Functional genomic characterization of virulence factors from necrotizing fasciitis-causing strains of Aeromonas hydrophila

Applied and Environmental Microbiology

Volumn 80, Issue 14, 2014, Pages 4162-4183

  Grim, Christopher J ^a   Kozlova, Elena V ^b   Ponnusamy, Duraisamy ^b   Fitts, Eric C ^b   Sha, Jian ^b   Kirtley, Michelle L ^b   van Lier, Christina J ^b   Tiner, Bethany L ^b   Erova, Tatiana E ^b   Joseph, Sandeep J ^c   Read, Timothy D ^c   Shak, Joshua R ^c   Joseph, Sam W ^d,e   Singletary, Ed ^f   Felland, Tracy ^g   Baze, Wallace B ^h   Horneman, Amy J ⁱ   Chopra, Ashok K ^b  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Bldg 142   (United States)

^e UNIVERSITY OF MARYLAND   (United States)

^f Doctors Hospital   (United States)

^g MERCY HEALTH SYSTEM   (United States)

^h UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

ⁱ VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS;

AEROMONAS HYDROPHILA; BIOFILM FORMATION; ENVIRONMENTAL ISOLATES; FUNCTIONAL GENOMIC ANALYSIS; FUNCTIONAL GENOMICS; POTENTIAL ABILITY; SECRETION SYSTEMS; VIRULENCE FACTORS;

GENES;

BACTERIUM; DATA SET; GENOME; GENOMICS; INFILTRATION; NUMERICAL MODEL; TOXIN; VIRULENCE;

BACTERIAL DNA; ENTEROTOXIN; FRESH WATER; VIRULENCE FACTOR;

AEROMONAS HYDROPHILA; ANIMAL; BACTERIAL GENE; BIOFILM; DISEASE MODEL; DNA SEQUENCE; FEMALE; GENETIC ASSOCIATION; GENETICS; GRAM NEGATIVE INFECTION; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOUSE; NECROTIZING FASCIITIS; PATHOGENICITY; PHYLOGENY; PLAGUE; PLASMID; SEQUENCE ALIGNMENT;

AEROMONAS HYDROPHILA; ANIMALS; BIOFILMS; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; ENTEROTOXINS; FASCIITIS, NECROTIZING; FEMALE; FRESH WATER; GENES, BACTERIAL; GENETIC ASSOCIATION STUDIES; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; MICE; PHYLOGENY; PLAGUE; PLASMIDS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS; WATER MICROBIOLOGY;

EID: 84903146551     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00486-14     Document Type: Article

References (100)

1. Von Graevenitz A, Mensch AH. 1968. The genus Aeromonas in human bacteriology-report of 30 cases and review of the literature. N. Engl. J. Med. 278:245-249. http://dx.doi.org/10.1056/NEJM196802012780504.
2. Presley SM, Rainwater TR, Austin GP, Platt SG, Zak JC, Cobb GP, Marsland EJ, Tian K, Zhang B, Anderson TA, Cox SB, Abel MT, Leftwich BD, Huddleston JR, Jeter RM, Kendall RJ. 2006. Assessment of pathogens and toxicants in New Orleans, LA following Hurricane Katrina. Environ. Sci. Technol. 40:468-474. http://dx.doi.org/10.1021 /es052219p.
3. Chen PL, Wu CJ, Chen CS, Tsai PJ, Tang HJ, Ko WC. 16 November 2013. A comparative study of clinical Aeromonas dhakensis and Aeromonas hydrophila isolates in southern Taiwan: A. dhakensis is more predominant and virulent. Clin. Microbiol. Infect. http://dx.doi.org/10.1111 /1469-0691.12456.
4. Palú AP, Gomes LM, Miguel MA, Balassiano IT, Queiroz ML, Freitas-Almeida AC, de Oliveira SS. 2006. Antimicrobial resistance in food and clinical Aeromonas isolates. Food Microbiol. 23:504-509. http://dx.doi.org/10.1016/j.fm.2005.07.002.
5. Chauret C, Volk C, Creason R, Jarosh J, Robinson J, Warnes C. 2001. Detection of Aeromonas hydrophila in a drinking-water distribution system: a field and pilot study. Can. J. Microbiol. 47:782-786. http://dx.doi.org/10.1139/w01-070.
6. Hiransuthikul N, Tantisiriwat W, Lertutsahakul K, Vibhagool A, Boonma P. 2005. Skin and soft-tissue infections among tsunami survivors in southern Thailand. Clin. Infect. Dis. 41:e93-96. http://dx.doi.org /10.1086/497372.
7. Figueras MJ, Aldea MJ, Fernandez N, Aspiroz C, Alperi A, Guarro J. 2007. Aeromonas hemolytic-uremic syndrome. A case and a review of the literature. Diagn. Microbiol. Infect. Dis. 58:231-234. http://dx.doi.org /10.1016/j.diagmicrobio.2006.11.023.
8. Figueras MJ. 2005. Clinical relevance of Aeromonas sM503. Rev. Med. Microbiol. 16:145-153. http://dx.doi.org/10.1097/01.revmedmi.000018 4410.98677.8a.
9. Monaghan SF, Anjaria D, Mohr A, Livingston DH. 2008. Necrotizing fasciitis and sepsis caused by Aeromonas hydrophila after crush injury of the lower extremity. Surg. Infect. 9:459-467. http://dx.doi.org/10.1089 /sur.2007.028.
10. Tsai YH, Huang KC, Huang TJ, Hsu RW. 2009. Case reports: fatal necrotizing fasciitis caused by Aeromonas sobria in two diabetic patients. Clin. Orthop. Relat. Res. 467:846-849. http://dx.doi.org/10.1007/s11999-008-0504-0.
11. Cui H, Hao S, Arous E. 2007. A distinct cause of necrotizing fasciitis: Aeromonas veronii biovar sobria. Surg. Infect. 8:523-528. http://dx.doi.org/10.1089/sur.2006.046.
12. Furusu A, Yoshizuka N, Abe K, Sasaki O, Miyazaki K, Miyazaki M, Hirakata Y, Ozono Y, Harada T, Kohno S. 1997. Aeromonas hydrophila necrotizing fasciitis and gas gangrene in a diabetic patient on haemodialysis. Nephrol. Dial. Transplant. 12:1730-1734. http://dx.doi.org/10.1093/ndt/12.8.1730.
13. Joseph SW, Daily OP, Hunt WS, Seidler RJ, Allen DA, Colwell RR. 1979. Aeromonas primary wound infection of a diver in polluted waters. J. Clin. Microbiol. 10:46-49.
14. Sever R, Lee Goldstein A, Steinberg E, Soffer D. 2013. Trauma with a touch of fresh water: necrotizing fasciitis caused by Aeromonas hydrophilia after a motorcycle accident. Am. Surg. 79:E326-E328.
15. Xu XJ, Ferguson MR, Popov VL, Houston CW, Peterson JW, Chopra AK. 1998. Role of a cytotoxic enterotoxin in Aeromonas-mediated infections: development of transposon and isogenic mutants. Infect. Immun. 66:3501-3509.
16. Ferguson MR, Xu XJ, Houston CW, Peterson JW, Coppenhaver DH, Popov VL, Chopra AK. 1997. Hyperproduction, purification, and mechanism of action of the cytotoxic enterotoxin produced by Aeromonas hydrophila. Infect. Immun. 65:4299-4308.
17. Galindo CL, Fadl AA, Sha J, Pillai L, Gutierrez C, Jr, Chopra AK. 2005. Microarray and proteomics analyses of human intestinal epithelial cells treated with the Aeromonas hydrophila cytotoxic enterotoxin. Infect. Immun. 73:2628-2643. http://dx.doi.org/10.1128/IAI.73.5.2628-2643.2005.
18. Galindo CL, Gutierrez C, Jr, Chopra AK. 2006. Potential involvement of galectin-3 and SNAP23 in Aeromonas hydrophila cytotoxic enterotoxin-induced host cell apoptosis. Microb. Pathog. 40:56-68. http://dx.doi.org/10.1016/j.micpath.2005.11.001.
19. Ribardo DA, Kuhl KR, Boldogh I, Peterson JW, Houston CW, Chopra AK. 2002. Early cell signaling by the cytotoxic enterotoxin of Aeromonas hydrophila in macrophages. Microb. Pathog. 32:149-163. http://dx.doi.org/10.1006/mpat.2001.0490.
20. Galindo CL, Fadl AA, Sha J, Gutierrez C, Jr, Popov VL, Boldogh I, Aggarwal BB, Chopra AK. 2004. Aeromonas hydrophila cytotoxic enterotoxin activates mitogen-activated protein kinases and induces apoptosis in murine macrophages and human intestinal epithelial cells. J. Biol. Chem. 279:37597-37612. http://dx.doi.org/10.1074/jbc.M404641200.
21. Rosenzweig JA, Chopra AK. 2013. The exoribonuclease polynucleotide phosphorylase influences the virulence and stress responses of yersiniae and many other pathogens. Front. Cell. Infect. Microbiol. 3:81. http://dx.doi.org/10.3389/fcimb.2013.00081.
22. Sha J, Wang SF, Suarez G, Sierra JC, Fadl AA, Erova TE, Foltz SM, Khajanchi BK, Silver A, Graf J, Schein CH, Chopra AK. 2007. Further characterization of a type III secretion system (T3SS) and of a new effector protein from a clinical isolate of Aeromonas hydrophila-part I. Microb. Pathog. 43:127-146. http://dx.doi.org/10.1016/j.micpath.2007.05.002.
23. Suarez G, Sierra JC, Sha J, Wang S, Erova TE, Fadl AA, Foltz SM, Horneman AJ, Chopra AK. 2008. Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 44:344-361. http://dx.doi.org/10.1016/j.micpath.2007.10.005.
24. Suarez G, Sierra JC, Erova TE, Sha J, Horneman AJ, Chopra AK. 2010. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192:155-168. http://dx.doi.org/10.1128/JB.01260-09.
25. Beaz-Hidalgo R, Martinez-Murcia A, Figueras MJ. 2013. Reclassification of Aeromonas hydrophila subsp. dhakensis Huys et al. 2002 and Aeromonas aquariorum Martinez-Murcia et al. 2008. as Aeromonas dhakensis sp. nov. comb nov. and emendation of the species Aeromonas hydrophila. Syst. Appl. Microbiol. 36:171-176. http://dx.doi.org/10.1016/j.syapm.2012.12.007.
26. Suarez G, Sierra JC, Kirtley ML, Chopra AK. 2010. Role of Hcp, a type 6 secretion system effector, of Aeromonas hydrophila in modulating activation of host immune cells. Microbiology 156:3678-3688. http://dx.doi.org/10.1099/mic.0.041277-0.
27. Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK, Chhabra SR, Williams P, Macintyre S, Stewart GS. 1997. Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J. Bacteriol. 179:5271-5281.
28. Kozlova EV, Khajanchi BK, Sha J, Chopra AK. 2011. Quorum sensing and c-di-GMP-dependent alterations in gene transcripts and virulence-associated phenotypes in a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 50:213-223. http://dx.doi.org/10.1016/j.micpath.2011.01.007.
29. Kirov SM, Castrisios M, Shaw JG. 2004. Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infect. Immun. 72:1939-1945. http://dx.doi.org/10.1128/IAI.72.4.1939-1945.2004.
30. Kirov SM, Tassell BC, Semmler AB, O'Donovan LA, Rabaan AA, Shaw JG. 2002. Lateral flagella and swarming motility in Aeromonas species. J. Bacteriol. 184:547-555. http://dx.doi.org/10.1128/JB.184.2.547-555.2002.
31. Ramachandran G, Tulapurkar ME, Harris KM, Arad G, Shirvan A, Shemesh R, Detolla LJ, Benazzi C, Opal SM, Kaempfer R, Cross AS. 2013. A peptide antagonist of CD28 signaling attenuates toxic shock and necrotizing soft-tissue infection induced by Streptococcus pyogenes. J. Infect. Dis. 207:1869-1877. http://dx.doi.org/10.1093/infdis/jit104.
32. Baker C, Antonovics J. 2012. Evolutionary determinants of genetic variation in susceptibility to infectious diseases in humans. PLoS One 7:e29089. http://dx.doi.org/10.1371/journal.pone.0029089.
33. Khajanchi BK, Fadl AA, Borchardt MA, Berg RL, Horneman AJ, Stemper ME, Joseph SW, Moyer NP, Sha J, Chopra AK. 2010. Distribution of virulence factors and molecular fingerprinting of Aeromonas species isolates from water and clinical samples: suggestive evidence of water-to-human transmission. Appl. Environ. Microbiol. 76:2313-2325. http://dx.doi.org/10.1128/AEM.02535-09.
34. Carnahan AM, Behram S, Joseph SW. 1991. Aerokey II: a flexible key for identifying clinical Aeromonas species. J. Clin. Microbiol. 29:2843-2849.
35. Abbott SL, Cheung WK, Janda JM. 2003. The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J. Clin. Microbiol. 41:2348-2357. http://dx.doi.org/10.1128/JCM.41.6.2348-2357.2003.
36. Havelaar AH, During M, Versteegh JF. 1987. Ampicillin-dextrin agar medium for the enumeration of Aeromonas species in water by membrane filtration. J. Appl. Bacteriol. 62:279-287. http://dx.doi.org/10.1111/j.1365-2672.1987.tb02410.x.
37. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380. http://dx.doi.org/10.1038/nature03959.
38. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I. 2009. ABySS: a parallel assembler for short read sequence data. Genome Res. 19:1117-1123. http://dx.doi.org/10.1101/gr.089532.108.
39. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. http://dx.doi.org/10.1186 /1471-2164-9-75.
40. Seshadri R, Joseph SW, Chopra AK, Sha J, Shaw J, Graf J, Haft D, Wu M, Ren Q, Rosovitz MJ, Madupu R, Tallon L, Kim M, Jin S, Vuong H, Stine OC, Ali A, Horneman AJ, Heidelberg JF. 2006. Genome sequence of Aeromonas hydrophila ATCC 7966T: jack of all trades. J. Bacteriol. 188:8272-8282. http://dx.doi.org/10.1128/JB.00621-06.
41. Michel C. 1979. Furunculosis of salmonids: vaccination attempts in rainbow trout (Salmo gairdneri) by formalin-killed germs. Ann. Rech. Vet. 10:33-40.
42. Grim CJ, Kozlova EV, Sha J, Fitts EC, van Lier CJ, Kirtley ML, Joseph SJ, Read TD, Burd EM, Tall BD, Joseph SW, Horneman AJ, Chopra AK, Shak JR. 2013. Characterization of Aeromonas hydrophila wound pathotypes by comparative genomic and functional analyses of virulence genes. mBio 4:e00064-13. http://dx.doi.org/10.1128/mBio.00064-13.
43. Wu CJ, Wang HC, Chen CS, Shu HY, Kao AW, Chen PL, Ko WC. 2012. Genome sequence of a novel human pathogen, Aeromonas aquariorum. J. Bacteriol. 194:4114-4115. http://dx.doi.org/10.1128/JB.00621-12.
44. Li Y, Liu Y, Zhou Z, Huang H, Ren Y, Zhang Y, Li G, Wang L. 2011. Complete genome sequence of Aeromonas veronii strain B565. J. Bacteriol. 193:3389-3390. http://dx.doi.org/10.1128/JB.00347-11.
45. Beatson SA, das Gracas de Luna M, Bachmann NL, Alikhan NF, Hanks KR, Sullivan MJ, Wee BA, Freitas-Almeida AC, Dos Santos PA, de Melo JT, Squire DJ, Cunningham AF, Fitzgerald JR, Henderson IR. 2011. Genome sequence of the emerging pathogen Aeromonas caviae. J. Bacteriol. 193:1286-1287. http://dx.doi.org/10.1128/JB.01337-10.
46. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch GD, Rodionov DA, Ruckert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y, Zagnitko O, Vonstein V. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33:5691-5702. http://dx.doi.org/10.1093/nar/gki866.
47. Chun J, Grim CJ, Hasan NA, Lee JH, Choi SY, Haley BJ, Taviani E, Jeon YS, Kim DW, Brettin TS, Bruce DC, Challacombe JF, Detter JC, Han CS, Munk AC, Chertkov O, Meincke L, Saunders E, Walters RA, Huq A, Nair GB, Colwell RR. 2009. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc. Natl. Acad. Sci. USA. 106:15442-15447. http://dx.doi.org/10.1073/pnas.0907787106.
48. Grim CJ, Kotewicz ML, Power KA, Gopinath G, Franco AA, Jarvis KG, Yan QQ, Jackson SA, Sathyamoorthy V, Hu L, Pagotto F, Iversen C, Lehner A, Stephan R, Fanning S, Tall BD. 2013. Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a specieslevel bidirectional divergence driven by niche adaptation. BMC Genomics 14:366. http://dx.doi.org/10.1186/1471-2164-14-366.
49. Richter M, Rossello-Mora R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA. 106:19126-19131. http://dx.doi.org/10.1073/pnas.0906412106.
50. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
51. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis comparison tool. Bioinformatics 21:3422-3423. http://dx.doi.org/10.1093/bioinformatics/bti553.
52. Li L, Stoeckert CJ, Jr, Roos DS. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189. http://dx.doi.org/10.1101/gr.1224503.
53. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. http: //dx.doi.org/10.1186/1471-2105-5-113.
54. Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56:564-577. http://dx.doi.org/10.1080 /10635150701472164.
55. Felsenstein J. 1988. Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22:521-565. http://dx.doi.org/10.1146 /annurev.ge.22.120188.002513.
56. Felsenstein J. 1989. Mathematics vs. evolution: mathematical evolutionary theory. Science 246:941-942. http://dx.doi.org/10.1126/science.246.4932.941.
57. O'Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461. http://dx.doi.org/10.1046/j.1365-2958.1998.00797.x.
58. Khajanchi BK, Kozlova EV, Sha J, Popov VL, Chopra AK. 2012. The two-component QseBC signalling system regulates in vitro and in vivo virulence of Aeromonas hydrophila. Microbiology 158:259-271. http: //dx.doi.org/10.1099/mic.0.051805-0.
59. Morohoshi T, Shiono T, Takidouchi K, Kato M, Kato N, Kato J, Ikeda T. 2007. Inhibition of quorum sensing in Serratia marcescens AS-1 by synthetic analogs of N-acylhomoserine lactone. Appl. Environ. Microbiol. 73:6339-6344. http://dx.doi.org/10.1128/AEM.00593-07.
60. Erova TE, Pillai L, Fadl AA, Sha J, Wang S, Galindo CL, Chopra AK. 2006. DNA adenine methyltransferase influences the virulence of Aeromonas hydrophila. Infect. Immun. 74:410-424. http://dx.doi.org/10.1128/IAI.74.1.410-424.2006.
61. Sha J, Kozlova EV, Chopra AK. 2002. Role of various enterotoxins in Aeromonas hydrophila-induced gastroenteritis: generation of enterotoxin gene-deficient mutants and evaluation of their enterotoxic activity. Infect. Immun. 70:1924-1935. http://dx.doi.org/10.1128/IAI.70.4.1924-1935.2002.
62. Khajanchi BK, Sha J, Kozlova EV, Erova TE, Suarez G, Sierra JC, Popov VL, Horneman AJ, Chopra AK. 2009. N-Acylhomoserine lactones involved in quorum sensing control the type VI secretion system, biofilm formation, protease production, and in vivo virulence in a clinical isolate of Aeromonas hydrophila. Microbiology 155:3518-3531. http: //dx.doi.org/10.1099/mic.0.031575-0.
63. Sierra JC, Suarez G, Sha J, Baze WB, Foltz SM, Chopra AK. 2010. Unraveling the mechanism of action of a new type III secretion system effector AexU from Aeromonas hydrophila. Microb. Pathog. 49:122-134. http://dx.doi.org/10.1016/j.micpath.2010.05.011.
64. Lory S, Strom MS, Johnson K. 1988. Expression and secretion of the cloned Pseudomonas aeruginosa exotoxin A by Escherichia coli. J. Bacteriol. 170:714-719.
65. Liu PV. 1973. Exotoxins of Pseudomonas aeruginosa. I. Factors that influence the production of exotoxin A. J. Infect. Dis. 128:506-513.
66. Bjorn MJ, Iglewski BH, Ives SK, Sadoff JC, Vasil ML. 1978. Effect of iron on yields of exotoxin A in cultures of Pseudomonas aeruginosa PA-103. Infect. Immun. 19:785-791.
67. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, Schweizer HP. 2005. A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2:443-448. http://dx.doi.org/10.1038/nmeth765.
68. Sha J, Rosenzweig JA, Kirtley ML, van Lier CJ, Fitts EC, Kozlova EV, Erova TE, Tiner BL, Chopra AK. 2013. A non-invasive in vivo imaging system to study dissemination of bioluminescent Yersinia pestis CO92 in a mouse model of pneumonic plague. Microb. Pathog. 55:39-50. http: //dx.doi.org/10.1016/j.micpath.2012.09.011.
69. Shak JR, Whitaker JA, Ribner BS, Burd EM. 2011. Aminoglycosideresistant Aeromonas hydrophila as part of a polymicrobial infection following a traumatic fall into freshwater. J. Clin. Microbiol. 49:1169-1170. http://dx.doi.org/10.1128/JCM.01949-10.
70. Reith ME, Singh RK, Curtis B, Boyd JM, Bouevitch A, Kimball J, Munholland J, Murphy C, Sarty D, Williams J, Nash JH, Johnson SC, Brown LL. 2008. The genome of Aeromonas salmonicida subsp. salmonicida A449: insights into the evolution of a fish pathogen. BMC Genomics 9:427. http://dx.doi.org/10.1186/1471-2164-9-427.
71. Worby CJ, Lipsitch M, Hanage WP. 2014. Within-host bacterial diversity hinders accurate reconstruction of transmission networks from genomic distance data. PLoS Comput. Biol. 10:e1003549. http://dx.doi.org/10.1371/journal.pcbi.1003549.
72. Iglewski BH, Liu PV, Kabat D. 1977. Mechanism of action of Pseudomonas aeruginosa exotoxin A: adenosine diphosphate-ribosylation of mammalian elongation factor 2 in vitro and in vivo. Infect. Immun. 15:138-144.
73. McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GS, Williams P. 1997. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of Nacylhomoserine lactones. Microbiology 143(Pt 12):3703-3711. http://dx.doi.org/10.1099/00221287-143-12-3703.
74. Pukatzki S, McAuley SB, Miyata ST. 2009. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12:11-17. http://dx.doi.org/10.1016/j.mib.2008.11.010.
75. Sierra JC, Suarez G, Sha J, Foltz SM, Popov VL, Galindo CL, Garner HR, Chopra AK. 2007. Biological characterization of a new type III secretion system effector from a clinical isolate of Aeromonas hydro-phila-part II. Microb. Pathog. 43:147-160. http://dx.doi.org/10.1016/j.micpath.2007.05.003.
76. Gray GL, Smith DH, Baldridge JS, Harkins RN, Vasil ML, Chen EY, Heyneker HL. 1984. Cloning, nucleotide sequence, and expression in Escherichia coli of the exotoxin A structural gene of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA. 81:2645-2649. http://dx.doi.org/10.1073/pnas.81.9.2645.
77. Matsui H, Sekiya Y, Nakamura M, Murayama SY, Yoshida H, Takahashi T, Imanishi K, Tsuchimoto K, Uchiyama T, Sunakawa K, Ubukata K. 2009. CD46 transgenic mouse model of necrotizing fasciitis caused by Streptococcus pyogenes infection. Infect. Immun. 77:4806-4814. http://dx.doi.org/10.1128/IAI.00577-09.
78. Borger van der Burg BL, Bronkhorst MW, Pahlplatz PV. 2006. Aeromonas hydrophila necrotizing fasciitis. A case report. J. Bone Joint Surg. Am. 88:1357-1360. http://dx.doi.org/10.2106/JBJS.C.00923.
79. Chern CH, How CK, Huang LJ. 2006. Images in emergency medicine. Necrotizing fasciitis caused by Aeromonas hydrophila. Ann. Emerg. Med. 48:216-225. http://dx.doi.org/10.1016/j.annemergmed.2005.12.027.
80. Psoinos CM, Flahive JM, Shaw JJ, Li Y, Ng SC, Tseng JF, Santry HP. 2013. Contemporary trends in necrotizing soft-tissue infections in the United States. Surgery 153:819-827. http://dx.doi.org/10.1016/j.surg.20 12.11.026.
81. Salcido RS. 2007. Necrotizing fasciitis: reviewing the causes and treatment strategies. Adv. Skin Wound Care 20:288-293, quiz 294-295. http: //dx.doi.org/10.1097/01.ASW.0000269317.76380.3b.
82. Keung EZ, Liu X, Nuzhad A, Adams C, Ashley SW, Askari R. 2013. Immunocompromised status in patients with necrotizing soft-tissue infection. JAMA Surg. 148:419-426. http://dx.doi.org/10.1001/jamasurg.2013.173.
83. Al Shukry S, Ommen J. 2013. Necrotizing fasciitis-report of ten cases and review of recent literature. J. Med. Life 6:189-194.
84. Johansson L, Thulin P, Low DE, Norrby-Teglund A. 2010. Getting under the skin: the immunopathogenesis of Streptococcus pyogenes deep tissue infections. Clin. Infect. Dis. 51:58-65. http://dx.doi.org/10.1086 /653116.
85. Skwor T, Shinko J, Augustyniak A, Gee C, Andraso G. 2014. Aeromonas hydrophila and Aeromonas veronii predominate among potentially pathogenic ciprofloxacin-and tetracycline-resistant Aeromonas isolates from Lake Erie. Appl. Environ. Microbiol. 80:841-848. http://dx.doi.org /10.1128/AEM.03645-13.
86. Ibekwe AM, Lyon SR. 2008. Microbiological evaluation of fecal bacterial composition from surface water through aquifer sand material. J. Water Health 6:411-421. http://dx.doi.org/10.2166/wh.2008.058.
87. Horneman AJ, Morris JG. 2012. Aeromonas. In Rose BD (ed), UpTo-Date: clinical reference library for physicians. Wolters Kluwer Health, Wellesley, MA.
88. Moormeier DE, Endres JL, Mann EE, Sadykov MR, Horswill AR, Rice KC, Fey PD, Bayles KW. 2013. Use of microfluidic technology to analyze gene expression during Staphylococcus aureus biofilm formation reveals distinct physiological niches. Appl. Environ. Microbiol. 79:3413-3424. http://dx.doi.org/10.1128/AEM.00395-13.
89. Kozlova EV, Popov VL, Sha J, Foltz SM, Erova TE, Agar SL, Horneman AJ, Chopra AK. 2008. Mutation in the S-ribosylhomocysteinase (luxS) gene involved in quorum sensing affects biofilm formation and virulence in a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 45:343-354. http://dx.doi.org/10.1016/j.micpath.2008.08.007.
90. Lynch MJ, Swift S, Kirke DF, Keevil CW, Dodd CE, Williams P. 2002. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 4:18-28. http://dx.doi.org/10.1046/j.1462-2920.2002.00264.x.
91. Canals R, Altarriba M, Vilches S, Horsburgh G, Shaw JG, Tomas JM, Merino S. 2006. Analysis of the lateral flagellar gene system of Aeromonas hydrophila AH-3. J. Bacteriol. 188:852-862. http://dx.doi.org/10.1128 /JB.188.3.852-862.2006.
92. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA. 2007. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189:3603-3612. http://dx.doi.org/10.1128 /JB.01685-06.
93. Shrout JD, Chopp DL, Just CL, Hentzer M, Givskov M, Parsek MR. 2006. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol. Microbiol. 62:1264-1277. http://dx.doi.org/10.1111/j.1365-2958.2006.05421.x.
94. Murray TS, Ledizet M, Kazmierczak BI. 2010. Swarming motility, secretion of type 3 effectors and biofilm formation phenotypes exhibited within a large cohort of Pseudomonas aeruginosa clinical isolates. J. Med. Microbiol. 59:511-520. http://dx.doi.org/10.1099/jmm.0.017715-0.
95. Wood TK, Gonzalez Barrios AF, Herzberg M, Lee J. 2006. Motility influences biofilm architecture in Escherichia coli. Appl. Microbiol. Biotechnol. 72:361-367. http://dx.doi.org/10.1007/s00253-005-0263-8.
96. Daddaoua A, Fillet S, Fernandez M, Udaondo Z, Krell T, Ramos JL. 2012. Genes for carbon metabolism and the ToxA virulence factor in Pseudomonas aeruginosa are regulated through molecular interactions of PtxR and PtxS. PLoS One 7:e39390. http://dx.doi.org/10.1371/journal.pone.0039390.
97. Stamenkovic I, Lew PD. 1984. Early recognition of potentially fatal necrotizing fasciitis. The use of frozen-section biopsy. N. Engl. J. Med. 310:1689-1693.
98. Johansson L, Linner A, Sunden-Cullberg J, Haggar A, Herwald H, Lore K, Treutiger CJ, Norrby-Teglund A. 2009. Neutrophil-derived hyperresistinemia in severe acute streptococcal infections. J. Immunol. 183:4047-4054. http://dx.doi.org/10.4049/jimmunol.0901541.
99. Lacy P. 2006. Mechanisms of degranulation in neutrophils. Allergy Asthma Clin. Immunol. 2:98-108. http://dx.doi.org/10.1186/1710-1492-2-3-98.
100. Lintges M, van der Linden M, Hilgers RD, Arlt S, Al-Lahham A, Reinert RR, Plucken S, Rink L. 2010. Superantigen genes are more important than theemmtype for the invasiveness of group A Streptococcus infection. J. Infect. Dis. 202:20-28. http://dx.doi.org/10.1086/653082.