The contribution of nutrient metal acquisition and metabolism to Acinetobacter baumannii survival within the host

Frontiers in Cellular and Infection Microbiology

Volumn 3, Issue DEC, 2013, Pages

  Mortensen, Brittany L ^a   Skaar, Eric P ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acinetobacter; Adherence; Iron; Pathogenesis; Persistence; Zinc

Indexed keywords

CALGRANULIN; CALGRANULIN A; CALGRANULIN B; FIBRONECTIN; IRON; NFUA PROTEIN; OUTER MEMBRANE PROTEIN A; PEPTIDES AND PROTEINS; PSORIASIN; UNCLASSIFIED DRUG; ZINC; METAL;

ACINETOBACTER BAUMANNII; CELL INVASION; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNITY; METAL METABOLISM; NONHUMAN; NUTRITIONAL PARAMETERS; REVIEW; ANIMAL; ENZYMOLOGY; HELICOBACTER INFECTION; HOMEOSTASIS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL; VERTEBRATE; ACINETOBACTER; ADHERENCE; PATHOGENESIS; PERSISTENCE;

ACINETOBACTER BAUMANNII; ANIMALS; BIOLOGICAL TRANSPORT; HELICOBACTER INFECTIONS; HOMEOSTASIS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METALS; MICROBIAL VIABILITY; VERTEBRATES;

ACINETOBACTER; ADHERENCE; IRON; PATHOGENESIS; PERSISTENCE; ZINC;

EID: 84897919153     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00095     Document Type: Review

References (120)

1. Actis, L. A., Tolmasky, M. E., Crosa, L. M., and Crosa, J. H. (1993). Effect of iron-limiting conditions on growth of clinical isolates of Acinetobacter baumannii. J. Clin. Microbiol. 31, 2812-2815.
2. Adams, M. D., Chan, E. R., Molyneaux, N. D., and Bonomo, R. A. (2010). Genomewide analysis of divergence of antibiotic resistance determinants in closely related isolates of Acinetobacter baumannii. Antimicrob. Agents Chemother. 54, 3569-3577. doi: 10.1128/AAC.00057-10.
3. Ammendola, S., Pasquali, P., Pistoia, C., Petrucci, P., Petrarca, P., Rotillio, G., et al. (2007). High-affinity Zn2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infect. Immun. 75, 5867-5876. doi: 10.1128/IAI.00559-07.
4. Angelini, S., Gerez, C., Ollagnier-de Choudens, S., Sanakis, Y., Fontecave, M., Barras, F., et al. (2008). NfuA, a new factor required for maturing Fe/S proteins in Escherichia coli under oxidative stress and iron starvation conditions. J. Biol. Chem. 283, 14084-14091. doi: 10.1074/jbc.M709405200.
5. Antunes, L. C., Imperi, F., Towner, K. J., and Visca, P. (2011). Genome-assisted identification of putative iron-utilization genes in Acinetobacter baumannii and their distribution among a genotypically diverse collection of clinical isolates. Res. Microbiol. 162, 279-284. doi: 10.1016/j.resmic.2010.10.010.
6. Armstrong, S. K., Pettis, G. S., Forrester, L. J., and McIntosh, M. A. (1989). The Escherichia coli enterobactin biosynthesis gene, entD: nucleotide sequence and membrane localization of its protein product. Mol. Microbiol. 3, 757-766. doi: 10.1111/j.1365-2958.1989.tb00224.x.
7. Aydemir, T. B., Liuzzi, J. P., McClellan, S., and Cousins, R. J. (2009). Zinc transporter ZIP8 (SLC39A8) and zinc influence IFN-gamma expression in activated human T cells. J. Leukoc. Biol. 86, 337-348. doi: 10.1189/jlb.1208759.
8. Bandyopadhyay, S., Chandramouli, K., and Johnson, M. K. (2008a). Iron-sulfur cluster biosynthesis. Biochem. Soc. Trans. 36, 1112-1119. doi: 10.1042/BST0361112.
9. Bandyopadhyay, S., Naik, S. G., O'Carroll, I. P., Huynh, B. H., Dean, D. R., Johnson, M. K., et al. (2008b). A proposed role for the Azotobacter vinelandii NfuA protein as an intermediate iron-sulfur cluster carrier. J. Biol. Chem. 283, 14092-14099. doi: 10.1074/jbc.M709161200.
10. Begum, N. A., Kobayashi, M., Moriwaki, Y., Matsumoto, M., Toyoshima, K., and Seya, T. (2002). Mycobacterium bovis BCG cell wall and lipopolysaccharide induce a novel gene, BIGM103, encoding a 7-TM protein: identification of a new protein family having Zn-transporter and Zn-metalloprotease signatures. Genomics 80, 630-645. doi: 10.1006/geno.2002.7000.
11. Bentancor, L. V., Camacho-Peiro, A., Bozkurt-Guzel, C., Pier, G. B., and Maira-Litran, T. (2012). Identification of Ata, a multifunctional trimeric autotransporter of Acinetobacter baumannii. J. Bacteriol. 194, 3950-3960. doi: 10.1128/JB.06769-11.
12. Bianchi, M., Niemiec, M. J., Siler, U., Urban, C. F., and Reichenbach, J. (2011). Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J. Allergy Clin. Immunol. 127, 1243-1252. doi: 10.1016/j.jaci.2011.01.021.
13. Brickman, T. J., and McIntosh, M. A. (1992). Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J. Biol. Chem. 267, 12350-12355.
14. Buchau, A. S., Hassan, M., Kukova, G., Lewerenz, V., Kellermann, S., Wurthner, J. U., et al. (2007). S100A15, an antimicrobial protein of the skin: regulation by E. coli through Toll-like receptor 4. J. Invest. Dermatol. 127, 2596-2604. doi: 10.1038/sj.jid.5700946.
15. Bury-Mone, S., Thiberge, J. M., Contreras, M., Maitournam, A., Labigne, A., and de Reuse, H. (2004). Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori. Mol. Microbiol. 53, 623-638. doi: 10.1111/j.1365-2958.2004.04137.x.
16. Calhoun, J. H., Murray, C. K., and Manring, M. M. (2008). Multidrug-resistant organisms in military wounds from Iraq and Afghanistan. Clin. Orthop. Relat. Res. 466, 1356-1362. doi: 10.1007/s11999-008-0212-9.
17. Camarena, L., Bruno, V., Euskirchen, G., Poggio, S., and Snyder, M. (2010). Molecular mechanisms of ethanol-induced pathogenesis revealed by RNA-sequencing. PLoS Pathog. 6:e1000834. doi: 10.1371/journal.ppat.1000834.
18. Campoy, S., Jara, M., Busquets, N., Perez de Rozas, A. M., Badiola, I., and Barbe, J. (2002). Role of the high-affinity zinc uptake znuABC system in Salmonella enterica serovar typhimurium virulence. Infect. Immun. 70, 4721-4725. doi: 10.1128/IAI.70.8.4721-4725.2002.
19. Cartron, M. L., Maddocks, S., Gillingham, P., Craven, C. J., and Andrews, S. C. (2006). Feo-transport of ferrous iron into bacteria. Biometals 19, 143-157. doi: 10.1007/s10534-006-0003-2.
20. Cellier, M. F., Courville, P., and Campion, C. (2007). Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect. 9, 1662-1670. doi: 10.1016/j.micinf.2007.09.006.
21. Chaturvedi, K. S., Hung, C. S., Crowley, J. R., Stapleton, A. E., and Henderson, J. P. (2012). The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat. Chem. Biol. 8, 731-736. doi: 10.1038/nchembio.1020.
22. Chimento, D. P., Kadner, R. J., and Wiener, M. C. (2003). The Escherichia coli outer membrane cobalamin transporter BtuB: structural analysis of calcium and substrate binding, and identification of orthologous transporters by sequence/structure conservation. J. Mol. Biol. 332, 999-1014. doi: 10.1016/j.jmb.2003.07.005.
23. Choi, C. H., Lee, E. Y., Lee, Y. C., Park, T. I., Kim, H. J., Hyun, S. H., et al. (2005). Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells. Cell. Microbiol. 7, 1127-1138. doi: 10.1111/j.1462-5822.2005.00538.x.
24. Choi, C. H., Lee, J. S., Lee, Y. C., Park, T. I., and Lee, J. C. (2008). Acinetobacter baumannii invades epithelial cells and outer membrane protein A mediates interactions with epithelial cells. BMC Microbiol. 8:216. doi: 10.1186/1471-2180-8-216.
25. Chu, B. C., Garcia-Herrero, A., Johanson, T. H., Krewulak, K. D., Lau, C. K., Peacock, R. S., et al. (2010). Siderophore uptake in bacteria and the battle for iron with the host; a bird's eye view. Biometals 23, 601-611. doi: 10.1007/s10534-010-9361-x.
26. Coderre, P. E., and Earhart, C. F. (1989). The entD gene of the Escherichia coli K12 enterobactin gene cluster. J. Gen. Microbiol. 135, 3043-3055. doi: 10.1099/00221287-135-11-3043.
27. Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., et al. (2008). Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965. doi: 10.1126/science.1152449.
28. Curtiss, R. 3rd., Wanda, S. Y., Gunn, B. M., Zhang, X., Tinge, S. A., Ananthnarayan, V., et al. (2009). Salmonella enterica serovar typhimurium strains with regulated delayed attenuation in vivo. Infect. Immun. 77, 1071-1082. doi: 10.1128/IAI.00693-08.
29. Dallo, S. F., Zhang, B., Denno, J., Hong, S., Tsai, A., Haskins, W., et al. (2012). Association of Acinetobacter baumannii EF-Tu with cell surface, outer membrane vesicles, and fibronectin. ScientificWorldJournal 2012, 128705. doi: 10.1100/2012/128705.
30. Damo, S. M., Kehl-Fie, T. E., Sugitani, N., Holt, M. E., Rathi, S., Murphy, W. J., et al. (2013). Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 110, 3841-3846. doi: 10.1073/pnas.1220341110.
31. Daniel, C., Haentjens, S., Bissinger, M. C., and Courcol, R. J. (1999). Characterization of the Acinetobacter baumannii Fur regulator: cloning and sequencing of the fur homolog gene. FEMS Microbiol. Lett. 170, 199-209. doi: 10.1016/S0378-1097(98)00533-3.
32. Davis, K. A., Moran, K. A., McAllister, C. K., and Gray, P. J. (2005). Multidrug-resistant Acinetobacter extremity infections in soldiers. Emerg. Infect. Dis. 11, 1218-1224. doi: 10.3201/eid1108.050103.
33. Davis, L. M., Kakuda, T., and DiRita, V. J. (2009). A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J. Bacteriol. 191, 1631-1640. doi: 10.1128/JB.01394-08.
34. de Breij, A., Dijkshoorn, L., Lagendijk, E., van der Meer, J., Koster, A., Bloemberg, G., et al. (2010). Do biofilm formation and interactions with human cells explain the clinical success of Acinetobacter baumannii? PLoS ONE 5:e10732. doi: 10.1371/journal.pone.0010732.
35. Dorsey, C. W., Beglin, M. S., and Actis, L. A. (2003a). Detection and analysis of iron uptake components expressed by Acinetobacter baumannii clinical isolates. J. Clin. Microbiol. 41, 4188-4193. doi: 10.1128/JCM.41.9.4188-4193.2003.
36. Dorsey, C. W., Tolmasky, M. E., Crosa, J. H., and Actis, L. A. (2003b). Genetic organization of an Acinetobacter baumannii chromosomal region harbouring genes related to siderophore biosynthesis and transport. Microbiology 149, 1227-1238. doi: 10.1099/mic.0.26204-0.
37. Dorsey, C. W., Tomaras, A. P., Connerly, P. L., Tolmasky, M. E., Crosa, J. H., and Actis, L. A. (2004). The siderophore-mediated iron acquisition systems of Acinetobacter baumannii ATCC 19606 and Vibrio anguillarum 775 are structurally and functionally related. Microbiology 150, 3657-3667. doi: 10.1099/mic.0.27371-0.
38. Doyle, J. S., Buising, K. L., Thursky, K. A., Worth, L. J., and Richards, M. J. (2011). Epidemiology of infections acquired in intensive care units. Semin. Respir. Crit. Care Med. 32, 115-138. doi: 10.1055/s-0031-1275525.
39. Echenique, J. R., Arienti, H., Tolmasky, M. E., Read, R. R., Staneloni, R. J., Crosa, J. H., et al. (1992). Characterization of a high-affinity iron transport system in Acinetobacter baumannii. J. Bacteriol. 174, 7670-7679.
40. Eijkelkamp, B. A., Hassan, K. A., Paulsen, I. T., and Brown, M. H. (2011a). Investigation of the human pathogen Acinetobacter baumannii under iron limiting conditions. BMC Genomics 12:126. doi: 10.1186/1471-2164-12-126.
41. Eijkelkamp, B. A., Stroeher, U. H., Hassan, K. A., Papadimitrious, M. S., Paulsen, I. T., Brown, M. H., et al. (2011b). Adherence and motility characteristics of clinical Acinetobacter baumannii isolates. FEMS Microbiol. Lett. 323, 44-51. doi: 10.1111/j.1574-6968.2011.02362.x.
42. Falagas, M. E., Karveli, E. A., Kelesidis, I., and Kelesidis, T. (2007). Community-acquired Acinetobacter infections. Eur. J. Clin. Microbiol. Infect. Dis. 26, 857-68. doi: 10.1007/s10096-007-0365-6.
43. Fournier, P. E., Vallenet, D., Barbe, V., Audic, S., Ogata, H., Poirel, L., et al. (2006). Comparative genomics of multidrug resistance in Acinetobacter baumannii. PLoS Genet. 2:e7. doi: 10.1371/journal.pgen.0020007.
44. Furrer, J. L., Sanders, D. N., Hook-Barnard, I. G., and McIntosh, M. A. (2002). Export of the siderophore enterobactin in Escherichia coli: involvement of a 43 kDa membrane exporter. Mol. Microbiol. 44, 1225-1234. doi: 10.1046/j.1365-2958.2002.02885.x.
45. Gaddy, J. A., Arivett, B. A., McConnell, M. J., Lopez-Rojas, R., Pachon, J., and Actis, L. A. (2012). 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. 80, 1015-1024. doi: 10.1128/IAI.06279-11.
46. Gaddy, J. A., Tomaras, A. P., and Actis, L. A. (2009). 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. 77, 3150-3160. doi: 10.1128/IAI.00096-09.
47. Gancz, H., Censini, S., and Merrell, D. S. (2006). Iron and pH homeostasis intersect at the level of Fur regulation in the gastric pathogen Helicobacter pylori. Infect. Immun. 74, 602-614. doi: 10.1128/IAI.74.1.602-614.2006.
48. Glaser, R., Harder, J., Lange, H., Bartels, J., Christophers, E., and Schroder, J. M. (2005). Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat. Immunol. 6, 57-64. doi: 10.1038/ni1142.
49. Goel, V. K., Kapil, A., Das, B., and Rao, D. N. (1998). Influence of iron on growth and extracellular products of Acinetobacter baumannii. Jpn. J. Med. Sci. Biol. 51, 25-33.
50. Hammer, N. D., and Skaar, E. P. (2011). Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu. Rev. Microbiol. 65, 129-147. doi: 10.1146/annurev-micro-090110-102851.
51. Hood, M. I., Mortensen, B. L., Moore, J. L., Zhang, Y., Kehl-Fie, T. E., Sugitani, N., et al. (2012). Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog. 8:e1003068. doi: 10.1371/journal.ppat.1003068.
52. Jabado, N., Jankowski, A., Dougaparsad, S., Picard, V., Grinstein, S., and Gros, P. (2000). Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J. Exp. Med. 192, 1237-1248. doi: 10.1084/jem.192.9.1237.
53. Jacobs, A. C., Hood, I., Boyd, K. L., Olson, P. D., Morrison, J. M., Carson, S., et al. (2010). Inactivation of phospholipase D diminishes Acinetobacter baumannii pathogenesis. Infect. Immun. 78, 1952-1962. doi: 10.1128/IAI.00889-09.
54. Kawamura-Sato, K., Wachino, J., Kondo, T., Ito, H., and Arakawa, Y. (2010). Correlation between reduced susceptibility to disinfectants and multidrug resistance among clinical isolates of Acinetobacter species. J. Antimicrob. Chemother. 65, 1975-1983. doi: 10.1093/jac/dkq227.
55. Kehl-Fie, T. E., Chitayat, S., Hood, M. I., Damo, S., Restrepo, N., Garcia, C., et al. (2011). Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10, 158-164. doi: 10.1016/j.chom.2011.07.004.
56. Kitamura, H., Morikawa, H., Kamon, H., Iguchi, M., Hojyo, S., Fukada, T., et al. (2006). Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat. Immunol. 7, 971-977. doi: 10.1038/ni1373.
57. Krewulak, K. D., and Vogel, H. J. (2011). TonB or not TonB: is that the question? Biochem. Cell Biol. 89, 87-97. doi: 10.1139/o10-141.
58. Kumar, P., Sannigrahi, S., and Tzeng, Y. L. (2012). The Neisseria meningitidis ZnuD zinc receptor contributes to interactions with epithelial cells and supports heme utilization when expressed in Escherichia coli. Infect. Immun. 80, 657-667. doi: 10.1128/IAI.05208-11.
59. Lee, H. W., Koh, Y. M., Kim, J., Lee, J. C., Lee, Y. C., Seol, S. Y., et al. (2008). Capacity of multidrug-resistant clinical isolates of Acinetobacter baumannii to form biofilm and adhere to epithelial cell surfaces. Clin. Microbiol. Infect. 14, 49-54. doi: 10.1111/j.1469-0691.2007.01842.x.
60. Lee, J. C., Koerten, H., van den Broek, P., Beekhuizen, H., Wolterbeek, R., van den Barselaar, M., et al. (2006). Adherence of Acinetobacter baumannii strains to human bronchial epithelial cells. Res. Microbiol. 157, 360-366. doi: 10.1016/j.resmic.2005.09.011.
61. Lee, K. C., and Eckert, R. L. (2007). S100A7 (Psoriasin)-mechanism of antibacterial action in wounds. J. Invest. Dermatol. 127, 945-957. doi: 10.1038/sj.jid.5700663.
62. Lewis, L. A., Gray, E., Wang, Y. P., Roe, B. A., and Dyer, D. W. (1997). Molecular characterization of hpuAB, the haemoglobin-haptoglobin-utilization operon of Neisseria meningitidis. Mol. Microbiol. 23, 737-749. doi: 10.1046/j.1365-2958.1997.2501619.x.
63. Li, W., He, J., Xie, L., Chen, T., and Xie, J. (2013). Comparative genomic insights into the biosynthesis and regulation of mycobacterial siderophores. Cell. Physiol. Biochem. 31, 1-13. doi: 10.1159/000343343.
64. Li, Y., Qiu, Y., Gao, H., Guo, Z., Han, Y., Song, Y., et al. (2009). Characterization of Zur-dependent genes and direct Zur targets in Yersinia pestis. BMC Microbiol. 9:128. doi: 10.1186/1471-2180-9-128.
65. Maciag, A., Dainese, E., Rodriguez, G. M., Milano, A., Provvedi, R., Pasca, M. R., et al. (2007). Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon. J. Bacteriol. 189, 730-740. doi: 10.1128/JB.01190-06.
66. May, J. J., Wendrich, T. M., and Marahiel, M. A. (2001). The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J. Biol. Chem. 276, 7209-7217. doi: 10.1074/jbc.M009140200.
67. McCormick, A., Heesemann, L., Wagener, J., Marcos, V., Hartl, D., Loeffler, J., et al. (2010). NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect. 12, 928-936. doi: 10.1016/j.micinf.2010.06.009.
68. Mey, A. R., Wyckoff, E. E., Kanukurthy, V., Fisher, C. R., and Payne, S. M. (2005). Iron and fur regulation in Vibrio cholerae and the role of fur in virulence. Infect. Immun. 73, 8167-8178. doi: 10.1128/IAI.73.12.8167-8178.2005.
69. Michalek, M., Gelhaus, C., Hecht, O., Podschun, R., Schroder, J. M., Leippe, M., et al. (2009). The human antimicrobial protein psoriasin acts by permeabilization of bacterial membranes. Dev. Comp. Immunol. 33, 740-746. doi: 10.1016/j.dci.2008.12.005.
70. T. Microbiology 150, 2587-2597. doi: 10.1099/mic.0.27141-0.
71. Moore, J. L., Becker, K. W., Nicklay, J. J., Boyd, K. L., Skaar, E. P., and Caprioli, R. M. (2013). Imaging mass spectrometry for assessing temporal proteomics: analysis of calprotectin in Acinetobacter baumannii pulmonary infection. Proteomics. doi: 10.1002/pmic.201300046. [Epub ahead of print].
72. Murakami, M., and Hirano, T. (2008). Intracellular zinc homeostasis and zinc signaling. Cancer Sci. 99, 1515-1522. doi: 10.1111/j.1349-7006.2008.00854.x.
73. Mussi, M. A., Gaddy, J. A., Cabruja, M., Arivett, B. A., Viale, A. M., Rasia, R., et al. (2010). The opportunistic human pathogen Acinetobacter baumannii senses and responds to light. J. Bacteriol. 192, 6336-6345. doi: 10.1128/JB.00917-10.
74. Nau, C. D., and Konisky, J. (1989). Evolutionary relationship between the TonB-dependent outer membrane transport proteins: nucleotide and amino acid sequences of the Escherichia coli colicin I receptor gene. J. Bacteriol. 171, 1041-1047.
75. Neely, A. N. (2000). A survey of gram-negative bacteria survival on hospital fabrics and plastics. J. Burn Care Rehabil. 21, 523-527. doi: 10.1097/00004630-200021060-00009.
76. Neugebauer, H., Herrmann, C., Kammer, W., Schwarz, G., Nordheim, A., and Braun, V. (2005). ExbBD-dependent transport of maltodextrins through the novel MalA protein across the outer membrane of Caulobacter crescentus. J. Bacteriol. 187, 8300-8311. doi: 10.1128/JB.187.24.8300-8311.2005.
77. Nwugo, C. C., Gaddy, J. A., Zimbler, D. L., and Actis, L. A. (2011). Deciphering the iron response in Acinetobacter baumannii: a proteomics approach. J. Proteomics 74, 44-58. doi: 10.1016/j.jprot.2010.07.010.
78. Parkhill, J., Wren, B. W., Thomson, N. R., Titball, R. W., Holden, M. T., Prentice, M. B., et al. (2001). Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523-527. doi: 10.1038/35097083.
79. Patzer, S. I., and Hantke, K. (1998). The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol. Microbiol. 28, 1199-1210. doi: 10.1046/j.1365-2958.1998.00883.x.
80. Pawlik, M. C., Hubert, K., Joseph, B., Claus, H., Schoen, C., and Vogel, U. (2012). The zinc-responsive regulon of Neisseria meningitidis comprises 17 genes under control of a Zur element. J. Bacteriol. 194, 6594-6603. doi: 10.1128/JB.01091-12.
81. Peleg, A. Y., Seifert, H., and Paterson, D. L. (2008). Acinetobacter baumannii: emergence of a successful pathogen. Clin. Microbiol. Rev. 21, 538-582. doi: 10.1128/CMR.00058-07.
82. Penwell, W. F., Arivett, B. A., and Actis, L. A. (2012). The Acinetobacter baumannii entA gene located outside the acinetobactin cluster is critical for siderophore production, iron acquisition and virulence. PLoS ONE 7:e36493. doi: 10.1371/journal.pone.0036493.
83. Peracino, B., Wagner, C., Balest, A., Balbo, A., Pergolizzi, B., Noegel, A. A., et al. (2006). Function and mechanism of action of Dictyostelium Nramp1 (Slc11a1) in bacterial infection. Traffic 7, 22-38. doi: 10.1111/j.1600-0854.2005.00356.x.
84. Pietzsch, J., and Hoppmann, S. (2009). Human S100A12: a novel key player in inflammation? Amino Acids 36, 381-389. doi: 10.1007/s00726-008-0097-7.
85. Pour, N. K., Dusane, D. H., Dhakephalkar, P. K., Zamin, F. R., Zinjarde, S. S., and Chopade, B. A. (2011). Biofilm formation by Acinetobacter baumannii strains isolated from urinary tract infection and urinary catheters. FEMS Immunol. Med. Microbiol. 62, 328-338. doi: 10.1111/j.1574-695X.2011.00818.x.
86. Proschak, A., Lubuta, P., Grun, P., Lohr, F., Wilharm, G., De Berardinis, V., et al. (2013). Structure and biosynthesis of fimsbactins A-F, siderophores from Acinetobacter baumannii and Acinetobacter baylyi. Chembiochem 14, 633-638. doi: 10.1002/cbic.201200764.
87. Py, B., Gerez, C., Angelini, S., Planel, R., Vinella, D., Loiseau, L., et al. (2012). Molecular organization, biochemical function, cellular role and evolution of NfuA, an atypical Fe-S carrier. Mol. Microbiol. 86, 155-171. doi: 10.1111/j.1365-2958.2012.08181.x.
88. Rakin, A., Schneider, L., and Podladchikova, O. (2012). Hunger for iron: the alternative siderophore iron scavenging systems in highly virulent Yersinia. Front. Cell. Infect. Microbiol. 2:151. doi: 10.3389/fcimb.2012.00151.
89. Robey, M., and Cianciotto, N. P. (2002). Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect. Immun. 70, 5659-6569. doi: 10.1128/IAI.70.10.5659-5669.2002.
90. Rowland, B. M., Grossman, T. H., Osburne, M. S., and Taber, H. W. (1996). Sequence and genetic organization of a Bacillus subtilis operon encoding 2,3-dihydroxybenzoate biosynthetic enzymes. Gene 178, 119-123. doi: 10.1016/0378-1119(96)00349-6.
91. Runyen-Janecky, L. J. (2013). Role and regulation of heme iron acquisition in gram-negative pathogens. Front. Cell. Infect. Microbiol. 3:55. doi: 10.3389/fcimb.2013.00055.
92. Runyen-Janecky, L. J., Reeves, S. A., Gonzales, E. G., and Payne, S. M. (2003). Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect. Immun. 71, 1919-1928. doi: 10.1128/IAI.71.4.1919-1928.2003.
93. Saha, R., Saha, N., Donofrio, R. S., and Bestervelt, L. L. (2013). Microbial siderophores: a mini review. J. Basic Microbiol. 53, 303-317. doi: 10.1002/jobm.201100552.
94. Sahl, J. W., Gillece, J. D., Schupp, J. M., Waddell, V. G., Driebe, E. M., Engelthaler, D. M., et al. (2013). Evolution of a pathogen: a comparative genomics analysis identifies a genetic pathway to pathogenesis in Acinetobacter. PLoS ONE 8:e54287. doi: 10.1371/journal.pone.0054287.
95. Sahl, J. W., Johnson, J. K., Harris, A. D., Phillippy, A. M., Hsiao, W. W., Thom, K. A., et al. (2011). Genomic comparison of multi-drug resistant invasive and colonizing Acinetobacter baumannii isolated from diverse human body sites reveals genomic plasticity. BMC Genomics 12:291. doi: 10.1186/1471-2164-12-291.
96. Schauer, K., Gouget, B., Carriere, M., Labigne, A., and de Reuse, H. (2007). Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol. Microbiol. 63, 1054-1068. doi: 10.1111/j.1365-2958.2006.05578.x.
97. Schroder, J., Jochmann, N., Rodionov, D. A., and Tauch, A. (2010). The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genomics 11:12. doi: 10.1186/1471-2164-11-12.
98. Sebeny, P. J., Riddle, M. S., and Petersen, K. (2008). Acinetobacter baumannii skin and soft-tissue infection associated with war trauma. Clin. Infect. Dis. 47, 444-449. doi: 10.1086/590568.
99. Smani, Y., Docobo-Perez, F., Lopez-Rojas, R., Dominguez-Herrera, J., Ibanez-Martinez, J., and Pachon, J. (2012a). Platelet-activating factor receptor initiates contact of Acinetobacter baumannii expressing phosphorylcholine with host cells. J. Biol. Chem. 287, 26901-26910. doi: 10.1074/jbc.M112.344556.
100. Smani, Y., McConnell, M. J., and Pachon, J. (2012b). Role of fibronectin in the adhesion of Acinetobacter baumannii to host cells. PLoS ONE 7:e33073. doi: 10.1371/journal.pone.0033073.
101. Smani, Y., Dominguez-Herrera, J., and Pachon, J. (2013). Association of the outer membrane protein Omp33with fitness and virulence of Acinetobacter baumannii. J. Infect. Dis. 10, 1561-1570. doi: 10.1093/infdis/jit386.
102. Stojiljkovic, I., Cobeljic, M., and Hantke, K. (1993). Escherichia coli K-12 ferrous iron uptake mutants are impaired in their ability to colonize the mouse intestine. FEMS Microbiol. Lett. 108, 111-115. doi: 10.1111/j.1574-6968.1993.tb06082.x.
103. Stork, M., Bos, M. P., Jongerius, I., de Kok, N., Schilders, I., Weynants, V. E., et al. (2010). An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Pathog. 6:e1000969. doi: 10.1371/journal.ppat.1000969.
104. Tamang, M. D., Kim, S., Kim, S. M., Kong, H. H., and Kim, J. (2011). Interaction of Acinetobacter baumannii 19606 and 1656-2 with Acanthamoeba castellanii. J. Microbiol. 49, 841-846. doi: 10.1007/s12275-011-1063-8.
105. Tomaras, A. P., Dorsey, C. W., Edelmann, R. E., and Actis, L. A. (2003). Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology 149, 3473-3484. doi: 10.1099/mic.0.26541-0.
106. Torres, V. J., Attia, A. S., Mason, W. J., Hood, M. I., Corbin, B. D., Beasley, F. C., et al. (2010). Staphylococcus aureus fur regulates the expression of virulence factors that contribute to the pathogenesis of pneumonia. Infect. Immun. 78, 1618-1628. doi: 10.1128/IAI.01423-09.
107. Troxell, B., and Hassan, H. M. (2013). Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front. Cell. Infect. Microbiol. 3:59. doi: 10.3389/fcimb.2013.00059.
108. Troxell, B., Sikes, M. L., Fink, R. C., Vazquez-Torres, A., Jones-Carson, J., and Hassan, H. M. (2011). Fur negatively regulates hns and is required for the expression of HilA and virulence in Salmonella enterica serovar Typhimurium. J. Bacteriol. 193, 497-505. doi: 10.1128/JB.00942-10.
109. Urban, C. F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., et al. (2009). Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5:e1000639. doi: 10.1371/journal.ppat.1000639.
110. Vallenet, D., Nordmann, P., Barbe, V., Poirel, L., Mangenot, S., Bataille, E., et al. (2008). Comparative analysis of Acinetobacters: three genomes for three lifestyles. PLoS ONE 3:e1805. doi: 10.1371/journal.pone.0001805.
111. Velayudhan, J., Castor, M., Richardson, A., Main-Hester, K. L., and Fang, F. C. (2007). The role of ferritins in the physiology of Salmonella enterica sv. Typhimurium: a unique role for ferritin B in iron-sulphur cluster repair and virulence. Mol. Microbiol. 63, 1495-1507. doi: 10.1111/j.1365-2958.2007.05600.x.
112. Velayudhan, J., Hughes, N. J., McColm, A. A., Bagshaw, J., Clayton, C. L., Andrews, S. C., et al. (2000). Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol. Microbiol. 37, 274-286. doi: 10.1046/j.1365-2958.2000.01987.x.
113. Vidal, R., Dominguez, M., Urrutia, H., Bello, H., Gonzalez, G., Garcia, A., et al. (1996). Biofilm formation by Acinetobacter baumannii. Microbios 86, 49-58.
114. Weinberg, E. D. (1975). Nutritional immunity. Host's attempt to withold iron from microbial invaders. JAMA 231, 39-41. doi: 10.1001/jama.231.1.39.
115. Wendt, C., Dietze, B., Dietz, E., and Ruden, H. (1997). Survival of Acinetobacter baumannii on dry surfaces. J. Clin. Microbiol. 35, 1394-1397.
116. Whitman, T. J. (2007). Infection control challenges related to war wound infections in the ICU setting. J. Trauma 62, S53. doi: 10.1097/TA.0b013e318065aa71.
117. Yamamoto, S., Okujo, N., and Sakakibara, Y. (1994). Isolation and structure elucidation of acinetobactin, a novel siderophore from Acinetobacter baumannii. Arch. Microbiol. 162, 249-254. doi: 10.1007/s002030050133.
118. Zimbler, D. L., Arivett, B. A., Beckett, A. C., Menke, S. M., and Actis, L. A. (2013). Functional features of TonB energy transduction systems of Acinetobacter baumannii. Infect. Immun. 81, 3382-3394. doi: 10.1128/IAI.00540-13.
119. Zimbler, D. L., Park, T. M., Arivett, B. A., Penwell, W. F., Greer, S. M., Woodruff, T. M., et al. (2012). Stress response and virulence functions of the Acinetobacter baumannii NfuA Fe-S scaffold protein. J. Bacteriol. 194, 2884-28893. doi: 10.1128/JB.00213-12.
120. Zimbler, D. L., Penwell, W. F., Gaddy, J. A., Menke, S. M., Tomaras, A. P., Connerly, P. L., et al. (2009). Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. Biometals 22, 23-32. doi: 10.1007/s10534-008-9202-3.