis PA. Front. Vet. Sci., 8.","DOI":"10.3389\/fvets.2021.814752"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1070","DOI":"10.1111\/mmi.12242","article-title":"The ferrous iron transporter FtrABCD is required for the virulence of Brucella abortus 2308 in mice","volume":"88","author":"Elhassanny","year":"2013","journal-title":"Mol. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Yuan, J.S., Reed, A., Chen, F., and Stewart, C.N. (2006). Statistical analysis of real-time PCR data. BMC Bioinform., 7.","DOI":"10.1186\/1471-2105-7-85"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.vetmic.2008.12.003","article-title":"Analysis of the occurrence and distribution of the Omp25\/Omp31 family of surface proteins in the six classical Brucella species","volume":"137","author":"Sancho","year":"2009","journal-title":"Vet. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1794","DOI":"10.1021\/pr101065j","article-title":"Andromeda: A peptide search engine integrated into the MaxQuant environment","volume":"10","author":"Cox","year":"2011","journal-title":"J. Proteome Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1038\/nbt.1511","article-title":"MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification","volume":"26","author":"Cox","year":"2008","journal-title":"Nat. Biotechnol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1038\/nature10098","article-title":"Global quantification of mammalian gene expression control","volume":"473","author":"Busse","year":"2011","journal-title":"Nature"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1186\/1297-9716-45-61","article-title":"Evaluation in mice of Brucella ovis attenuated mutants for use as live vaccines against B. ovis infection","volume":"45","author":"Sancho","year":"2014","journal-title":"Vet. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3503","DOI":"10.1128\/AEM.00299-16","article-title":"Agrobacterium tumefaciens Zur Regulates the High-Affinity Zinc Uptake System TroCBA and the Putative Metal Chaperone YciC, along with ZinT and ZnuABC, for Survival under Zinc-Limiting Conditions","volume":"82","author":"Chaoprasid","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"mfab046","DOI":"10.1093\/mtomcs\/mfab046","article-title":"COG0523 proteins: A functionally diverse family of transition metal-regulated G3E P-loop GTP hydrolases from bacteria to man","volume":"13","author":"Edmonds","year":"2021","journal-title":"Metallomics"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1016\/j.bpj.2024.03.010","article-title":"Coupling of zinc and GTP binding drives G-domain folding in Acinetobacter baumannii ZigA","volume":"123","author":"Osterberg","year":"2024","journal-title":"Biophys. J."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1111\/mmi.14956","article-title":"Histidine auxotroph mutant is defective for cell separation and allows the identification of crucial factors for cell division in Brucella abortus","volume":"118","author":"Roba","year":"2022","journal-title":"Mol. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1128\/JB.01124-09","article-title":"Metabolic control of virulence genes in Brucella abortus: HutC coordinates virB expression and the histidine utilization pathway by direct binding to both promoters","volume":"192","author":"Sieira","year":"2010","journal-title":"J. Bacteriol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2616","DOI":"10.1128\/JB.01650-14","article-title":"Acinetobacter baumannii response to host-mediated zinc limitation requires the transcriptional regulator Zur","volume":"196","author":"Mortensen","year":"2014","journal-title":"J. Bacteriol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Hood, M.I., Mortensen, B.L., Moore, J.L., Zhang, Y., Kehl-Fie, T.E., Sugitani, N., Chazin, W.J., Caprioli, R.M., and Skaar, E.P. (2012). Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog., 8.","DOI":"10.1371\/journal.ppat.1003068"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1039\/C7MT00126F","article-title":"Zinc transporters YbtX and ZnuABC are required for the virulence of Yersinia pestis in bubonic and pneumonic plague in mice","volume":"9","author":"Bobrov","year":"2017","journal-title":"Metallomics"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"7016","DOI":"10.1038\/s41467-021-27297-2","article-title":"Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut","volume":"12","author":"Behnsen","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1794","DOI":"10.1128\/IAI.71.4.1794-1803.2003","article-title":"Genetic organization and iron-responsive regulation of the Brucella abortus 2,3-dihydroxybenzoic acid biosynthesis operon, a cluster of genes required for wild-type virulence in pregnant cattle","volume":"71","author":"Bellaire","year":"2003","journal-title":"Infect. Immun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1099\/00221287-148-2-353","article-title":"Brucella abortus strain 2308 produces brucebactin, a highly efficient catecholic siderophore","volume":"148","author":"Sangari","year":"2002","journal-title":"Microbiology"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1186\/s13567-020-00824-7","article-title":"Disruption of pyruvate phosphate dikinase in Brucella ovis PA CO2-dependent and independent strains generates attenuation in the mouse model","volume":"51","author":"Iriarte","year":"2020","journal-title":"Vet. Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"6709","DOI":"10.1128\/JB.00680-06","article-title":"Transcriptional response of Escherichia coli to TPEN","volume":"188","author":"Sigdel","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0014-2999(03)02005-3","article-title":"N,N,N\u2019,N\u2019-tetrakis(2-pyridylmethyl)ethylenediamine inhibits ligand binding to certain G protein-coupled receptors","volume":"474","author":"Webster","year":"2003","journal-title":"Eur. J. Pharmacol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev.micro.112408.134247","article-title":"TonB-dependent transporters: Regulation, structure, and function","volume":"64","author":"Noinaj","year":"2010","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"7996","DOI":"10.1038\/ncomms8996","article-title":"The molecular mechanism of Zinc acquisition by the neisserial outer-membrane transporter ZnuD","volume":"6","author":"Calmettes","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"fuaa045","DOI":"10.1093\/femsre\/fuaa045","article-title":"The one hundred year journey of the genus Brucella (Meyer and Shaw 1920)","volume":"45","author":"Moreno","year":"2021","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2488","DOI":"10.1126\/science.1060331","article-title":"Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis","volume":"292","author":"Outten","year":"2001","journal-title":"Science"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"37517","DOI":"10.1074\/jbc.274.53.37517","article-title":"DNA distortion mechanism for transcriptional activation by ZntR, a Zn(II)-responsive MerR homologue in Escherichia coli","volume":"274","author":"Outten","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2719","DOI":"10.1016\/S0021-9258(18)89421-2","article-title":"Cytosolic Ca2+ homeostasis in Ehrlich and Yoshida carcinomas. A new, membrane-permeant chelator of heavy metals reveals that these ascites tumor cell lines have normal cytosolic free Ca2+","volume":"260","author":"Arslan","year":"1985","journal-title":"J. Biol. Chem."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.tvjl.2010.05.021","article-title":"Differences in the outer membrane-related properties of the six classical Brucella species","volume":"189","author":"Sancho","year":"2011","journal-title":"Vet. J."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Stranahan, L.W., and Arenas-Gamboa, A.M. (2021). When the Going Gets Rough: The Significance of Brucella Lipopolysaccharide Phenotype in Host-Pathogen Interactions. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.713157"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Silva, T.M., Mol, J.P., Winter, M.G., Atluri, V., Xavier, M.N., Pires, S.F., Paix\u00e3o, T.A., Andrade, H.M., Santos, R.L., and Tsolis, R.M. (2014). The predicted ABC transporter AbcEDCBA is required for type IV secretion system expression and lysosomal evasion by Brucella ovis. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0114532"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1016\/j.vetmic.2013.09.003","article-title":"Brucella ovis lacking a species-specific putative ATP-binding cassette transporter is attenuated but immunogenic in rams","volume":"167","author":"Silva","year":"2013","journal-title":"Vet. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"354649","DOI":"10.1155\/2009\/354649","article-title":"ATP-Binding Cassette Systems of Brucella","volume":"2009","author":"Jenner","year":"2009","journal-title":"Comp. Funct. Genom."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"28455","DOI":"10.1074\/jbc.M301415200","article-title":"The metal specificity and selectivity of ZntA from Escherichia coli using the acylphosphate intermediate","volume":"278","author":"Hou","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1007\/s10534-014-9763-2","article-title":"Deregulation of transition metals homeostasis is a key feature of cadmium toxicity in Salmonella","volume":"27","author":"Ammendola","year":"2014","journal-title":"BioMetals"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.micinf.2009.12.008","article-title":"Cholesterol, ganglioside GM1 and class A scavenger receptor contribute to infection by Brucella ovis and Brucella canis in murine macrophages","volume":"12","year":"2010","journal-title":"Microbes Infect."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/19\/1753\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T04:18:30Z","timestamp":1791087510000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/19\/1753"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,10,2]]},"references-count":70,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2026,10]]}},"alternative-id":["biology15191753"],"URL":"https:\/\/doi.org\/10.3390\/biology15191753","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,10,2]]}}}