Joint transcriptional control of virulence and resistance to antibiotic and environmental stress in acinetobacter baumannii

mBio

Volumn 6, Issue 6, 2015, Pages

  Gebhardt, Michael J ^a   Gallagher, Larry A ^b   Jacobson, Rachael K ^a   Usacheva, Elena A ^c   Peterson, Lance R ^c   Zurawski, Daniel V ^d   Shuman, Howard A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; APRAMYCIN; HYGROMYCIN; KANAMYCIN; TETRACYCLINE; TRANSCRIPTION FACTOR; ANTIINFECTIVE AGENT; TRANSPOSON;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BACTERIUM MUTANT; CONTROLLED STUDY; ENVIRONMENTAL STRESS; GALLERIA MELLONELLA; GENE IDENTIFICATION; GENE SEQUENCE; LARVA; MOLECULAR BIOLOGY; MULTIDRUG RESISTANCE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TRANSPOSON; ANIMAL; DNA SEQUENCE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LEPIDOPTERA; MICROBIOLOGY; VIRULENCE;

ACINETOBACTER BAUMANNII; ANIMALS; ANTI-BACTERIAL AGENTS; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; LARVA; LEPIDOPTERA; MUTAGENESIS, INSERTIONAL; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 84952845522     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01660-15     Document Type: Article

References (61)

1. Visca P, Seifert H, Towner KJ. 2011. Acinetobacter infection-an emerging threat to human health. IUBMB Life 63:1048-1054. http://dx.doi.org/ 10.1002/iub.534.
2. Spellberg B, Rex JH. 2013. The value of single-pathogen antibacterial agents. Nat Rev Drug Discov 12:963. http://dx.doi.org/10.1038/nrd3957-c1.
3. Göttig S, Gruber TM, Higgins PG, Wachsmuth M, Seifert H, Kempf VAJ. 2014. Detection of pan drug-resistant Acinetobacter baumannii in Germany. J Antimicrob Chemother 69:2578-2579. http://dx.doi.org/ 10.1093/jac/dku170.
4. Peleg AY, de Breij A, Adams MD, Cerqueira GM, Mocali S, Galardini M, Nibbering PH, Earl AM, Ward DV, Paterson DL, Seifert H, Dijkshoorn L. 2012. The success of Acinetobacter species; genetic, metabolic and virulence attributes. PLoS One 7:e46984. http://dx.doi.org/10.1371/ journal.pone.0046984.
5. Antunes LCS, Visca P, Towner KJ. 2014. Acinetobacter baumannii: evolution of a global pathogen. Pathog Dis 71:292-301. http://dx.doi.org/ 10.1111/2049-632X.12125.
6. Cox JS, Chen B, McNeil M, Jacobs WR, Jr. 1999. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402:79-83. http://dx.doi.org/10.1038/47042.
7. Slauch JM, Camilli A. 2000. IVET and RIVET: use of gene fusions to identify bacterial virulence factors specifically induced in host tissues. Methods Enzymol 326:73-96.
8. Gallagher LA, Shendure J, Manoil C. 2011. Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq. mBio 2:e00315-00310. http://dx.doi.org/10.1128/mBio.00315-10.
9. van Opijnen T, Bodi KL, Camilli A. 2009. Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nat Methods 6:767-772. http://dx.doi.org/10.1038/nmeth.1377.
10. van Opijnen T, Camilli A. 2013. Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms. Nat Rev Microbiol 11: 435-442. http://dx.doi.org/10.1038/nrmicro3033.
11. Wang N, Ozer EA, Mandel MJ, Hauser AR. 2014. Genome-wide identification of Acinetobacter baumannii genes necessary for persistence in the lung. mBio 5:e01163-01114. http://dx.doi.org/10.1128/mBio.01163-14.
12. Gallagher LA, Ramage E, Weiss EJ, Radey M, Hayden HS, Held KG, Huse HK, Zurawski DV, Brittnacher MJ, Manoil C. 2015. Resources for genetic and genomic analysis of emerging pathogen Acinetobacter baumannii. J Bacteriol 197:2027-2035. http://dx.doi.org/10.1128/JB.00131-15.
13. Jacobs AC, Thompson MG, Black CC, Kessler JL, Clark LP, McQueary CN, Gancz HY, Corey BW, Moon JK, Si Y, Owen MT, Hallock JD, Kwak YI, Summers A, Li CZ, Rasko DA, Penwell WF, Honnold CL, Wise MC, Waterman PE, Lesho EP, Stewart RL, Actis LA, Palys TJ, Craft DW, Zurawski DV. 2014. AB5075, a highly virulent isolate of Acinetobacter baumannii, as a model strain for the evaluation of pathogenesis and antimicrobial treatments. mBio 5:e01076-14. http://dx.doi.org/ 10.1128/mBio.01076-14.
14. Zurawski DV, Thompson MG, McQueary CN, Matalka MN, Sahl JW, Craft DW, Rasko DA. 2012. Genome sequences of four divergent multidrug-resistant Acinetobacter baumannii strains isolated from patients with sepsis or osteomyelitis. J Bacteriol 194:1619-1620. http:// dx.doi.org/10.1128/JB.06749-11.
15. Peleg AY, Jara S, Monga D, Eliopoulos GM, Moellering RC, Jr., Mylonakis E. 2009. Galleria mellonella as a model system to study Acinetobacter baumannii pathogenesis and therapeutics. Antimicrob Agents Chemother 53:2605-2609. http://dx.doi.org/10.1128/AAC.01533-08.
16. Boucher H, Talbot G, Bradley J, Edwards J, Gilbert D, Rice L, Scheld M, Spellberg B, Bartlett J. 2009. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48:1-12. http://dx.doi.org/10.1086/595011.
17. Wright MS, Haft DH, Harkins DM, Perez F, Hujer KM, Bajaksouzian S, Benard MF, Jacobs MR, Bonomo RA, Adams MD. 2014. New insights into dissemination and variation of the health care-associated pathogen Acinetobacter baumannii from genomic analysis. mBio 5:e00963-13. http://dx.doi.org/10.1128/mBio.00963-13.
18. Geisinger E, Isberg RR. 2015. Antibiotic modulation of capsular exopolysaccharide and virulence in Acinetobacter baumannii. PLoS Pathog 11: e1004691. http://dx.doi.org/10.1371/journal.ppat.1004691.
19. Roux D, Danilchanka O, Guillard T, Cattoir V, Aschard H, Fu Y, Angoulvant F, Messika J, Ricard J, Mekalanos JJ, Lory S, Pier GB, Skurnik D. 2015. Fitness cost of antibiotic susceptibility during bacterial infection. Sci Transl Med 7:297ra114. http://dx.doi.org/10.1126/ scitranslmed.aab1621.
20. Fuchs BB, O'Brien E, El Khoury JB, Mylonakis E. 2010. Methods for using Galleria mellonella as a model host to study fungal pathogenesis. Virulence 1:475-482. http://dx.doi.org/10.4161/viru.1.6.12985.
21. Kavanagh K, Reeves EP. 2004. Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev 28:101-112. http://dx.doi.org/10.1016/j.femsre.2003.09.002.
22. Jander G, Rahme LG, Ausubel FM. 2000. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182:3843-3845. http://dx.doi.org/10.1128/JB.182.13.3843-3845.2000.
23. Lionakis MS. 2011. Drosophila and Galleria insect model hosts: new tools for the study of fungal virulence, pharmacology and immunology. Virulence 2:521-527. http://dx.doi.org/10.4161/viru.2.6.18520.
24. Mukherjee K, Altincicek B, Hain T, Domann E, Vilcinskas A, Chakraborty T. 2010. Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol 76:310-317. http:// dx.doi.org/10.1128/AEM.01301-09.
25. Hood MI, Skaar EP. 2012. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10:525-537. http:// dx.doi.org/10.1038/nrmicro2836.
26. Gaddy JA, Arivett BA, McConnell MJ, Lopez-Rojas R, Pachon J, Actis LA. 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. http://dx.doi.org/10.1128/IAI.06279-11.
27. Zimbler DL, Penwell WF, Gaddy JA, Menke SM, Tomaras AP, Connerly PL, Actis LA. 2009. Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. Biometals 22:23-32. http:// dx.doi.org/10.1007/s10534-008-9202-3.
28. Hood MI, Mortensen BL, Moore JL, Zhang Y, Kehl-Fie TE, Sugitani N, Chazin WJ, Caprioli RM, Skaar EP. 2012. Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog 8:e1003068. http://dx.doi.org/10.1371/journal.ppat.1003068.
29. Mortensen BL, Rathi S, Chazin WJ, Skaar EP. 2014. Acinetobacter baumannii response to host-mediated zinc limitation requires the transcriptional regulator Zur. J Bacteriol 196:2616-2626. http://dx.doi.org/ 10.1128/JB.01650-14.
30. Campanini B, Pieroni M, Raboni S, Bettati S, Benoni R, Pecchini C, Costantino G, Mozzarelli A. 2015. Inhibitors of the sulfur assimilation pathway in bacterial pathogens as enhancers of antibiotic therapy. Curr Med Chem 22: 187-213. http://dx.doi. org/1 0. 2 1 7 4 / 0929867321666141112122553.
31. van der Ploeg J, Eichhorn E, Leisinger T. 2001. Sulfonate-sulfur metabolism and its regulation in Escherichia coli. Arch Microbiol 176:1-8. http://dx.doi.org/10.1007/s002030100298.
32. Wyatt GR, Loughheed TC, Wyatt SS. 1956. The chemistry of insect hemolymph; organic components of the hemolymph of the silkworm, Bombyx mori, and two other species. J Gen Physiol 39:853-868. http:// dx.doi.org/10.1085/jgp.39.6.853.
33. Álvarez R, Neumann G, Frávega J, Díaz F, Tejías C, Collao B, Fuentes JA, Paredes-Sabja D, Calderón IL, Gil F. 2015. CysB-dependent upregulation of the Salmonella typhimurium cysJIH operon in response to antimicrobial compounds that induce oxidative stress. Biochem Biophys Res Commun 458:46-51 http://dx.doi.org/10.1016/j.bbrc.2015.01.058.
34. Turnbull AL, Surette MG. 2010. Cysteine biosynthesis, oxidative stress and antibiotic resistance in Salmonella typhimurium. Res Microbiol 161: 643-650. http://dx.doi.org/10.1016/j.resmic.2010.06.004.
35. Shatalin K, Shatalina E, Mironov A, Nudler E. 2011. H2S: a universal defense against antibiotics in bacteria. Science 334:986-990. http:// dx.doi.org/10.1126/science.1209855.
36. Cerqueira GM, Kostoulias X, Khoo C, Aibinu I, Qu Y, Traven A, Peleg AY. 2014. A global virulence regulator in Acinetobacter baumannii and its control of the phenylacetic acid catabolic pathway. J Infect Dis 210:46-55. http://dx.doi.org/10.1093/infdis/jiu024.
37. Russo T, MacDonald U, Beanan J, Olson R, MacDonald I, Sauberan S, Luke N, Schultz L, Umland T. 2009. Penicillin-binding protein 7/8 contributes to the survival of Acinetobacter baumannii in vitro and in vivo. J Infect Dis 199:513-521. http://dx.doi.org/10.1086/596317.
38. May JM, Sherman DJ, Simpson BW, Ruiz N, Kahne D. 2015. Lipopolysaccharide transport to the cell surface: periplasmic transport and assembly into the outer membrane. Philos Trans R Soc Lond B Biol Sci 370: 20150027. http://dx.doi.org/10.1098/rstb.2015.0027.
39. Bos MP, Tommassen J. 2011. The LptD chaperone LptE is not directly involved in lipopolysaccharide transport in Neisseria meningitidis. J Biol Chem 286:28688-28696. http://dx.doi.org/10.1074/jbc.M111.239673.
40. Russo TA, Luke NR, Beanan JM, Olson R, Sauberan SL, MacDonald U, Schultz LW, Umland TC, Campagnari AA. 2010. The K1 capsular polysaccharide of Acinetobacter baumannii strain 307-0294 is a major virulence factor. Infect Immun 78:3993-4000. http://dx.doi.org/10.1128/ IAI.00366-10.
41. Krishnan N, Hyršl P, Šimek V. 2006. Nitric oxide production by hemocytes of larva and pharate prepupa of Galleria mellonella in response to bacterial lipopolysaccharide: cytoprotective or cytotoxic? Comp Biochem Physiol C Toxicol Pharmacol 142:103-110. http://dx.doi.org/10.1016/ j.cbpc.2005.10.016.
42. Kim B, Richards SM, Gunn JS, Slauch JM. 2010. Protecting against antimicrobial effectors in the phagosome allows SodCII to contribute to virulence in Salmonella enterica serovar Typhimurium. J Bacteriol 192: 2140-2149. http://dx.doi.org/10.1128/JB.00016-10.
43. Makinoshima H, Glickman MS. 2006. Site-2 proteases in prokaryotes: regulated intramembrane proteolysis expands to microbial pathogenesis. Microbes Infect 8:1882-1888. http://dx.doi.org/10.1016/ j.micinf.2006.02.021.
44. Micklinghoff JC, Schmidt M, Geffers R, Tegge W, Bange F. 2010. Analysis of expression and regulatory functions of the ribosome-binding protein TypA in Mycobacterium tuberculosis under stress conditions. Arch Microbiol 192:499-504. http://dx.doi.org/10.1007/s00203-010-0571-y.
45. Neidig A, Yeung AT, Rosay T, Tettmann B, Strempel N, Rueger M, Lesouhaitier O, Overhage J. 2013. TypA is involved in virulence, antimicrobial resistance and biofilm formation in Pseudomonas aeruginosa.BMC Microbiol 13:77. http://dx.doi.org/10.1186/1471-2180-13-77.
46. Kvint K, Nachin L, Diez A, Nyström T. 2003. The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 6:140-145. http://dx.doi.org/10.1016/S1369-5274(03)00025-0.
47. Yoon E, Nait Chabane Y, Goussard S, Snesrud E, Courvalin P, Dé E, Grillot-Courvalin C. 2015. Contribution of resistance-nodulation-cell division efflux systems to antibiotic resistance and biofilm formation in Acinetobacter baumannii. mBio 6:e00309-15. http://dx.doi.org/10.1128/ mBio.00309-15.
48. Damier-Piolle L, Magnet S, Bremont S, Lambert T, Courvalin P, Magnet S. 2008. AdeIJK, a resistance-nodulation-cell division pump effluxing multiple antibiotics in Acinetobacter baumannii. Antimicrob Agents Chemother 52:557-562. http://dx.doi.org/10.1128/AAC.00732-07.
49. Hassan KA, Liu Q, Henderson PJF, Paulsen IT. 2015. Homologs of the Acinetobacter baumannii AceI transporter represent a new family of bacterial multidrug efflux systems. mBio 6:e01982-14. http://dx.doi.org/ 10.1128/mBio.01982-14.
50. Liou M, Soo P, Ling S, Kuo H, Tang CY, Chang K. 2014. The sensor kinase BfmS mediates virulence in Acinetobacter baumannii. J Microbiol Immunol Infect 47:275-281. http://dx.doi.org/10.1016/j.jmii.2012.12.004.
51. Tomaras AP, Flagler MJ, Dorsey CW, Gaddy JA, Actis LA. 2008. Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology. Microbiology 154:3398-3409. http://dx.doi.org/10.1099/mic.0.2008/ 019471-0.
52. Ratajczak A, Geissdorfer W, Hillen W. 1998. Expression of alkane hydroxylase from Acinetobacter sp. strain ADP1 is induced by a broad range of n-alkanes and requires the transcriptional activator AlkR. J Bacteriol 180:5822-5827.
53. Kobayashi K, Fujikawa M, Kozawa T. 2014. Oxidative stress sensing by the iron-sulfur cluster in the transcription factor, SoxR. J Inorg Biochem 133:87-91. http://dx.doi.org/10.1016/j.jinorgbio.2013.11.008.
54. Rumbo-Feal S, Gómez MJ, Gayoso C, Álvarez-Fraga L, Cabral MP, Aransay AM, Rodríguez-Ezpeleta N, Fullaondo A, Valle J, Tomás M, Bou G, Poza M. 2013. Whole transcriptome analysis of Acinetobacter baumannii Assessed by RNA-sequencing reveals different mRNA expression profiles in biofilm compared to planktonic cells. PLoS One 8:e72968. http://dx.doi.org/10.1371/journal.pone.0072968.
55. CLSI. 2014. Performance standards for antimicrobial susceptibility testing; twenty-fourth informational Supplement. CLSI document M100-S24. Clinical and Laboratory Standards Institute, Wayne, PA.
56. Kawamura-Sato K, Wachino J, Kondo T, Ito H, Arakawa Y. 2010. Correlation between reduced susceptibility to disinfectants and multidrug resistance among clinical isolates of Acinetobacter species. J Antimicrob Chemother 65:1975-1983. http://dx.doi.org/10.1093/jac/dkq227.
57. Scott NE, Kinsella RL, Edwards AVG, Larsen MR, Dutta S, Saba J, Foster LJ, Feldman MF. 2014. Diversity within the O-linked protein glycosylation systems of Acinetobacter species. Mol Cell Proteomics 13: 2354-2370. http://dx.doi.org/10.1074/mcp.M114.038315.
58. Kessler D. 2006. Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol Rev 30:825-840. http:// dx.doi.org/10.1111/j.1574-6976.2006.00036.x.
59. Adams MD, Goglin K, Molyneaux N, Hujer KM, Lavender H, Jamison JJ, MacDonald IJ, Martin KM, Russo T, Campagnari AA, Hujer AM, Bonomo RA, Gill SR. 2008. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J Bacteriol 190:8053-8064. http://dx.doi.org/10.1128/JB.00834-08.
60. Jacobs AC, Thompson MG, Gebhardt M, Corey BW, Yildirim S, Shuman HA, Zurawski DV. 2014. Genetic manipulation of Acinetobacter baumannii. Curr Protoc Microbiol 35:6G.2.1-6G.2.11. http://dx.doi.org/ 10.1002/9780471729259.mc06g02s35.
61. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res 19:1639-1645 http://dx.doi.org/10.1101/ gr.092759.109.