{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T17:57:56Z","timestamp":1790618276761,"version":"4.1.0"},"reference-count":74,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2020,5,30]],"date-time":"2020-05-30T00:00:00Z","timestamp":1590796800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["DFG, SFB 958"],"award-info":[{"award-number":["DFG, SFB 958"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>Brucellosis is a zoonotic infection caused by bacteria of the genus Brucella. The species, B. abortus and B. melitensis, major causative agents of human brucellosis, share remarkably similar genomes, but they differ in their natural hosts, phenotype, antigenic, immunogenic, proteomic and metabolomic properties. In the present study, label-free quantitative proteomic analysis was applied to investigate protein expression level differences. Type strains and field strains were each cultured six times, cells were harvested at a midlogarithmic growth phase and proteins were extracted. Following trypsin digestion, the peptides were desalted, separated by reverse-phase nanoLC, ionized using electrospray ionization and transferred into an linear trap quadrapole (LTQ) Orbitrap Velos mass spectrometer to record full scan MS spectra (m\/z 300\u20131700) and tandem mass spectrometry (MS\/MS) spectra of the 20 most intense ions. Database matching with the reference proteomes resulted in the identification of 826 proteins. The Cluster of Gene Ontologies of the identified proteins revealed differences in bimolecular transport and protein synthesis mechanisms between these two strains. Among several other proteins, antifreeze proteins, Omp10, superoxide dismutase and 30S ribosomal protein S14 were predicted as potential virulence factors among the proteins differentially expressed. All mass spectrometry data are available via ProteomeXchange with identifier PXD006348.<\/jats:p>","DOI":"10.3390\/biom10060836","type":"journal-article","created":{"date-parts":[[2020,6,2]],"date-time":"2020-06-02T09:19:27Z","timestamp":1591089567000},"page":"836","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Pan-Proteomic Analysis and Elucidation of Protein Abundance among the Closely Related Brucella Species, Brucella abortus and Brucella melitensis"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1924-2988","authenticated-orcid":false,"given":"Jayaseelan","family":"Murugaiyan","sequence":"first","affiliation":[{"name":"Institute of Animal Hygiene and Environmental Health, Freie Universit\u00e4t Berlin, Centre for Infectious Medicine, Robert-von-Ostertag-Str. 7-13, 14163 Berlin, Germany"},{"name":"Department of Biotechnology, SRM University AP, Andhra Pradesh, Neerukonda, Mangalagiri, Guntur 522 502, India"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Murat","family":"Eravci","sequence":"additional","affiliation":[{"name":"Institute of Chemistry and Biochemistry, Freie Universit\u00e4t Berlin, Thielallee 63, 14195 Berlin, Germany"},{"name":"Sussex Neuroscience, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5507-4694","authenticated-orcid":false,"given":"Christoph","family":"Weise","sequence":"additional","affiliation":[{"name":"Institute of Chemistry and Biochemistry, Freie Universit\u00e4t Berlin, Thielallee 63, 14195 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Uwe","family":"Roesler","sequence":"additional","affiliation":[{"name":"Institute of Animal Hygiene and Environmental Health, Freie Universit\u00e4t Berlin, Centre for Infectious Medicine, Robert-von-Ostertag-Str. 7-13, 14163 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa D.","family":"Sprague","sequence":"additional","affiliation":[{"name":"Friedrich-Loeffler-Institute, Institute of Bacterial Infections and Zoonoses, Naumburger Str. 96a, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heinrich","family":"Neubauer","sequence":"additional","affiliation":[{"name":"Friedrich-Loeffler-Institute, Institute of Bacterial Infections and Zoonoses, Naumburger Str. 96a, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6259-1932","authenticated-orcid":false,"given":"Gamal","family":"Wareth","sequence":"additional","affiliation":[{"name":"Friedrich-Loeffler-Institute, Institute of Bacterial Infections and Zoonoses, Naumburger Str. 96a, 07743 Jena, Germany"},{"name":"Faculty of Veterinary Medicine, Benha University, Moshtohor, Toukh 13736, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,5,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3569","DOI":"10.1128\/jb.172.7.3569-3576.1990","article-title":"Brucella abortus 16S rRNA and lipid A reveal a phylogenetic relationship with members of the alpha-2 subdivision of the class Proteobacteria","volume":"172","author":"Moreno","year":"1990","journal-title":"J. Bacteriol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/1475-2859-5-13","article-title":"Brucella spp noncanonical LPS: Structure, biosynthesis, and interaction with host immune system","volume":"5","author":"Cardoso","year":"2006","journal-title":"Microb. Cell Fact."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"55","DOI":"10.4103\/0974-2727.72149","article-title":"Brucellosis: Review on the recent trends in pathogenicity and laboratory diagnosis","volume":"2","author":"Christopher","year":"2010","journal-title":"J. Lab. Physicians"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.1016\/j.meegid.2009.07.001","article-title":"Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens","volume":"9","author":"Whatmore","year":"2009","journal-title":"Infect. Genet. Evol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1099\/00207713-35-3-292","article-title":"Brucella, a Monospecific Genus as Shown by Deoxyribonucleic-Acid Hybridization","volume":"35","author":"Verger","year":"1985","journal-title":"Int. J. Syst. Bacteriol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Brenner, D., Krieg, N., Staley, J., and Garrity, G. (2005). Classification of Procaryotic Organisms and the Concept of Bacterial Speciation. Bergey\u2019s Manual\u00ae of Systematic Bacteriology, Springer US.","DOI":"10.1007\/0-387-28021-9_4"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"8353","DOI":"10.1128\/IAI.73.12.8353-8361.2005","article-title":"Whole-genome analyses of speciation events in pathogenic Brucellae","volume":"73","author":"Chain","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2715","DOI":"10.1128\/JB.187.8.2715-2726.2005","article-title":"Completion of the genome sequence of Brucella abortus and comparison to the highly similar genomes of Brucella melitensis and Brucella suis","volume":"187","author":"Halling","year":"2005","journal-title":"J. Bacteriol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6012","DOI":"10.1128\/JB.01483-12","article-title":"Genome sequences of three live attenuated vaccine strains of Brucella species and implications for pathogenesis and differential diagnosis","volume":"194","author":"Wang","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Singh, D.K., Kumar, A., Tiwari, A.K., Sankarasubramanian, J., Vishnu, U.S., Sridhar, J., Gunasekaran, P., and Rajendhran, J. (2015). Draft Genome Sequence of Brucella abortus Virulent Strain 544. Genome Announc., 3.","DOI":"10.1128\/genomeA.00419-15"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1073\/pnas.221575398","article-title":"The genome sequence of the facultative intracellular pathogen Brucella melitensis","volume":"99","author":"DelVecchio","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"5040","DOI":"10.1128\/JB.186.15.5040-5051.2004","article-title":"Comparative whole-genome hybridization reveals genomic islands in Brucella species","volume":"186","author":"Rajashekara","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1016\/S1286-4579(01)01427-7","article-title":"Classification of Brucella spp. isolated from marine mammals by DNA polymorphism at the omp2 locus","volume":"3","author":"Cloeckaert","year":"2001","journal-title":"Microbes. Infect. Inst. Pasteur"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/S0378-1135(02)00211-0","article-title":"Major outer membrane proteins of Brucella spp.: Past, present and future","volume":"90","author":"Cloeckaert","year":"2002","journal-title":"Vet. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Adone, R., Muscillo, M., La Rosa, G., Francia, M., and Tarantino, M. (2011). Antigenic, immunologic and genetic characterization of rough strains B. abortus RB51, B. melitensis B115 and B. melitensis B18. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0024073"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.molimm.2011.08.009","article-title":"Immunoproteomic analysis of Brucella melitensis and identification of a new immunogenic candidate protein for the development of brucellosis subunit vaccine","volume":"49","author":"Yang","year":"2011","journal-title":"Mol. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.jim.2005.11.003","article-title":"Immunoproteomic characterization of Brucella abortus 1119-3 preparations used for the serodiagnosis of Brucella infections","volume":"309","author":"Scholz","year":"2006","journal-title":"J. Immunol. Methods"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3619","DOI":"10.1016\/j.vaccine.2015.06.045","article-title":"An influenza viral vector Brucella abortus vaccine induces good cross-protection against Brucella melitensis infection in pregnant heifers","volume":"33","author":"Tabynov","year":"2015","journal-title":"Vaccine"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1186\/s13567-015-0199-7","article-title":"Recent advances in Brucella abortus vaccines","volume":"46","author":"Dorneles","year":"2015","journal-title":"Vet. Res."},{"key":"ref_20","first-page":"577","article-title":"Laboratory-based diagnosis of brucellosis\u2014A review of the literature. Part II: Serological tests for brucellosis","volume":"49","author":"Tomaso","year":"2003","journal-title":"Clin. Lab."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Al Dahouk, S., Scholz, H.C., Tomaso, H., Bahn, P., Gollner, C., Karges, W., Appel, B., Hensel, A., Neubauer, H., and Nockler, K. (2010). Differential phenotyping of Brucella species using a newly developed semi-automated metabolic system. BMC Microbiol., 10.","DOI":"10.1186\/1471-2180-10-269"},{"key":"ref_22","unstructured":"Baron, S. (1996). Brucella. Medical Microbiology, University of Texas Medical Branch at Galveston. [4th ed.]."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Wareth, G., Eravci, M., Weise, C., Roesler, U., Melzer, F., Sprague, L.D., Neubauer, H., and Murugaiyan, J. (2016). Comprehensive identification of immunodominant proteins of Brucella abortus and Brucella melitensis using antibodies in the sera from naturally infected hosts. Int. J. Mol. Sci., 17.","DOI":"10.3390\/ijms17050659"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/j.bbrc.2014.11.059","article-title":"Proteomics-based identification of immunodominant proteins of Brucellae using sera from infected hosts points towards enhanced pathogen survival during the infection","volume":"456","author":"Wareth","year":"2015","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3767","DOI":"10.1002\/pmic.200500730","article-title":"Proteomic analysis of Brucella abortus cell envelope and identification of immunogenic candidate proteins for vaccine development","volume":"6","author":"Connolly","year":"2006","journal-title":"Proteomics"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1016\/S0378-1135(02)00239-0","article-title":"Brucella proteomes\u2014A review","volume":"90","author":"DelVecchio","year":"2002","journal-title":"Vet. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1731","DOI":"10.1021\/pr060135p","article-title":"Comparative proteome analysis of laboratory grown Brucella abortus 2308 and Brucella melitensis 16M","volume":"5","author":"Eschenbrenner","year":"2006","journal-title":"J. Proteome Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4962","DOI":"10.1128\/JB.184.18.4962-4970.2002","article-title":"Comparative proteome analysis of Brucella melitensis vaccine strain Rev 1 and a virulent strain, 16M","volume":"184","author":"Eschenbrenner","year":"2002","journal-title":"J. Bacteriol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Lamontagne, J., Beland, M., Forest, A., Cote-Martin, A., Nassif, N., Tomaki, F., Moriyon, I., Moreno, E., and Paramithiotis, E. (2010). Proteomics-based confirmation of protein expression and correction of annotation errors in the Brucella abortus genome. BMC Genom., 11.","DOI":"10.1186\/1471-2164-11-300"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1111\/j.1749-6632.2002.tb04358.x","article-title":"Global analysis of Brucella melitensis proteomes","volume":"969","author":"Mujer","year":"2002","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2959","DOI":"10.1016\/j.jprot.2011.07.020","article-title":"Comparative proteome analysis of Brucella abortus 2308 and its virB type IV secretion system mutant reveals new T4SS-related candidate proteins","volume":"74","year":"2011","journal-title":"J. Proteom."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1002\/1615-9861(200208)2:8<1047::AID-PROT1047>3.0.CO;2-8","article-title":"Global analysis of the Brucella melitensis proteome: Identification of proteins expressed in laboratory-grown culture","volume":"2","author":"Wagner","year":"2002","journal-title":"Proteomics"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2347","DOI":"10.3389\/fmicb.2017.02347","article-title":"Relative Quantitative Proteomic Analysis of Brucella abortus Reveals Metabolic Adaptation to Multiple Environmental Stresses","volume":"8","author":"Zai","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Zai, X., Yang, Q., Liu, K., Li, R., Qian, M., Zhao, T., Li, Y., Yin, Y., Dong, D., and Fu, L. (2017). A comprehensive proteogenomic study of the human Brucella vaccine strain 104 M. BMC Genom., 18.","DOI":"10.1186\/s12864-017-3800-9"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/227680a0","article-title":"Cleavage of structural proteins during the assembly of the head of bacteriophage T4","volume":"227","author":"Laemmli","year":"1970","journal-title":"Nature"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1002\/elps.200305844","article-title":"Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis","volume":"25","author":"Candiano","year":"2004","journal-title":"Electrophoresis"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Murugaiyan, J., Eravci, M., Weise, C., and Roesler, U. (2016). Label-free quantitative proteomic analysis of harmless and pathogenic strains ofinfectious microalgae, Prototheca spp.. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18010059"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1021\/ac026117i","article-title":"Stop and go extraction tips for matrix-assisted laser desorption\/ionization, nanoelectrospray, and LC\/MS sample pretreatment in proteomics","volume":"75","author":"Rappsilber","year":"2003","journal-title":"Anal. Chem."},{"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":"698","DOI":"10.1038\/nprot.2009.36","article-title":"A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics","volume":"4","author":"Cox","year":"2009","journal-title":"Nat. Protoc."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.immuni.2010.01.013","article-title":"Quantitative proteomics reveals subset-specific viral recognition in dendritic cells","volume":"32","author":"Luber","year":"2010","journal-title":"Immunity"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2513","DOI":"10.1074\/mcp.M113.031591","article-title":"Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ","volume":"13","author":"Cox","year":"2014","journal-title":"Mol. Cell. Proteom."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate\u2014A practical and powerful approach to multiple testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. B Met."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"11033","DOI":"10.1093\/nar\/gkw880","article-title":"2016 update of the PRIDE database and its related tools","volume":"44","author":"Vizcaino","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1038\/nbt.2839","article-title":"ProteomeXchange provides globally coordinated proteomics data submission and dissemination","volume":"32","author":"Vizcaino","year":"2014","journal-title":"Nat. Biotechnol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"D286","DOI":"10.1093\/nar\/gkv1248","article-title":"eggNOG 4.5: A hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences","volume":"44","author":"Szklarczyk","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources","volume":"4","author":"Huang","year":"2009","journal-title":"Nat. Protoc."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/nar\/gkn923","article-title":"Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists","volume":"37","author":"Huang","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Garg, A., and Gupta, D. (2008). VirulentPred: A SVM based prediction method for virulent proteins in bacterial pathogens. BMC Bioinform., 9.","DOI":"10.1186\/1471-2105-9-62"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"D442","DOI":"10.1093\/nar\/gky1106","article-title":"The PRIDE database and related tools and resources in 2019: Improving support for quantification data","volume":"47","author":"Csordas","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_51","first-page":"823","article-title":"Metabolic characterization of Brucella strains that show conflicting identity by biochemical and serological methods","volume":"26","author":"Meyer","year":"1962","journal-title":"Bull. World Health Organ."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2","DOI":"10.3389\/fcimb.2012.00002","article-title":"Analyses of Brucella pathogenesis, host immunity, and vaccine targets using systems biology and bioinformatics","volume":"2","author":"He","year":"2012","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1002\/elps.1150180128","article-title":"Mapping and identification of Brucella melitensis proteins by two-dimensional electrophoresis and microsequencing","volume":"18","author":"Cloeckaert","year":"1997","journal-title":"Electrophoresis"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Crasta, O.R., Folkerts, O., Fei, Z., Mane, S.P., Evans, C., Martino-Catt, S., Bricker, B., Yu, G., Du, L., and Sobral, B.W. (2008). Genome sequence of Brucella abortus vaccine strain S19 compared to virulent strains yields candidate virulence genes. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002193"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1594","DOI":"10.1021\/pr800978p","article-title":"Intracellular adaptation of Brucella abortus","volume":"8","author":"Lamontagne","year":"2009","journal-title":"J. Proteome Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"6130","DOI":"10.1128\/JB.185.20.6130-6136.2003","article-title":"Molecular characterization of Brucella abortus chromosome II recombination","volume":"185","author":"Tsoktouridis","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2954","DOI":"10.1128\/IAI.68.5.2954-2961.2000","article-title":"Characterization of heat, oxidative, and acid stress responses in Brucella melitensis","volume":"68","author":"Cloeckaert","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"UniProt (2017). UniProt: The universal protein knowledgebase. Nucleic Acids Res., 45, D158\u2013D169.","DOI":"10.1093\/nar\/gkw1099"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Heberle, H., Meirelles, G.V., da Silva, F.R., Telles, G.P., and Minghim, R. (2015). InteractiVenn: A web-based tool for the analysis of sets through Venn diagrams. BMC Bioinform., 16.","DOI":"10.1186\/s12859-015-0611-3"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Silva, T.M.A., Mol, J.P.S., Winter, M.G., Atluri, V., Xavier, M.N., Pires, S.F., Paixao, 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_61","doi-asserted-by":"crossref","unstructured":"Jenner, D.C., Dassa, E., Whatmore, A.M., and Atkins, H.S. (2009). ATP-Binding Cassette Systems of Brucella. Comp. Funct. Genom., 354649.","DOI":"10.1155\/2009\/354649"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Smircich, P., Eastman, G., Bispo, S., Duhagon, M.A., Guerra-Slompo, E.P., Garat, B., Goldenberg, S., Munroe, D.J., Dallagiovanna, B., and Holetz, F. (2015). Ribosome profiling reveals translation control as a key mechanism generating differential gene expression in Trypanosoma cruzi. BMC Genom., 16.","DOI":"10.1186\/s12864-015-1563-8"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1128\/IAI.01097-12","article-title":"Diverse genetic regulon of the virulence-associated transcriptional regulator MucR in Brucella abortus 2308","volume":"81","author":"Caswell","year":"2013","journal-title":"Infect. Immun."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"5540","DOI":"10.1128\/IAI.70.10.5540-5546.2002","article-title":"Effect of omp10 or omp19 deletion on Brucella abortus outer membrane properties and virulence in mice","volume":"70","author":"Tibor","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Goolab, S., Roth, R.L., van Heerden, H., and Crampton, M.C. (2015). Analyzing the molecular mechanism of lipoprotein localization in Brucella. Front. Microbiol., 6.","DOI":"10.3389\/fmicb.2015.01189"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.micpath.2015.05.004","article-title":"Evaluation of the combined use of the recombinant Brucella abortus Omp10, Omp19 and Omp28 proteins for the clinical diagnosis of bovine brucellosis","volume":"83\u201384","author":"Simborio","year":"2015","journal-title":"Microb. Pathog."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"2873","DOI":"10.1128\/IAI.73.5.2873-2880.2005","article-title":"The Brucella abortus Cu,Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages an wild-type virulence in experimentally infected mice","volume":"73","author":"Gee","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"842","DOI":"10.1007\/s12275-010-0422-1","article-title":"Asc1p, a ribosomal protein, plays a pivotal role in cellular adhesion and virulence in Candida albicans","volume":"48","author":"Kim","year":"2010","journal-title":"J. Microbiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1007\/s12010-016-2076-x","article-title":"Immunogenicity analysis of a novel subunit vaccine candidate molecule-recombinant L7\/L12 ribosomal protein of Brucella suis","volume":"179","author":"Du","year":"2016","journal-title":"Appl. Biochem. Biotechnol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1111\/2049-632X.12079","article-title":"Identification of a protective protein from stationary-phase exoproteome of Brucella abortus","volume":"70","author":"Jain","year":"2014","journal-title":"Pathog. Dis."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1146\/annurev-micro-090110-102905","article-title":"Interactions of the human pathogenic Brucella Species with their hosts","volume":"65","author":"Atluri","year":"2011","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1038\/ng.2007.38","article-title":"Genomic analysis of Bartonella identifies type IV secretion systems as host adaptability factors","volume":"39","author":"Saenz","year":"2007","journal-title":"Nat. Genet."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/S0378-1135(02)00219-5","article-title":"Type IV secretion and Brucella virulence","volume":"90","author":"Boschiroli","year":"2002","journal-title":"Vet. Microbiol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3569","DOI":"10.1128\/JB.01767-08","article-title":"Analysis of ten Brucella genomes reveals evidence for horizontal gene transfer despite a preferred intracellular lifestyle","volume":"191","author":"Wattam","year":"2009","journal-title":"J. Bacteriol."}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/10\/6\/836\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:33:58Z","timestamp":1760175238000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/10\/6\/836"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,30]]},"references-count":74,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,6]]}},"alternative-id":["biom10060836"],"URL":"https:\/\/doi.org\/10.3390\/biom10060836","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,5,30]]}}}