Characterization of Aeromonas hydrophila wound pathotypes by comparative genomic and functional analyses of virulence genes

mBio

Volumn 4, Issue 2, 2013, Pages

  Grim, Christopher J ^a   Kozlov, Elena V ^b   Sha, Jian ^b   Fitts, Eric C ^b   van Lier, Christina J ^b   Kirtley, Michelle L ^b   Joseph, Sandeep J ^c   Read, Timothy D ^c   Burd, Eileen M ^c   Tall, Ben D ^a   Joseph, Sam W ^d,e   Horneman, Amy J ^f   Chopra, Ashok K ^b   Shak, Joshua R ^c  

^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 VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACT PROTEIN; AEXU PROTEIN; BACTERIAL TOXIN; ENTEROTOXIN; EXOTOXIN; HEMOLYSIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AEROMONAS AQUARIORUM; AEROMONAS HYDROPHILA; AEROMONAS PUNCTATA; AEROMONAS SALMONICIDA; AEROMONAS VERONII; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL MOTILITY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTOXICITY; ELECTRON MICROSCOPY; ENVIRONMENT; FEMALE; FLAGELLUM; GENE SEQUENCE; GENOMICS; LETHALITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; SEROTYPE; STRAIN DIFFERENCE; WOUND INFECTION; ANIMAL; BACTERIAL GENOME; CYTOLOGY; DISEASE MODEL; DNA SEQUENCE; GENETICS; GENOTYPE; GRAM NEGATIVE INFECTION; HUMAN; ISOLATION AND PURIFICATION; LOCOMOTION; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY;

AEROMONAS HYDROPHILA; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FLAGELLA; GENOME, BACTERIAL; GENOTYPE; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; LOCOMOTION; MICE; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS; WOUND INFECTION;

EID: 84880060237     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00064-13     Document Type: Article

References (78)

1. Horneman AJ, Ali A. 2011. Aeromonas, p -658-665. In Versalovic J (ed), Manual of clinical microbiology, 10th ed. ASM Press, Washington, DC.
2. Janda JM, Abbott SL. 2010. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev. 23:35-73.
3. Parker JL, Shaw JG. 2011. Aeromonas spp. Clinical microbiology and disease. J. Infect. 62:109-118.
4. Huang KF, Hung MH, Lin YS, Lu CL, Liu C, Chen CC, Lee YH. 2011. Independent predictors of mortality for necrotizing fasciitis: a retrospective analysis in a single institution. J. Trauma 71:467-473.
5. Roberts MT, Enoch DA, Harris KA, Karas JA. 2006. Aeromonas veronii biovar sobria bacteraemia with septic arthritis confirmed by 16S rDNA PCR in an immunocompetent adult. J. Med. Microbiol. 55:241-243.
6. Abuhammour W, Hasan RA, Rogers D. 2006. Necrotizing fasciitis caused by Aeromonas hydrophilia [sic] in an immunocompetent child. Pediatr. Emerg. Care 22:48-51.
7. Dwivedi M, Mishra A, Prasad A, Azim A, Singh RK, Baronia AK, Prasad KN, Dwivedi UN. 2008. Aeromonas caviae septicemia in immunocompetent gastrointestinal carriers. Braz. J. Infect. Dis. 12:547-548.
8. 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.
9. Chopra AK, Houston CW, Peterson JW, Jin GF. 1993. Cloning, expression, and sequence analysis of a cytolytic enterotoxin gene from Aeromonas hydrophila. Can. J. Microbiol. 39:513-523.
10. 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.
11. Zacaria J, Delamare AP, Costa SO, Echeverrigaray S. 2010. Diversity of extracellular proteases among Aeromonas determined by zymogram analysis. J. Appl. Microbiol. 109:212-219.
12. 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.
13. Yu HB, Rao PS, Lee HC, Vilches S, Merino S, Tomas JM, Leung KY. 2004. A type III secretion system is required for Aeromonas hydrophila AH-1 pathogenesis. Infect. Immun. 72:1248-1256.
14. Sen K, Lye D. 2007. Importance of flagella and enterotoxins for Aeromonas virulence in a mouse model. Can. J. Microbiol. 53:261-269.
15. 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.
16. Joseph SW, Carnahan AM, Brayton PR, Fanning GR, Almazan R, Drabick C, Trudo EW, Jr, Colwell RR. 1991. Aeromonas jandaei and Aeromonas veronii dual infection of a human wound following aquatic exposure. J. Clin. Microbiol. 29:565-569.
17. T: Jack of all trades. J. Bacteriol. 188:8272-8282.
18. Morgan DR, Johnson PC, DuPont HL, Satterwhite TK, Wood LV. 1985. Lack of correlation between known virulence properties of Aeromonas hydrophila and enteropathogenicity for humans. Infect. Immun. 50: 62-65.
19. 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.
20. 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 N-acylhomoserine lactones. Microbiology 143:3703-3711.
21. Jangid K, Kong R, Patole MS, Shouche YS. 2007. luxRI homologs are universally present in the genus Aeromonas. BMC Microbiol. 7:93. http://dx.doi.10.1186/1471-2180-7-93.
22. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
23. Gracey M, Burke V, Robinson J. 1982. Aeromonas-associated gastroenteritis. Lancet ii:1304-1306.
24. Rautelin H, Hänninen ML, Sivonen A, Turunen U, Valtonen V. 1995. Chronic diarrhea due to a single strain of Aeromonas caviae. Eur. J. Clin. Microbiol. Infect. Dis. 14:51-53.
25. Chopra AK, Houston CW. 1999. Enterotoxins in Aeromonas-associated gastroenteritis. Microbes Infect. 1:1129-1137.
26. Janda JM, Abbott SL. 1998. Evolving concepts regarding the genus Aeromonas: an expanding panorama of species, disease presentations, and unanswered questions. Clin. Infect. Dis. 27:332-344.
27. Pukatzki S, McAuley SB, Miyata ST. 2009. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12:11-17.
28. 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.
29. Sierra JC, Suarez G, Sha J, Foltz SM, Popov VL, Galindo CL, Garner HR, Chopra AK. 2007. Biological characterization of a new type III se- cretion system effector from a clinical isolate of Aeromonas hydrophila- part II. Microb. Pathog. 43:147-160.
30. Zhang YL, Arakawa E, Leung KY. 2002. Novel Aeromonas hydrophila PPD134/91 genes involved in O-antigen and capsule biosynthesis. Infect. Immun. 70:2326-2335.
31. Tomich M, Herfst CA, Golden JW, Mohr CD. 2002. Role of flagella in host cell invasion by Burkholderia cepacia. Infect. Immun. 70:1799-1806.
32. Merino S, Rubires X, Aguilar A, Tomás JM. 1997. The role of flagella and motility in the adherence and invasion to fish cell lines by Aeromonas hydrophila serogroup O:34 strains. FEMS Microbiol. Lett. 151:213-217.
33. 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.10.1186/1471-2164-9-427.
34. Kearns DB. 2010. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 8:634-644.
35. Mattick JS. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289-314.
36. Thurlow LR, Hanke ML, Fritz T, Angle A, Aldrich A, Williams SH, Engebretsen IL, Bayles KW, Horswill AR, Kielian T. 2011. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J. Immunol. 186:6585-6596.
37. Kozlova EV, Khajanchi BK, Popov VL, Wen J, Chopra AK. 2012. Impact of QseBC system in c-di-GMP-dependent quorum sensing regulatory network in a clinical isolate SSU of Aeromonas hydrophila. Microb. Pathog. 53:115-124.
38. Kozlova EV, Khajanchi BK, Sha J, Chopra AK. 2011. Quorum sensing and c-di-GMP-dependent alterations in gene transcripts and virulenceassociated phenotypes in a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 50:213-223.
39. 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.
40. Swift S, Lynch MJ, Fish L, Kirke DF, Tomás JM, Stewart GS, Williams P. 1999. Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect. Immun. 67:5192-5199.
41. 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.
42. Joseph LA, Wright AC. 2004. Expression of Vibrio vulnificus capsular polysaccharide inhibits biofilm formation. J. Bacteriol. 186:889-893.
43. Enos-Berlage JL, Guvener ZT, Keenan CE, McCarter LL. 2005. Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol. Microbiol. 55:1160-1182.
44. Chopra AK, Xu X, Ribardo D, Gonzalez M, Kuhl K, Peterson JW, Houston CW. 2000. The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infect. Immun. 68:2808-2818.
45. 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.
46. 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.
47. 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.
48. Ly KT, Casanova JE. 2007. Mechanisms of Salmonella entry into host cells. Cell. Microbiol. 9:2103-2111.
49. Burdette DL, Yarbrough ML, Orvedahl A, Gilpin CJ, Orth K. 2008. Vibrio parahaemolyticus orchestrates a multifaceted host cell infection by induction of autophagy, cell rounding, and then cell lysis. Proc. Natl. Acad. Sci. U. S. A. 105:12497-12502.
50. Konradt C, Frigimelica E, Nothelfer K, Puhar A, Salgado-Pabon W, di Bartolo V, Scott-Algara D, Rodrigues CD, Sansonetti PJ, Phalipon A. 2011. The Shigella flexneri type three secretion system effector IpgD inhibits T cell migration by manipulating host phosphoinositide metabolism. Cell Host Microbe 9:263-272.
51. 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.
52. Ljungh A, Wadström T. 1981. Aeromonas toxins. Pharmacol. Ther. 15: 339-354.
53. Nieto TP, Ellis AE. 1986. Characterization of extracellular metallo- and serine-proteases of Aeromonas hydrophila strain B51. J. Gen. Microbiol. 132:1975-1979.
54. Leung KY, Stevenson RM. 1988. Tn5-induced protease-deficient strains of Aeromonas hydrophila with reduced virulence for fish. Infect. Immun. 56:2639-2644.
55. Sakai DK. 1985. Loss of virulence in a protease-deficient mutant of Aeromonas salmonicida. Infect. Immun. 48:146-152.
56. Daher RK, Filion G, Tan SG, Dallaire-Dufresne S, Paquet VE, Charette SJ. 2011. Alteration of virulence factors and rearrangement of pAsa5 plasmid caused by the growth of Aeromonas salmonicida in stressful conditions. Vet. Microbiol. 152:353-360.
57. Tanaka KH, Dallaire-Dufresne S, Daher RK, Frenette M, Charette SJ. 2012. An insertion sequence-dependent plasmid rearrangement in Aeromonas salmonicida causes the loss of the type three secretion system. PLoS One 7:e33725. http://dx.doi.10.1371/journal.pone.0033725.
58. Poole K. 2012. Bacterial stress responses as determinants of antimicrobial resistance. J. Antimicrob. Chemother. 67:2069-2089.
59. Daily OP, Joseph SW, Coolbaugh JC, Walker RI, Merrell BR, Rollins DM, Seidler RJ, Colwell RR, Lissner CR. 1981. Association of Aeromonas sobria with human infection. J. Clin. Microbiol. 13:769-777.
60. Joseph SW, Carnahan AM. 2000. Update on the genus Aeromonas. ASM News 66:218-223.
61. Carnahan AM, Behram S, Joseph SW. 1991. Aerokey II: a flexible key for identifying clinical Aeromonas species. J. Clin. Microbiol. 29:2843-2849.
62. 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.
63. 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, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM, Rothberg JM. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380.
64. 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.10.1186/1471-2164-9-75.
65. 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.
66. Li Y, Liu Y, Zhou Z, Huang H, Ren Y, Zhang Y, Li G, Zhou Z, Wang L. 2011. Complete genome sequence of Aeromonas veronii strain B565. J. Bacteriol. 193:3389-3390.
67. Beatson SA, das Graças 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.
68. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crécy-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, Rückert 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.
69. Richter M, Rosselló-Móra R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. U. S. A. 106: 19126-19131.
70. 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.
71. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis comparison tool. Bioinformatics 21: 3422-3423.
72. Gavín R, Rabaan AA, Merino S, Tomás JM, Gryllos I, Shaw JG. 2002. Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43:383-397.
73. 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.
74. 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.
75. 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 ofN-acylhomoserine lactone. Appl. Environ. Microbiol. 73:6339-6344.
76. Sha J, Lu M, Chopra AK. 2001. Regulation of the cytotoxic enterotoxin gene in Aeromonas hydrophila: characterization of an iron uptake regulator. Infect. Immun. 69:6370-6381.
77. Erova TE, Sha J, Horneman AJ, Borchardt MA, Khajanchi BK, Fadl AA, Chopra, AK. 2007. Identification of a new hemolysin from diarrheal isolate SSU of Aeromonas hydrophila. FEMS Microbiol. Lett. 275: 301-311.
78. Erova TE, Pillai L, Fadl AA, Sha J, Wang S, Galindo CL, Chopra AK. 2006.DNAadenine methyltransferase influences the virulence of Aeromonas hydrophila. Infect. Immun. 74:410-424.