Pneumonia infection in mice reveals the involvement of the feoA gene in the pathogenesis of Acinetobacter baumannii

References

• Global priority list of antibiotic-resistant bacteria to guide research, discovery and development of new antibiotics. Geneva (Switzerland): World Health Organization. 2017.
   Google Scholar
• Peleg AY, Seifert H, Paterson DL. Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev. 2008;21:538–82. doi:10.1128/CMR.00058-07.
   PubMed Web of Science ®Google Scholar
• Maragakis LL, Perl TM. Acinetobacter baumannii: epidemiology, antimicrobial resistance, and treatment options. Clin Infect Dis. 2008;46:1254–63. doi:10.1086/529198.
   PubMed Web of Science ®Google Scholar
• Gales AC, Jones RN, Sader HS. Contemporary activity of colistin and polymyxin B against a worldwide collection of Gram-negative pathogens: results from the SENTRY Antimicrobial Surveillance Program (2006–09). J Antimicrob Chemother. 2011;66:2070–4. doi:10.1093/jac/dkr239.
   PubMed Web of Science ®Google Scholar
• Karaiskos I, Souli M, Galani I, et al. Colistin: still a lifesaver for the 21st century? Expert Opin Drug Metab Toxicol. 2017;13:59–71. doi:10.1080/17425255.2017.1230200.
   PubMed Web of Science ®Google Scholar
• Pournaras S, Koumaki V, Gennimata V, et al. In Vitro Activity of Tigecycline Against Acinetobacter baumannii: Global Epidemiology and Resistance Mechanisms. Adv Exp Med Biol. 2016;897:1–14.
   PubMed Web of Science ®Google Scholar
• Bou G, Cerveró G, Domínguez MA, et al. PCR-based DNA fingerprinting (REP-PCR, AP-PCR) and pulsed-field gel electrophoresis characterization of a nosocomial outbreak caused by imipenem- and meropenem-resistant Acinetobacter baumannii. Clin Microbiol Infect. 2000;6:635–43. doi:10.1046/j.1469-0691.2000.00181.x.
   PubMed Web of Science ®Google Scholar
• Higgins PG, Dammhayn C, Hackel M, et al. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother. 2010;65:233–8. doi:10.1093/jac/dkp428.
   PubMed Web of Science ®Google Scholar
• Valencia R, Arroyo LA, Conde M, et al. Nosocomial outbreak of infection with pan-drug-resistant Acinetobacter baumannii in a tertiary care university hospital. Infect Control Hosp Epidemiol. 2009;30:257–63. doi:10.1086/595977.
   PubMed Web of Science ®Google Scholar
• Corbella X, Montero A, Pujol M, et al. Emergence and rapid spread of carbapenem resistance during a large and sustained hospital outbreak of multiresistant Acinetobacter baumannii. J Clin Microbiol. 2000;38:4086–95.
   PubMed Web of Science ®Google Scholar
• McConnell MJ, Actis L, Pachón J. Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiol Rev. 2013;37:130–55. doi:10.1111/j.1574-6976.2012.00344.x.
   PubMed Web of Science ®Google Scholar
• Smani Y, Dominguez-Herrera J, Pachón J. Association of the outer membrane protein Omp33 with fitness and virulence of Acinetobacter baumannii. J Infect Dis. 2013;208:1561–70. doi:10.1093/infdis/jit386.
   PubMed Web of Science ®Google Scholar
• Lee JC, Koerten H, van den Broek P, et al. Adherence of Acinetobacter baumannii strains to human bronchial epithelial cells. Res Microbiol. 2006;157:360–6. doi:10.1016/j.resmic.2005.09.011.
   PubMed Web of Science ®Google Scholar
• Pérez A, Merino M, Rumbo-Feal S, et al. The FhaB/FhaC two-partner secretion system is involved in adhesion of Acinetobacter baumannii AbH12O-A2 strain. Virulence. 2017;8(6):959–974. doi:10.1080/21505594.
   Google Scholar
• Méndez JA, Mateos J, Beceiro A, et al. Quantitative proteomic analysis of host–pathogen interactions: a study of Acinetobacter baumannii responses to host airways. BMC Genomics. 2015;16:422. doi:10.1186/s12864-015-1608-z.
   PubMed Web of Science ®Google Scholar
• Merino M, Alvarez-Fraga L, Gomez MJ, et al. Complete Genome Sequence of the Multiresistant Acinetobacter baumannii Strain AbH12O-A2, Isolated during a Large Outbreak in Spain. Genome Announc. 2014;2: doi:10.1128/genomeA.01182-14.
   PubMedGoogle Scholar
• Acosta J, Merino M, Viedma E, et al. Multidrug-resistant Acinetobacter baumannii Harboring OXA-24 carbapenemase, Spain. Emerg Infect Dis. 2011;17:1064–7. doi:10.3201/eid/1706.091866.
   PubMed Web of Science ®Google Scholar
• Gaddy JA, Arivett BA, McConnell MJ, et al. Role of acinetobactin-mediated iron acquisition functions in the interaction of Acinetobacter baumannii strain ATCC 19606T with human lung epithelial cells, Galleria mellonella caterpillars, and mice. Infect Immun. 2012;80:1015–24. doi:10.1128/IAI.06279-11.
   PubMed Web of Science ®Google Scholar
• Mendez JA, Soares NC, Mateos J, et al. Extracellular proteome of a highly invasive multidrug-resistant clinical strain of Acinetobacter baumannii. J Proteome Res. 2012;11:5678–94. doi:10.1021/pr300496c.
   PubMed Web of Science ®Google Scholar
• Loehfelm TW, Luke NR, Campagnari AA. Identification and characterization of an Acinetobacter baumannii biofilm-associated protein. J Bacteriol. 2008;190:1036–44. doi:10.1128/JB.01416-07.
   PubMed Web of Science ®Google Scholar
• Choi AH, Slamti L, Avci FY, et al. The pgaABCD locus of Acinetobacter baumannii encodes the production of poly-beta-1–6-N-acetylglucosamine, which is critical for biofilm formation. J Bacteriol. 2009;191:5953–63. doi:10.1128/JB.00647-09.
   PubMed Web of Science ®Google Scholar
• Tomaras AP, Flagler MJ, Dorsey CW, et al. Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology. Microbiology. 2008;154:3398–409. doi:10.1099/mic.0.2008/019471-0.
   PubMed Web of Science ®Google Scholar
• Tomaras AP, Dorsey CW, Edelmann RE, et al. Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology. 2003;149:3473–84. doi:10.1099/mic.0.26541-0.
   PubMed Web of Science ®Google Scholar
• de Breij A, Gaddy J, van der Meer J, et al. CsuA/BABCDE-dependent pili are not involved in the adherence of Acinetobacter baumannii ATCC19606(T) to human airway epithelial cells and their inflammatory response. Res Microbiol. 2009;160:213–8. doi:10.1016/j.resmic.2009.01.002.
   PubMed Web of Science ®Google Scholar
• Gaddy JA, Tomaras AP, Actis LA. The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells. Infect Immun. 2009;77:3150–60. doi:10.1128/IAI.00096-09.
   PubMed Web of Science ®Google Scholar
• Dashper SG, Butler CA, Lissel JP, et al. A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J Biol Chem. 2005;280:28095–102. doi:10.1074/jbc.M503896200.
   PubMed Web of Science ®Google Scholar
• Nairz M, Schroll A, Sonnweber T, et al. The struggle for iron – a metal at the host-pathogen interface. Cell Microbiol. 2010;12:1691–702. doi:10.1111/j.1462-5822.2010.01529.x.
   PubMed Web of Science ®Google Scholar
• Chu BC, Garcia-Herrero A, Johanson TH, et al. Siderophore uptake in bacteria and the battle for iron with the host; a bird's eye view. Biometals. 2010;23:601–11. doi:10.1007/s10534-010-9361-x.
   PubMed Web of Science ®Google Scholar
• Proschak A, Lubuta P, Grun P, et al. Structure and biosynthesis of fimsbactins A-F, siderophores from Acinetobacter baumannii and Acinetobacter baylyi. Chembiochem. 2013;14:633–8. doi:10.1002/cbic.201200764.
   PubMed Web of Science ®Google Scholar
• Penwell WF, DeGrace N, Tentarelli S, et al. Discovery and Characterization of New Hydroxamate Siderophores, Baumannoferrin A and B, produced by Acinetobacter baumannii. Chembiochem. 2015;16:1896–1904. doi:10.1002/cbic.201500147.
   PubMed Web of Science ®Google Scholar
• Shapiro JA, Wencewicz TA. Acinetobactin Isomerization Enables Adaptive Iron Acquisition in Acinetobacter baumannii through pH-Triggered Siderophore Swapping. ACS Infect Dis. 2016;2:157–68. doi:10.1021/acsinfecdis.5b00145.
   PubMed Web of Science ®Google Scholar
• Weaver EA, Wyckoff EE, Mey AR, et al. FeoA and FeoC are essential components of the Vibrio cholerae ferrous iron uptake system, and FeoC interacts with FeoB. J Bacteriol. 2013;195:4826–35. doi:10.1128/JB.00738-13.
   PubMed Web of Science ®Google Scholar
• Naikare H, Palyada K, Panciera R, et al. Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun. 2006;74:5433–44. doi:10.1128/IAI.00052-06.
   PubMed Web of Science ®Google Scholar
• Mortensen BL, Skaar EP. The contribution of nutrient metal acquisition and metabolism to Acinetobacter baumannii survival within the host. Front Cell Infect Microbiol. 2013;3:95. doi:10.3389/fcimb.2013.00095.
   PubMed Web of Science ®Google Scholar
• Runyen-Janecky LJ, Reeves SA, Gonzales EG, et al. Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun. 2003;71:1919–28. doi:10.1128/IAI.71.4.1919-1928.2003.
   PubMed Web of Science ®Google Scholar
• Robey M, Cianciotto NP. Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect Immun. 2002;70:5659–69. doi:10.1128/IAI.70.10.5659-5669.2002.
   PubMed Web of Science ®Google Scholar
• Velayudhan J, Hughes NJ, McColm AA, et al. Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol Microbiol. 2000;37:274–86. doi:10.1046/j.1365-2958.2000.01987.x.
   PubMed Web of Science ®Google Scholar
• Stojiljkovic I, Cobeljic M, Hantke K. Escherichia coli K-12 ferrous iron uptake mutants are impaired in their ability to colonize the mouse intestine. FEMS Microbiol Lett. 1993;108:111–5. doi:10.1111/j.1574-6968.1993.tb06082.x.
   PubMed Web of Science ®Google Scholar
• Boyer E, Bergevin I, Malo D, et al. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect Immun. 2002;70:6032–42. doi:10.1128/IAI.70.11.6032-6042.2002.
   PubMed Web of Science ®Google Scholar
• Kammler M, Schön C, Hantke K. Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol. 1993;175:6212–9. doi:10.1128/jb.175.19.6212-6219.1993.
   PubMed Web of Science ®Google Scholar
• Stevenson B, Wyckoff EE, Payne SM. Vibrio cholerae FeoA, FeoB, and FeoC Interact To Form a Complex. J Bacteriol. 2016;198:1160–70. doi:10.1128/JB.00930-15.
   PubMed Web of Science ®Google Scholar
• Hantke K. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet. 1981;182:288–92. doi:10.1007/BF00269672.
   PubMedGoogle Scholar
• Hantke K. Ferrous Iron Transport, p 178–184. In: Crosa J, Mey A, Payne S, editors. Iron Transport in Bacteria. Washington, DC: ASM Press; 2004. doi:10.1128/9781555816544.ch12.
   Google Scholar
• Hantke K. Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism. Mol Gen Genet. 1987;210:135–9. doi:10.1007/BF00337769.
   PubMedGoogle Scholar
• Cartron ML, Maddocks S, Gillingham P, et al. Feo-transport of ferrous iron into bacteria. Biometals. 2006;19:143–57. doi:10.1007/s10534-006-0003-2.
   PubMed Web of Science ®Google Scholar
• Subashchandrabose S, Smith S, DeOrnellas V, et al. Acinetobacter baumannii Genes Required for Bacterial Survival during Bloodstream Infection. mSphere. 2015;1: doi:10.1128/mSphere.00013-15.
   PubMed Web of Science ®Google Scholar
• Antunes LC, Imperi F, Towner KJ, et al. Genome-assisted identification of putative iron-utilization genes in Acinetobacter baumannii and their distribution among a genotypically diverse collection of clinical isolates. Res Microbiol. 2011;162:279–84. doi:10.1016/j.resmic.2010.10.010.
   PubMed Web of Science ®Google Scholar
• Beceiro A, Tomas M, Bou G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin Microbiol Rev. 2013;26:185–230. doi:10.1128/CMR.00059-12.
   PubMed Web of Science ®Google Scholar
• Dorsey CW, Beglin MS, Actis LA. Detection and analysis of iron uptake components expressed by Acinetobacter baumannii clinical isolates. J Clin Microbiol. 2003;41:4188–93. doi:10.1128/JCM.41.9.4188-4193.2003.
   PubMed Web of Science ®Google Scholar
• Catel-Ferreira M, Marti S, Guillon L, et al. The outer membrane porin OmpW of Acinetobacter baumannii is involved in iron uptake and colistin binding. FEBS Lett. 2016;590:224–31. doi:10.1002/1873-3468.12050.
   PubMed Web of Science ®Google Scholar
• Catel-Ferreira M, Nehme R, Molle V, et al. Deciphering the function of the outer membrane protein OprD homologue of Acinetobacter baumannii. Antimicrob Agents Chemother. 2012;56:3826–32. doi:10.1128/AAC.06022-11.
   PubMed Web of Science ®Google Scholar
• Murray GL, Tsyganov K, Kostoulias XP, et al. Global gene expression profile of Acinetobacter baumannii during bacteremia. J Infect Dis. 2017;215:S52–7. doi:10.1093/infdis/jiw529.
   PubMed Web of Science ®Google Scholar
• Miethke M, Marahiel MA. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev. 2007;71:413–51. doi:10.1128/MMBR.00012-07.
   PubMed Web of Science ®Google Scholar
• Zimbler DL, Penwell WF, Gaddy JA, et al. Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. Biometals. 2009;22:23–32. doi:10.1007/s10534-008-9202-3.
   PubMed Web of Science ®Google Scholar
• Harding RA, Royt PW. Acquisition of iron from citrate by Pseudomonas aeruginosa. J Gen Microbiol. 1990;136:1859–67. doi:10.1099/00221287-136-9-1859.
   PubMedGoogle Scholar
• Ratledge C, Dover LG. Iron metabolism in pathogenic bacteria. Annu Rev Microbiol. 2000;54:881–941. doi:10.1146/annurev.micro.54.1.881.
   PubMed Web of Science ®Google Scholar
• Marshall B, Stintzi A, Gilmour C, et al. Citrate-mediated iron uptake in Pseudomonas aeruginosa: involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter. Microbiology. 2009;155:305–15. doi:10.1099/mic.0.023531-0.
   PubMed Web of Science ®Google Scholar
• Ganne G, Brillet K, Basta B, et al. Iron Release from the Siderophore Pyoverdine in Pseudomonas aeruginosa Involves Three New Actors: FpvC, FpvG, and FpvH. ACS Chem Biol. 2017;12:1056–65. doi:10.1021/acschembio.6b01077.
   PubMed Web of Science ®Google Scholar
• Louvel H, Saint Girons I, Picardeau M. Isolation and characterization of FecA- and FeoB-mediated iron acquisition systems of the spirochete Leptospira biflexa by random insertional mutagenesis. J Bacteriol. 2005;187:3249–54. doi:10.1128/JB.187.9.3249-3254.2005.
   PubMed Web of Science ®Google Scholar
• Sahl JW, Gillece JD, Schupp JM, et al. Evolution of a pathogen: a comparative genomics analysis identifies a genetic pathway to pathogenesis in Acinetobacter. PLoS One. 2013;8:e54287. doi:10.1371/journal.pone.0054287.
   PubMed Web of Science ®Google Scholar
• Rumbo-Feal S, Gomez MJ, Gayoso C, et al. Whole transcriptome analysis of Acinetobacter baumannii assessed by RNA-sequencing reveals different mRNA expression profiles in biofilm compared to planktonic cells. PLoS One. 2013;8:e72968. doi:10.1371/journal.pone.0072968.
   PubMed Web of Science ®Google Scholar
• Eijkelkamp BA, Hassan KA, Paulsen IT, et al. Investigation of the human pathogen Acinetobacter baumannii under iron limiting conditions. BMC genomics. 2011;12:126. doi:10.1186/1471-2164-12-126.
   PubMed Web of Science ®Google Scholar
• Miller AF. Superoxide dismutases: ancient enzymes and new insights. FEBS Lett. 2012;586:585–95. doi:10.1016/j.febslet.2011.10.048.
   PubMed Web of Science ®Google Scholar
• Lenski RE. Quantifying fitness and gene stability in microorganisms. Biotechnology. 1991;15:173–92.
   PubMedGoogle Scholar
• Madigan MT MJ, Dunlap PV, Clark DP. Brock biology of microorganisms. 12th ed. Texas, USA: Pearson Education Inc. 2009.
   Google Scholar
• Hassett DJ, Cohen MS. Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells. FASEB J. 1989;3:2574–82.
   PubMed Web of Science ®Google Scholar
• Rumbo-Feal S, Perez A, Ramelot TA, et al. Contribution of the A. baumannii A1S_0114 Gene to the Interaction with Eukaryotic Cells and Virulence. Front Cell Infect Microbiol. 2017;7:108. doi:10.3389/fcimb.2017.00108.
   PubMed Web of Science ®Google Scholar
• Álvarez-Fraga L, Pérez A, Rumbo-Feal S, et al. Analysis of the role of the LH92_11085 gene of a biofilm hyper-producing Acinetobacter baumannii strain on biofilm formation and attachment to eukaryotic cells. Virulence. 2016;7:443–55. doi:10.1080/21505594.2016.1145335.
   PubMed Web of Science ®Google Scholar
• Hamad MA, Zajdowicz SL, Holmes RK, et al. An allelic exchange system for compliant genetic manipulation of the select agents Burkholderia pseudomallei and Burkholderia mallei. Gene. 2009;430:123–31. doi:10.1016/j.gene.2008.10.011.
   PubMed Web of Science ®Google Scholar
• CLSI W, PA, USA. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically–Tenth Edition: Approved Standard M07-A10, 2015.
   Google Scholar
• Hornsey M, Longshaw C, Phee L, et al. In vitro activity of telavancin in combination with colistin versus Gram-negative bacterial pathogens. Antimicrob Agents Chemother. 2012;56:3080–5. doi:10.1128/AAC.05870-11.
   PubMed Web of Science ®Google Scholar
• Kaplan EL, Meier P. Nonparametric Estimation from Incomplete Observations. J Am Statist Assoc. 1958;53:457–81. doi:10.1080/01621459.1958.10501452.
   Web of Science ®Google Scholar
• Lopez-Rojas R, Dominguez-Herrera J, McConnell MJ, et al. Impaired virulence and in vivo fitness of colistin-resistant Acinetobacter baumannii. J Infect Dis. 2011;203:545–8. doi:10.1093/infdis/jiq086.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Hernandez MJ, Pachon J, Pichardo C, et al. Imipenem, doxycycline and amikacin in monotherapy and in combination in Acinetobacter baumannii experimental pneumonia. J Antimicrob Chemother. 2000;45:493–501. doi:10.1093/jac/45.4.493.
   PubMed Web of Science ®Google Scholar