Differential role of the T6SS in acinetobacter baumannii virulence

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Repizo, Guillermo D ^a   Gagné, Stéphanie ^a   Foucault Grunenwald, Marie Laure ^b   Borges, Vitor ^c   Charpentier, Xavier ^b   Limansky, Adriana S ^d   Gomes, João Paulo ^c   Viale, Alejandro M ^d   Salcedo, Suzana P ^a  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DE LYON   (France)

^c NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^d UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ACINETOBACTER BAUMANNII; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOFILM; CONTROLLED STUDY; ESCHERICHIA COLI; GALLERIA MELLONELLA; GENE IDENTIFICATION; KLEBSIELLA PNEUMONIAE; MULTIDRUG RESISTANCE; NONHUMAN; PSEUDOMONAS AERUGINOSA; STRAIN DIFFERENCE; TYPE IV SECRETION SYSTEM; ACINETOBACTER INFECTION; ANIMAL; BIOMASS; GENE EXPRESSION REGULATION; GENE LOCUS; GENE ORDER; GENETIC COMPLEMENTATION; GENETICS; HUMAN; MICROBIOLOGY; MOLECULAR GENETICS; MOTH; MUTATION; ORGANISMAL INTERACTION; PATHOGENICITY; PHENOTYPE; PHYSIOLOGY; TYPE VI SECRETION SYSTEM; VIRULENCE;

TYPE VI SECRETION SYSTEM;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANIMALS; BIOFILMS; BIOMASS; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; GENETIC COMPLEMENTATION TEST; GENETIC LOCI; HUMANS; MICROBIAL INTERACTIONS; MOLECULAR SEQUENCE DATA; MOTHS; MUTATION; PHENOTYPE; TYPE VI SECRETION SYSTEMS; VIRULENCE;

EID: 84946906380     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138265     Document Type: Article

References (42)

1. McConnell MJ, Actis L, Pachón J. Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiology Reviews. 2012; 37: 130-155. doi: 10.1111/j. 1574-6976.2012.00344.x PMID: 22568581
2. Zarrilli R, Pournaras S, Giannouli M, Tsakris A. Global evolution of multidrug-resistant Acinetobacter baumannii clonal lineages. Int J Antimicrob Agents. 2013; 41: 11-19. doi: 10.1016/j.ijantimicag.2012. 09.008 PMID: 23127486
3. Espinal P, Martí S, Vila J. Effect of biofilm formation on the survival of Acinetobacter baumannii on dry surfaces. J Hosp Infect. 2012; 80: 56-60. doi: 10.1016/j.jhin.2011.08.013 PMID: 21975219
4. Longo F, Vuotto C, Donelli G. Biofilm formation in Acinetobacter baumannii. New Microbiol. 2014; 37: 119-127. PMID: 24858639
5. Rumbo-Feal S, Gómez MJ, Gayoso C, Álvarez-Fraga L, Cabral MP, Aransay AM, 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. PMID: 24023660
6. Lees-Miller RG, Iwashkiw JA, Scott NE, Seper A, Vinogradov E, Schild S, et al. A common pathway for O-linked protein-glycosylation and synthesis of capsule in Acinetobacter baumannii. Mol Microbiol. 2013; 89: 816-830. doi: 10.1111/mmi.12300 PMID: 23782391
7. Iwashkiw JA, Seper A, Weber BS, Scott NE, Vinogradov E, Stratilo C, et al. Identification of a general O-linked protein glycosylation system in Acinetobacter baumannii and its role in virulence and biofilm formation. PLoS Pathog. 2012; 8: e1002758. doi: 10.1371/journal.ppat.1002758.t003 PMID: 22685409
8. 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: 3150-3160. doi: 10.1128/IAI.00096-09 PMID: 19470746
9. Mortensen BL, Skaar EP. Host-microbe interactions that shape the pathogenesis of Acinetobacter baumannii infection. Cell Microbiol. 2012; 14: 1336-1344. doi: 10.1111/j.1462-5822.2012.01817.x PMID: 22640368
10. Weber BS, Miyata ST, Iwashkiw JA, Mortensen BL, Skaar EP, Pukatzki S, et al. Genomic and functional analysis of the Type VI Secretion System in Acinetobacter. PLoS ONE. 2013; 8: e55142. PMID: 23365692
11. Carruthers MD, Nicholson PA, Tracy EN, Munson RS. Acinetobacter baumannii Utilizes a Type VI Secretion System for bacterial competition. PLoS ONE. 2013; 8: e59388. PMID: 23527179
12. Basler M, Ho BT, Mekalanos JJ. Tit-for-tat: type VI secretion system counterattack during bacterial cellcell interactions. Cell. 2013; 152: 884-894. doi: 10.1016/j.cell.2013.01.042 PMID: 23415234
13. Zoued A, Brunet YR, Durand E, Aschtgen M-S, Logger L, Douzi B, et al. Architecture and assembly of the Type VI secretion system. Biochim Biophys Acta. 2014; 1843: 1664-1673. doi: 10.1016/j.bbamcr. 2014.03.018 PMID: 24681160
14. Borgeaud S, Metzger LC, Scrignari T, Blokesch M. Bacterial evolution. The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science. 2015; 347: 63-67. doi: 10.1126/science. 1260064 PMID: 25554784
15. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature. 2013; 500: 350-353. doi: 10.1038/nature12453 PMID: 23925114
16. Wright MS, Haft DH, Harkins DM, Perez F, Hujer KM, Bajaksouzian S, et al. New insights into dissemination and variation of the health care-associated pathogen Acinetobacter baumannii from genomic analysis. mBio. 2014; 5: e00963-13. doi: 10.1128/mBio.00963-13 PMID: 24449752
17. Jones CL, Clancy M, Honnold C, Singh S, Snesrud E, Onmus-Leone F, et al. Fatal outbreak of an emerging clone of extensively drug-resistant Acinetobacter baumannii with enhanced virulence. Clin Infect Dis. 2015; 61: 145-154. doi: 10.1093/cid/civ225 PMID: 25824815
18. Mussi MA, Limansky AS, Viale AM. Acquisition of resistance to carbapenems in multidrug-resistant clinical strains of Acinetobacter baumannii: natural insertional inactivation of a gene encoding a member of a novel family of beta-barrel outer membrane proteins. Antimicrob Agents Chemother. 2005; 49: 1432-1440. doi: 10.1128/AAC.49.4.1432-1440.2005 PMID: 15793123
19. Tomaras AP, Dorsey CW, Edelmann RE, Actis LA. Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology (Reading, Engl). 2003; 149: 3473-3484.
20. Mussi MA, Relling VM, Limansky AS, Viale AM. CarO, an Acinetobacter baumannii outer membrane protein involved in carbapenem resistance, is essential for l-ornithine uptake. FEBS Letters. 2007; 581: 5573-5578. doi: 10.1016/j.febslet.2007.10.063 PMID: 17997983
21. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene. 1998; 212: 77-86. PMID: 9661666
22. Hachani A, Lossi NS, Hamilton A, Jones C, Bleves S, Albesa-Jové D, et al. Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. Journal of Biological Chemistry. 2011; 286: 12317-12327. doi: 10.1074/jbc.M110.193045 PMID: 21325275
23. Choi K-H, Schweizer HP. mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nature Protocols. 2006; 1: 153-161. doi: 10.1038/nprot.2006.24 PMID: 17406227
24. Piechaud M, Second L. Studies of 26 strains of Moraxella Iwoffi. Ann Inst Pasteur (Paris). 1951; 80: 97-99.
25. Wilharm G, Piesker J, Laue M, Skiebe E. DNA Uptake by the nosocomial pathogen Acinetobacter baumannii occurs during movement along wet surfaces. J Bacteriol. 2013; 195: 4146-4153. doi: 10.1128/JB.00754-13 PMID: 23852865
26. Mussi MA, Limansky AS, Relling V, Ravasi P, Arakaki A, Actis LA, et al. Horizontal gene transfer and assortative recombination within the Acinetobacter baumannii clinical population provide genetic diversity at the single carO gene, encoding a major outer membrane protein channel. J Bacteriol. 2011; 193: 4736-4748. doi: 10.1128/JB.01533-10 PMID: 21764928
27. Unterweger D, Miyata ST, Bachmann V, Brooks TM, Mullins T, Kostiuk B, et al. The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition. Nature Communications. 2014; 5: 3549. doi: 10.1038/ncomms4549 PMID: 24686479
28. Moscoso JA, Mikkelsen H, Heeb S, Williams P, Filloux A. The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol. 2011; 13: 3128-3138. doi: 10.1111/j.1462-2920.2011.02595.x PMID: 21955777
29. Mussi MA, Gaddy JA, Cabruja M, Arivett BA, Viale AM, Rasia R, et al. The opportunistic human pathogen Acinetobacter baumannii senses and responds to light. J Bacteriol. 2010; 192: 6336-6345. doi: 10. 1128/JB.00917-10 PMID: 20889755
30. Zhang L, Xu J, Xu J, Zhang H, He L, Feng J. TssB is essential for virulence and required for type VI secretion system in Ralstonia solanacearum. Microb Pathog. 2014; 74: 1-7. doi: 10.1016/j.micpath. 2014.06.006 PMID: 24972114
31. Enos-Berlage JL, Guvener ZT, Keenan CE, McCarter LL. Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol Microbiol. 2005; 55: 1160-1182. doi: 10.1111/j.1365-2958.2004.04453.x PMID: 15686562
32. Aschtgen M-S, Bernard CS, De Bentzmann S, Lloubès R, Cascales E. SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J Bacteriol. 2008; 190: 7523-7531. doi: 10.1128/JB.00945-08 PMID: 18805985
33. Lopez-Rojas R, Dominguez-Herrera J, McConnell MJ, Docobo-Perez F, Smani Y, Fernandez-Reyes M, et al. Impaired virulence and in vivo fitness of colistin-resistant Acinetobacter baumannii. Journal of Infectious Diseases. 2011; 203: 545-548. doi: 10.1093/infdis/jiq086 PMID: 21216865
34. Peleg AY, Jara S, Monga D, Eliopoulos GM, Moellering RC, Mylonakis E. Galleria mellonella as a model system to study Acinetobacter baumannii pathogenesis and therapeutics. Antimicrob Agents Chemother. 2009; 53: 2605-2609. doi: 10.1128/AAC.01533-08 PMID: 19332683
35. Harding CR, Schroeder GN, Reynolds S, Kosta A, Collins JW, Mousnier A, et al. Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect Immun. 2012; 80: 2780-2790. doi: 10.1128/IAI.00510-12 PMID: 22645286
36. Jander G, Rahme LG, Ausubel FM. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol. 2000; 182: 3843-3845. PMID: 10851003
37. Heindorf M, Kadari M, Heider C, Skiebe E, Wilharm G. Impact of Acinetobacter baumannii superoxide dismutase on motility, virulence, oxidative stress resistance and susceptibility to antibiotics. PLoS ONE. 2014; 9: e101033. PMID: 25000585
38. Jacobs AC, Thompson MG, Black CC, Kessler JL, Clark LP, McQueary CN, et al. AB5075, a highly virulent isolate of Acinetobacter baumannii, as a model strain for the evaluation of pathogenesis and antimicrobial treatments. mBio. 2014; 5: e01076-14. doi: 10.1128/mBio.01076-14 PMID: 24865555
39. Weber BS, Ly PM, Irwin JN, Pukatzki S, Feldman MF. A multidrug resistance plasmid contains the molecular switch for type VI secretion in Acinetobacter baumannii. Proc Natl Acad Sci U S A. 2015; 112: 9442-9447. doi: 10.1073/pnas.1502966112 PMID: 26170289
40. Koskiniemi S, Lamoureux JG, Nikolakakis KC, t'Kint de Roodenbeke C, Kaplan MD, Low DA, et al. Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci U S A. 2013; 110: 7032-7037. doi: 10.1073/pnas.1300627110 PMID: 23572593
41. Salomon D, Kinch LN, Trudgian DC, Guo X, Klimko JA, Grishin NV, et al. Marker for type VI secretion system effectors. Proc Natl Acad Sci U S A. 2014; 111: 9271-9276. doi: 10.1073/pnas.1406110111 PMID: 24927539
42. Bergin D, Reeves EP, Renwick J, Wientjes FB, Kavanagh K. Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun. 2005; 73: 4161-4170. doi: 10.1128/IAI.73.7.4161-4170.2005 PMID: 15972506