Journal of Microbiology

, Volume 50, Issue 3, pp 434–443

Extracellular stress and lipopolysaccharide modulate Acinetobacter baumannii surface-associated motility

  • Christin N. McQueary
  • Benjamin C. Kirkup
  • Yuanzheng Si
  • Miriam Barlow
  • Luis A. Actis
  • David W. Craft
  • Daniel V. Zurawski
Articles

Abstract

Acinetobacter baumannii is a nosocomial bacterial pathogen, and infections attributed to this species are further complicated by a remarkable ability to acquire antimicrobial resistance genes and to survive in a desiccated state. While the antibiotic resistance and biofilm formation of A. baumannii is well-documented, less is known about the virulence attributes of this organism. Recent studies reported A. baumannii strains display a motility phenotype, which appears to be partially dependent upon Type IV pili, autoinducer molecules, and the response to blue light. In this study, we wanted to determine the prevalence of this trait in genetically diverse clinical isolates, and any additional required factors, and environmental cues that regulate motility. When strains are subjected to a wide array of stress conditions, A. baumannii motility is significantly reduced. In contrast, when extracellular iron is provided or salinity is reduced, motility is significantly enhanced. We further investigated whether the genes required for the production of lipopolysaccharide (lpsB) and K1 capsule (epsA/ptk) are required for motility as demonstrated in other Gram-negative bacteria. Transposon mutagenesis resulted in reduced motility by the insertion derivatives of each of these genes. The presence of the parental allele provided in trans, in the insertion mutant background, could only restore motility in the lpsB mutant. The production of core LPS directly contributes to the motility phenotype, while capsular polysaccharide may have an indirect effect. Further, the data suggest motility is regulated by extracellular conditions, indicating that A. baumannii is actively sensing the environment and responding accordingly.

Keywords

motility LPS swarming biofilm nosocomial pathogen extracellular stressors bacteria optical mapping 

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References

  1. Adams, M.D., Goglin, K., Molyneaux, N., Hujer, K.M., Lavender, H., Jamison, J.J., MacDonald, I.J., Martin, K.M., Russo, T., Campagnari, A.A., andet al. 2008. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J. Bacteriol.190, 8053–8064.PubMedCrossRefGoogle Scholar
  2. Adams, D., Yee, L., Rimmer, J.A., Williams, R., Martin, H., and Ovington, C. 2011. Investigation and management of an A. baumannii outbreak in ICU. Br. J. Nurs.20,140, 142, 144–147.Google Scholar
  3. Alarcon, I., Evans, D.J., and Fleiszig, S.M. 2009. The role of twitching motility in Pseudomonas aeruginosa exit from and translocation of corneal epithelial cells. Invest. Ophthalmol. Vis. Sci.50, 2237–2244.PubMedCrossRefGoogle Scholar
  4. Ali, A., Johnson, J.A., Franco, A.A., Metzger, D.J., Connell, T.D., Morris, J.G.Jr., and Sozhamannan, S. 2000. Mutations in the extracellular protein secretion pathway genes (eps) interfere with rugose polysaccharide production in and motility of Vibrio cholerae. Infect. Immun.68, 1967–1974.PubMedCrossRefGoogle Scholar
  5. Alsultan, A.A., Hamouda, A., Evans, B.A., and Amyes, S.G. 2009. Acinetobacter baumannii: emergence of four strains with novel bla (OXA-51-like) genes in patients with diabetes mellitus. J. Chemother.21, 290–295.PubMedGoogle Scholar
  6. Banin, E., Vasil, M.L., and Greenberg, E.P. 2005. Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. USA102, 11076–11081.PubMedCrossRefGoogle Scholar
  7. Beavers, S.F., Blossom, D.B., Wiemken, T.L., Kawaoka, K.Y., Wong, A., Goss, L., McCormick, M.I., Thoroughman, D., and Srinivasan, A. 2009. Comparison of risk factors for recovery of Acinetobacter baumannii during outbreaks at two Kentucky hospitals, 2006. Public Health Rep.124, 868–874.PubMedGoogle Scholar
  8. Brisou, J. 1953. Essay on the system of the genus Achromobacter. Ann. Inst. Pasteur (Paris)84, 812–814.Google Scholar
  9. Burrows, L.L. 2005. Weapons of mass retraction. Mol. Microbiol.57, 878–888.PubMedCrossRefGoogle Scholar
  10. Butler, M.T., Wang, Q., and Harshey, R.M. 2010. Cell density and mobility protect swarming bacteria against antibiotics. Proc. Natl. Acad. Sci. USA107, 3776–3781.PubMedCrossRefGoogle Scholar
  11. Caiazza, N.C., Shanks, R.M., and O’Toole, G.A. 2005. Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J. Bacteriol.187, 7351–7361.PubMedCrossRefGoogle Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. Chang, H.L., Tang, C.H., Hsu, Y.M., Wan, L., Chang, Y.F., Lin, C.T., Tseng, Y.R., Lin, Y.J., Sheu, J.J., Lin, C.W., andet al. 2009. Nosocomial outbreak of infection with multidrug-resistant Acinetobacter baumannii in a medical center in Taiwan. Infect. Control Hosp. Epidemiol.30, 34–38.PubMedCrossRefGoogle Scholar
  14. Chen, B.G., Turner, L., and Berg, H.C. 2007. The wetting agent required for swarming in Salmonella enterica serovar typhimurium is not a surfactant. J. Bacteriol.189, 8750–8753.PubMedCrossRefGoogle Scholar
  15. Choi, W.S., Kim, S.H., Jeon, E.G., Son, M.H., Yoon, Y.K., Kim, J.Y., Kim, M.J., Sohn, J.W., and Park, D.W. 2010. Nosocomial outbreak of carbapenem-resistant Acinetobacter baumannii in intensive care units and successful outbreak control program. J. Korean Med. Sci.25, 999–1004.PubMedCrossRefGoogle Scholar
  16. Choi, C.H., Lee, E.Y., Lee, Y.C., Park, T.I., Kim, H.J., Hyun, S.H., Kim, S.A., Lee, S.K., and Lee, J.C. 2005. Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells. Cell Microbiol.7, 1127–1138.PubMedCrossRefGoogle Scholar
  17. Cisneros, J.M. and Rodriguez-Bano, J. 2002. Nosocomial bacteremia due to Acinetobacter baumannii: epidemiology, clinical features and treatment. Clin. Microbiol. Infect.8, 687–693.PubMedCrossRefGoogle Scholar
  18. Clemmer, K.M., Bonomo, R.A., and Rather, P.N. 2011. Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology157, 2534–2544.PubMedCrossRefGoogle Scholar
  19. Cuthbertson, L., Mainprize, I.L., Naismith, J.H., and Whitfield, C. 2009. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in Gram-negative bacteria. Microbiol. Mol. Biol. Rev.73, 155–177.PubMedCrossRefGoogle Scholar
  20. D’Arezzo, S., Principe, L., Capone, A., Petrosillo, N., Petrucca, A., and Visca, P. 2011. Changing carbapenemase gene pattern in an epidemic multidrug-resistant Acinetobacter baumannii lineage causing multiple outbreaks in central Italy. J. Antimicrob. Chemother.66, 54–61.PubMedCrossRefGoogle Scholar
  21. Da Re, S. and Ghigo, J.M. 2006. A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J. Bacteriol.188, 3073–3087.PubMedCrossRefGoogle Scholar
  22. Dalla-Costa, L.M., Coelho, J.M., Souza, H.A., Castro, M.E., Stier, C.J., Bragagnolo, K.L., Rea-Neto, A., Penteado-Filho, S.R., Livermore, D.M., and Woodford, N. 2003. Outbreak of carbapenem-resistant Acinetobacter baumannii producing the OXA-23 enzyme in Curitiba, Brazil. J. Clin. Microbiol.41, 3403–3406.PubMedCrossRefGoogle Scholar
  23. Dallo, S.F. and Weitao, T. 2010. Insights into Acinetobacter war-wound infections, biofilms, and control. Adv. Skin Wound Care23, 169–174.PubMedCrossRefGoogle Scholar
  24. Dijkshoorn, L., Nemec, A., and Seifert, H. 2007. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat. Rev. Microbiol.5, 939–951.PubMedCrossRefGoogle Scholar
  25. Dixon, B. 2008. There’s the rub: infection control that spreads infection. Lancet Infect. Dis.8, 91–91.PubMedCrossRefGoogle Scholar
  26. Eijkelkamp, B.A., Hassan, K.A., Paulsen, I.T., and Brown, M.H. 2011. Investigation of the human pathogen Acinetobacter baumannii under iron limiting conditions. BMC Genomics12, 126.PubMedCrossRefGoogle Scholar
  27. Ellison, R.T.3rd, Giehl, T.J., and LaForce, F.M. 1988. Damage of the outer membrane of enteric Gram-negative bacteria by lactoferrin and transferrin. Infect. Immun.56, 2774–2781.PubMedGoogle Scholar
  28. Falagas, M.E., Karveli, E.A., Kelesidis, I., and Kelesidis, T. 2007. Community-acquired Acinetobacter infections. Eur. J. Clin. Microbiol. Infect. Dis.26, 857–868.PubMedCrossRefGoogle Scholar
  29. Firehammer, B.D. 1987. Inhibition of growth and swarming of Proteus mirabilis and Proteus vulgaris by triclosan. J. Clin. Microbiol.25, 1312–1313.PubMedGoogle Scholar
  30. Fong, J.C., Syed, K.A., Klose, K.E., and Yildiz, F.H. 2010. Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology156, 2757–2769.PubMedCrossRefGoogle Scholar
  31. Forbes, S.J., Eschmann, M., and Mantis, N.J. 2008. Inhibition of Salmonella enterica serovar typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immun.76, 4137–4144.PubMedCrossRefGoogle Scholar
  32. Forman, H.J. and Torres, M. 2001. Redox signaling in macrophages. Mol. Aspects Med.22, 189–216.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. Gootz, T.D. and Marra, A. 2008. Acinetobacter baumannii: an emerging multidrug-resistant threat. Expert Rev. Anti. Infect. Ther.6, 309–325.PubMedCrossRefGoogle Scholar
  35. Guerrero, D.M., Perez, F., Conger, N.G., Solomkin, J.S., Adams, M.D., Rather, P.N., and Bonomo, R.A. 2010. Acinetobacter baumannii-associated skin and soft tissue infections: recognizing a broadening spectrum of disease. Surg. Infect. (Larchmt)11, 49–57.CrossRefGoogle Scholar
  36. Halvorsen, J.F. 1963. Gliding Motility in the Organisms Bacterium anitratum (B5w), Moraxella lwoffi and Alkaligenes haemolysans, as compared to Moraxella nonliquefaciens. Acta. Pathol. Microbiol. Scand.59, 200–204.PubMedCrossRefGoogle Scholar
  37. Heilmann, C., Gerke, C., Perdreau-Remington, F., and Gotz, F. 1996. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect. Immun.64, 277–282.PubMedGoogle Scholar
  38. Hod, E.A., Zhang, N., Sokol, S.A., Wojczyk, B.S., Francis, R.O., Ansaldi, D., Francis, K.P., Della-Latta, P., Whittier, S., Sheth, S., andet al. 2010. Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood115, 4284–4292.PubMedCrossRefGoogle Scholar
  39. Hood, M.I., Jacobs, A.C., Sayood, K., Dunman, P.M., and Skaar, E.P. 2010. Acinetobacter baumannii increases tolerance to antibiotics in response to monovalent cations. Antimicrob. Agents Chemother.54, 1029–1041.PubMedCrossRefGoogle Scholar
  40. Huang, T.P., Somers, E.B., and Wong, A.C. 2006. Differential biofilm formation and motility associated with lipopolysaccharide/ exopolysaccharide-coupled biosynthetic genes in Stenotrophomonas maltophilia. J. Bacteriol.188, 3116–3120.PubMedCrossRefGoogle Scholar
  41. Jacobs, A.C., Hood, I., Boyd, K.L., Olson, P.D., Morrison, J.M., Carson, S., Sayood, K., Iwen, P.C., Skaar, E.P., and Dunman, P.M. 2010. Inactivation of phospholipase D diminishes Acinetobacter baumannii pathogenesis. Infect. Immun.78, 1952–1962.PubMedCrossRefGoogle Scholar
  42. Jamieson, W.D., Pehl, M.J., Gregory, G.A., and Orwin, P.M. 2009. Coordinated surface activities in Variovorax paradoxus EPS. BMC Microbiol.9, 124.PubMedCrossRefGoogle Scholar
  43. Joly-Guillou, M.L. 2005. Clinical impact and pathogenicity of Acinetobacter. Clin. Microbiol. Infect.11, 868–873.PubMedCrossRefGoogle Scholar
  44. Karthikeyan, K., Thirunarayan, M.A., and Krishnan, P. 2010. Coexistence of blaOXA-23 with blaNDM-1 and armA in clinical isolates of Acinetobacter baumannii from India. J. Antimicrob. Chemother.65, 2253–2254.PubMedCrossRefGoogle Scholar
  45. Kearns, D.B. and Losick, R. 2003. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol.49, 581–590.PubMedCrossRefGoogle Scholar
  46. Ko, K.S., Suh, J.Y., Kwon, K.T., Jung, S.I., Park, K.H., Kang, C.I., Chung, D.R., Peck, K.R., and Song, J.H. 2007. High rates of resistance to colistin and polymyxin B in subgroups of Acinetobacter baumannii isolates from Korea. J. Antimicrob. Chemother.60, 1163–1167.PubMedCrossRefGoogle Scholar
  47. La Forgia, C., Franke, J., Hacek, D.M., Thomson, R.B.Jr., Robicsek, A., and Peterson, L.R. 2010. Management of a multidrug-resistant Acinetobacter baumannii outbreak in an intensive care unit using novel environmental disinfection: a 38-month report. Am. J. Infect. Control38, 259–263.PubMedCrossRefGoogle Scholar
  48. Lancero, H., Caberoy, N.B., Castaneda, S., Li, Y., Lu, A., Dutton, D., Duan, X.Y., Kaplan, H.B., Shi, W., and Garza, A.G. 2004. Characterization of a Myxococcus xanthus mutant that is defective for adventurous motility and social motility. Microbiology150, 4085–4093.PubMedCrossRefGoogle Scholar
  49. Lee, J., Bansal, T., Jayaraman, A., Bentley, W.E., and Wood, T.K. 2007. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl. Environ. Microbiol.73, 4100–4109.PubMedCrossRefGoogle Scholar
  50. Letunic, I. and Bork, P. 2011. Interactive tree of life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res.39, W475–478.PubMedCrossRefGoogle Scholar
  51. Lindberg, R.B., Wetzler, T.F., Newton, A., Howard, J.M., Davis, J.H., and Strawitz, J. 1955. The bacterial flora of the blood stream in the Korean battle casualty. Ann. Surg.141, 366–368.PubMedCrossRefGoogle Scholar
  52. Lindum, P.W., Anthoni, U., Christophersen, C., Eberl, L., Molin, S., and Givskov, M. 1998. N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J. Bacteriol.180, 6384–6388.PubMedGoogle Scholar
  53. Liu, J.B., Tang, T.S., and Xiao, D.S. 2004. Changes of free iron contents and its correlation with lipid peroxidation after experimental spinal cord injury. Chin. J. Traumatol.7, 229–232.PubMedGoogle Scholar
  54. Loehfelm, T.W., Luke, N.R., and Campagnari, A.A. 2008. Identification and characterization of an Acinetobacter baumannii biofilm-associated protein. J. Bacteriol.190, 1036–1044.PubMedCrossRefGoogle Scholar
  55. Luke, N.R., Sauberan, S.L., Russo, T.A., Beanan, J.M., Olson, R., Loehfelm, T.W., Cox, A.D., St Michael, F., Vinogradov, E.V., and Campagnari, A.A. 2010. Identification and characterization of a glycosyltransferase involved in Acinetobacter baumannii lipopolysaccharide core biosynthesis. Infect. Immun.78, 2017–2023.PubMedCrossRefGoogle Scholar
  56. Marchaim, D., Navon-Venezia, S., Leavitt, A., Chmelnitsky, I., Schwaber, M.J., and Carmeli, Y. 2007. Molecular and epidemiologic study of polyclonal outbreaks of multidrug-resistant Acinetobacter baumannii infection in an Israeli hospital. Infect. Control Hosp. Epidemiol.28, 945–950.PubMedCrossRefGoogle Scholar
  57. Matsuyama, T., Bhasin, A., and Harshey, R.M. 1995. Mutational analysis of flagellum-independent surface spreading of Serratia marcescens 274 on a low-agar medium. J. Bacteriol.177, 987–991.PubMedGoogle Scholar
  58. McQueary, C.N. and Actis, L.A. 2011. Acinetobacter baumannii biofilms: Variations among strains and correlations with other cell properties. J. Microbiol.49, 243–250.PubMedCrossRefGoogle Scholar
  59. Miller, J. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold spring Harbor, New York, N.Y., USA.Google Scholar
  60. Montefour, K., Frieden, J., Hurst, S., Helmich, C., Headley, D., Martin, M., and Boyle, D.A. 2008. Acinetobacter baumannii: an emerging multidrug-resistant pathogen in critical care. Crit. Care Nurse28, 15–25; quiz 26.PubMedGoogle Scholar
  61. Mussi, M.A., Gaddy, J.A., Cabruja, M., Arivett, B.A., Viale, A.M., Rasia, R., and Actis, L.A. 2010. The opportunistic human pathogen Acinetobacter baumannii senses and responds to light. J. Bacteriol.192, 6336–6345.PubMedCrossRefGoogle Scholar
  62. 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. Proteomics74, 44–58.PubMedCrossRefGoogle Scholar
  63. O’Toole, G.A. and Kolter, R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol.30, 295–304.PubMedCrossRefGoogle Scholar
  64. Park, Y.K., Choi, J.Y., Shin, D., and Ko, K.S. 2011. Correlation between overexpression and amino acid substitution of the PmrAB locus and colistin resistance in Acinetobacter baumannii. Int. J. Antimicrob. Agents37, 525–530.PubMedCrossRefGoogle Scholar
  65. Patriquin, G.M., Banin, E., Gilmour, C., Tuchman, R., Greenberg, E.P., and Poole, K. 2008. Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J. Bacteriol.190, 662–671.PubMedCrossRefGoogle Scholar
  66. Peleg, A.Y., Seifert, H., and Paterson, D.L. 2008. Acinetobacter baumannii: emergence of a successful pathogen. Clin. Microbiol. Rev.21, 538–582.PubMedCrossRefGoogle Scholar
  67. Perez, F., Endimiani, A., Ray, A.J., Decker, B.K., Wallace, C.J., Hujer, K.M., Ecker, D.J., Adams, M.D., Toltzis, P., Dul, M.J., andet al. 2010. Carbapenem-resistant Acinetobacter baumannii and Klebsiella pneumoniae across a hospital system: impact of post-acute care facilities on dissemination. J. Antimicrob. Che mother.65, 1807–1818.CrossRefGoogle Scholar
  68. Petersen, K., Riddle, M.S., Danko, J.R., Blazes, D.L., Hayden, R., Tasker, S.A., and Dunne, J.R. 2007. Trauma-related infections in battlefield casualties from Iraq. Ann. Surg.245, 803–811.PubMedCrossRefGoogle Scholar
  69. Piskin, N., Celebi, G., Kulah, C., Mengeloglu, Z., and Yumusak, M. 2011. Activity of a dry mist-generated hydrogen peroxide disinfection system against methicillin-resistant Staphylococcus aureus and Acinetobacter baumannii. Am. J. Infect. Control.37, 525–530.Google Scholar
  70. Prates, C.G., Martins, A.F., Superti, S.V., Lopes, F.S., Ramos, F., Cantarelli, V.V., and Zavascki, A.P. 2011. Risk factors for 30-day mortality in patients with carbapenem-resistant Acinetobacter baumannii during an outbreak in an intensive care unit. Epidemiol. Infect.139, 411–418.PubMedCrossRefGoogle Scholar
  71. Rashid, M.H. and Kornberg, A. 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA97, 4885–4890.PubMedCrossRefGoogle Scholar
  72. Ray, A., Perez, F., Beltramini, A.M., Jakubowycz, M., Dimick, P., Jacobs, M.R., Roman, K., Bonomo, R.A., and Salata, R.A. 2010. Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital. Infect. Control Hosp. Epidemiol.31, 1236–1241.PubMedCrossRefGoogle Scholar
  73. Russo, T.A., Luke, N.R., Beanan, J.M., Olson, R., Sauberan, S.L., Macdonald, U., Schultz, L.W., Umland, T.C., and Campagnari, A.A. 2010. The K1 capsular polysaccharide of Acinetobacter baumannii 307-0294 is a major virulence factor. Infect. Immun.78, 3993–4000.PubMedCrossRefGoogle Scholar
  74. Russo, T.A., MacDonald, U., Beanan, J.M., Olson, R., MacDonald, I.J., Sauberan, S.L., Luke, N.R., Schultz, L.W., and Umland, T.C. 2009. Penicillin-binding protein 7/8 contributes to the survival of Acinetobacter baumannii in vitro and in vivo. J. Infect. Dis.199, 513–521.PubMedCrossRefGoogle Scholar
  75. Scott, P., Deye, G., Srinivasan, A., Murray, C., Moran, K., Hulten, E., Fishbain, J., Craft, D., Riddell, S., Lindler, L., andet al. 2007. An outbreak of multidrug-resistant Acinetobacter baumannii-calcoaceticus complex infection in the US military health care system associated with military operations in Iraq. Clin. Infect. Dis.44, 1577–1584.PubMedCrossRefGoogle Scholar
  76. Smith, M.G., Gianoulis, T.A., Pukatzki, S., Mekalanos, J.J., Ornston, L.N., Gerstein, M., and Snyder, M. 2007. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev.21, 601–614.PubMedCrossRefGoogle Scholar
  77. Stepanovic, S., Vukovic, D., Dakic, I., Savic, B., and Svabic-Vlahovic, M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods40, 175–179.PubMedCrossRefGoogle Scholar
  78. Strom, M.S. and Lory, S. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol.47, 565–596.PubMedCrossRefGoogle Scholar
  79. Toguchi, A., Siano, M., Burkart, M., and Harshey, R.M. 2000. Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide. J. Bacteriol.182, 6308–6321.PubMedCrossRefGoogle Scholar
  80. 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. Microbiology149, 3473–3484.PubMedCrossRefGoogle Scholar
  81. Tong, M.J. 1972. Septic complications of war wounds. JAMA219, 1044–1047.PubMedCrossRefGoogle Scholar
  82. Wakimoto, N., Nishi, J., Sheikh, J., Nataro, J.P., Sarantuya, J., Iwashita, M., Manago, K., Tokuda, K., Yoshinaga, M., and Kawano, Y. 2004. Quantitative biofilm assay using a microtiter plate to screen for enteroaggregative Escherichia coli. Am. J. Trop. Med. Hyg.71, 687–690.PubMedGoogle Scholar
  83. Yang, Z., Lux, R., Hu, W., Hu, C., and Shi, W. 2010. PilA localization affects extracellular polysaccharide production and fruiting body formation in Myxococcus xanthus. Mol. Microbiol.76, 1500–1513.PubMedCrossRefGoogle Scholar
  84. Yun, H.C., Branstetter, J.G., and Murray, C.K. 2008. Osteomyelitis in military personnel wounded in Iraq and Afghanistan. J. Trauma64, S163–168; discussion S168.PubMedCrossRefGoogle Scholar
  85. Zimbler, D.L., Penwell, W.F., Gaddy, J.A., Menke, S.M., Tomaras, A.P., Connerly, P.L., and Actis, L.A. 2009. Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. BioMetals22, 23–32.PubMedCrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Christin N. McQueary
    • 1
  • Benjamin C. Kirkup
    • 1
    • 2
  • Yuanzheng Si
    • 1
  • Miriam Barlow
    • 3
  • Luis A. Actis
    • 4
  • David W. Craft
    • 1
  • Daniel V. Zurawski
    • 1
  1. 1.Division of Bacterial and Rickettsial Disease, Department of Wound InfectionsWalter Reed Army Institute of ResearchSilver SpringUSA
  2. 2.Department of Medicine, Infectious Diseases DivisionUniformed Services University of the Health Sciences. F. Edward Hebert School of MedicineBethesdaUSA
  3. 3.School of Natural SciencesUniversity of CaliforniaMercedUSA
  4. 4.Department of MicrobiologyMiami UniversityOxfordUSA

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