Aeromonas hydrophila and Aeromonas veronii predominate among potentially pathogenic ciprofloxacin- and tetracycline-resistant Aeromonas isolates from Lake Erie

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 841-848

  Skwor, Troy ^a,b,c   Shinko, Jasmine ^c   Augustyniak, Alexander ^c   Gee, Christopher ^d   Andraso, Greg ^c  

^a Starr Science Building   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c GANNON UNIVERSITY   (United States)

^d BEHREND COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEROMONAS HYDROPHILA; ANTIBIOTIC RESISTANCE; CULTURABLE BACTERIA; HUMAN EPITHELIAL CELLS; PATHOGENIC STRAINS; PHYLOGENETIC ANALYSIS; RELATIVE ABUNDANCE; RESTRICTION FRAGMENT LENGTH POLYMORPHISMS;

AMINO ACIDS; ANTIBIOTICS; LAKES; RNA; WATER QUALITY;

GENES;

ANTIBIOTIC RESISTANCE; ANTIBIOTICS; ASSESSMENT METHOD; BACTERIUM; CYTOPLASM; PATHOGEN; PATHOGENICITY; PHYLOGENETICS; POLYMERASE CHAIN REACTION; POLYMORPHISM; RELATIVE ABUNDANCE; VIRULENCE; WATER QUALITY;

GREAT LAKES [NORTH AMERICA]; LAKE ERIE;

ANTIINFECTIVE AGENT; CIPROFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING); RNA 16S; TETRACYCLINE; VIRULENCE FACTOR;

AEROMONAS; ANTIBIOTIC RESISTANCE; ARTICLE; CELL SURVIVAL; CLASSIFICATION; DNA SEQUENCE; DRUG EFFECT; EPITHELIUM CELL; GENETICS; HEMOLYSIS; ISOLATION AND PURIFICATION; LAKE; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

AEROMONAS; ANTI-BACTERIAL AGENTS; CELL SURVIVAL; CIPROFLOXACIN; DNA GYRASE; DRUG RESISTANCE, BACTERIAL; EPITHELIAL CELLS; HEMOLYSIS; LAKES; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; TETRACYCLINE; VIRULENCE FACTORS;

EID: 84892975310     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03645-13     Document Type: Article

References (53)

1. Sinha S, Shimada T, Ramamurthy T, Bhattacharya SK, Yamasaki S, Takeda Y, Nair GB. 2004. Prevalence, serotype distribution, antibiotic susceptibility and genetic profiles of mesophilic Aeromonas species isolated from hospitalized diarrhoeal cases in Kolkata, India. J. Med. Microbiol. 53:527-534. http://dx.doi.org/10.1099/jmm.0.05269-0.
2. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF. 2011. Evidence for a core gut microbiota in the zebrafish. ISME J. 5:1595-1608. http://dx.doi.org/10.1038/ismej.2011.38.
3. Nonomura H, Kato N, Ohno Y, Itokazu M, Matsunaga T, Watanabe K. 1996. Indigenous bacterial flora of medicinal leeches and their susceptibilities to 15 antimicrobial agents. J. Med. Microbiol. 45:490-493. http: //dx.doi.org/10.1099/00222615-45-6-490.
4. Gu J-D, Mitchell R. 2002. Indigenous microflora and opportunistic pathogens of the freshwater zebra mussel, Dreissena polymorpha. Hydrobiologia 474:81-90. http://dx.doi.org/10.1023/A:1016517107473.
5. Janda JM, Abbott SL. 2010. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev. 23:35-73. http://dx.doi.org/10.1128/CMR.00039-09.
6. Ewart KV, Belanger JC, Williams J, Karakach T, Penny S, Tsoi SC, Richards RC, Douglas SE. 2005. Identification of genes differentially expressed in Atlantic salmon (Salmo salar) in response to infection by Aeromonas salmonicida using cDNA microarray technology. Dev. Comp. Immunol. 29:333-347. http://dx.doi.org/10.1016/j.dci.2004.08.004.
7. Toranzo AE, Magarinos B, Romalde JL. 2005. A review of the main bacterial fish diseases in mariculture systems. Aquaculture 246:37-61. http://dx.doi.org/10.1016/j.aquaculture.2005.01.002.
8. Rahman M, Colque-Navarro P, Kuhn I, Huys G, Swings J, Mollby R. 2002. Identification and characterization of pathogenic Aeromonas veronii biovar sobria associated with epizootic ulcerative syndrome in fish in Bangladesh. Appl. Environ. Microbiol. 68:650-655. http://dx.doi.org/10.1128/AEM.68.2.650-655.2002.
9. Deodhar LP, Saraswathi K, Varudkar A. 1991. Aeromonas spp. and their association with human diarrheal disease. J. Clin. Microbiol. 29:853-856.
10. 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.
11. 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-E96. http://dx.doi.org/10.1086/497372.
12. Maegele M, Gregor S, Steinhausen E, Bouillon B, Heiss MM, Perbix W, Wappler F, Rixen D, Geisen J, Berger-Schreck B, Schwarz R. 2005. The long-distance tertiary air transfer and care of tsunami victims: injury pattern and microbiological and psychological aspects. Crit. Care Med. 33: 1136-1140. http://dx.doi.org/10.1097/01.CCM.0000163269.42524.50.
13. Mukhopadhyay C, Bhargava A, Ayyagari A. 2003. Aeromonas hydrophila and aspiration pneumonia: a diverse presentation. Yonsei Med. J. 44: 1087-1090.
14. Ko WC, Yu KW, Liu CY, Huang CT, Leu HS, Chuang YC. 1996. Increasing antibiotic resistance in clinical isolates of Aeromonas strains in Taiwan. Antimicrob. Agents Chemother. 40:1260-1262.
15. Vila J, Ruiz J, Gallardo F, Vargas M, Soler L, Figueras MJ, Gascon J. 2003. Aeromonas spp. and traveler's diarrhea: clinical features and antimicrobial resistance. Emerg. Infect. Dis. 9:552-555. http://dx.doi.org/10.3201/eid0905.020451.
16. Want SV, Millership SE. 1990. Effects of incorporating ampicillin, bile salts and carbohydrates in media on the recognition and selection of Aeromonas spp. from faeces. J. Med. Microbiol. 32:49-54. http://dx.doi.org/10.1099/00222615-32-1-49.
17. Goni-Urriza M, Capdepuy M, Arpin C, Raymond N, Caumette P, Quentin C. 2000. Impact of an urban effluent on antibiotic resistance of riverine Enterobacteriaceae and Aeromonas spp. Appl. Environ. Microbiol. 66:125-132. http://dx.doi.org/10.1128/AEM.66.1.125-132.2000.
18. U.S. Environmental Protection Agency. 2001. Method 1605: Aeromonas in finished water by membrane filtration using ampicillin-dextrin agar with vancomycin (ADA-V). Reference no. EPA-821-R-01-034. U.S. Environmental Protection Agency, Office of Water, Washington, DC.
19. Handfield M, Simard P, Letarte R. 1996. Differential media for quantitative recovery of waterborne Aeromonas hydrophila. Appl. Environ. Microbiol. 62:3544-3547.
20. Aravena-Roman M, Inglis TJJ, Henderson B, Riley TV, Chang BJ. 2012. Antimicrobial susceptibilities of Aeromonas strains isolated from clinical and environmental sources to 26 antimicrobial agents. Antimicrob. Agents Chemother. 56:1110-1112. http://dx.doi.org/10.1128/AAC.05387-11.
21. Borrell N, Acinas SG, Figueras MJ, Martinez-Murcia AJ. 1997. Identification of Aeromonas clinical isolates by restriction fragment length polymorphism of PCR-amplified 16S rRNA genes. J. Clin. Microbiol. 35:1671- 1674.
22. Martino ME, Fasolato L, Montemurro F, Rosteghin M, Manfrin A, Patarnello T, Novelli E, Cardazzo B. 2011. Determination of microbial diversity of Aeromonas strains on the basis of multilocus sequence typing, phenotype, and presence of putative virulence genes. Appl. Environ. Microbiol. 77:4986-5000. http://dx.doi.org/10.1128/AEM.00708-11.
23. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
24. 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.
25. Tamura K, Nei M, Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. U. S. A. 101:11030-11035. http://dx.doi.org/10.1073/pnas.0404206101.
26. Cumberbatch N, Gurwith MJ, Langston C, Sack RB, Brunton JL. 1979. Cytotoxic enterotoxin produced by Aeromonas hydrophila: relationship of toxigenic isolates to diarrheal disease. Infect. Immun. 23:829-837.
27. Nam IY, Joh K. 2007. Rapid detection of virulence factors of Aeromonas isolated from a trout farm by hexaplex-PCR. J. Microbiol. 45:297-304.
28. Igbinosa IH, Okoh AI. 2012. Antibiotic susceptibility profile of Aeromonas species isolated from wastewater treatment plant. ScientificWorld-Journal 2012:764563. http://dx.doi.org/10.1100/2012/764563.
29. Obi CL, Ramalivhana J, Samie A, Igumbor EO. 2007. Prevalence, pathogenesis, antibiotic susceptibility profiles, and in-vitro activity of selected medicinal plants against Aeromonas isolates from stool samples of patients in the Venda region of South Africa. J. Health Popul. Nutr. 25:428-435.
30. Leslie H. 2007. Beach management by DCNR, p 16-28. In Beach closures at Presque Isle State Park: Past, Present, and Future Conference proceedings. US Department of Commerce, National Technical Information Service, Alexandria, VA.
31. Worthen PL, Gode CJ, Graf J. 2006. Culture-independent characterization of the digestive-tract microbiota of the medicinal leech reveals a tripartite symbiosis. Appl. Environ. Microbiol. 72:4775-4781. http://dx.doi.org/10.1128/AEM.00356-06.
32. Andraso GM. 2005. Summer food habits of pumpkinseeds (Lepomis gibbosus) and bluegills (Lepomis macrochirus) in Presque Isle Bay, Lake Erie. J. Great Lakes Res. 31:397- 404. http://dx.doi.org/10.1016/S0380 -1330(05)70271-9.
33. Andraso GM, Ganger MT, Adamczyk J. 2011. Size-selective predation by round gobies (Neogobius melanostomus) on dreissenid mussels in the field. J. Great Lakes Res. 37:298-304. http://dx.doi.org/10.1016/j.jglr.2011.02.006.
34. Moura A, Oliveira C, Henriques I, Smalla K, Correia A. 2012. Broad diversity of conjugative plasmids in integron-carrying bacteria from wastewater environments. FEMS Microbiol. Lett. 330:157-164. http://dx.doi.org/10.1111/j.1574-6968.2012.02544.x.
35. Borrego JJ, Morinigo MA, Martinez-Manzanares E, Bosca M, Castro D, Barja JL, Toranzo AE. 1991. Plasmid associated virulence properties of environmental isolates of Aeromonas hydrophila. J. Med. Microbiol. 35: 264-269. http://dx.doi.org/10.1099/00222615-35-5-264.
36. Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P. 2008. Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp. Emerg. Infect. Dis. 14:231-237. http://dx.doi.org/10.3201/eid1402.070677.
37. Han JE, Kim JH, Choresca CH, Jr, Shin SP, Jun JW, Chai JY, Park SC. 2012. A small IncQ-type plasmid carrying the quinolone resistance (qnrS2) gene from Aeromonas hydrophila. Lett. Appl. Microbiol. 54:374- 376. http://dx.doi.org/10.1111/j.1472-765X.2012.03208.x.
38. Figueira V, Vaz-Moreira I, Silva M, Manaia CM. 2011. Diversity and antibiotic resistance of Aeromonas spp. in drinking and waste water treatment plants. Water Res. 45:5599-5611. http://dx.doi.org/10.1016/j.watres.2011.08.021.
39. Han JE, Kim JH, Cheresca CH, Jr, Shin SP, Jun JW, Chai JY, Han SY, Park SC. 2012. First description of the qnrS-like (qnrS5) gene and analysis of quinolone resistance-determining regions in motile Aeromonas spp. from diseased fish and water. Res. Microbiol. 163:73-79. http://dx.doi.org /10.1016/j.resmic.2011.09.001.
40. 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-tohuman transmission. Appl. Environ. Microbiol. 76:2313-2325. http://dx.doi.org/10.1128/AEM.02535-09.
41. Bo JN, Howard SP. 1991. Mutagenesis and isolation of Aeromonas hydrophila genes which are required for extracellular secretion. J. Bacteriol. 173:1241-1249.
42. Burr SE, Stuber K, Wahli T, Frey J. 2002. Evidence for a type III secretion system in Aeromonas salmonicida subsp. salmonicida. J. Bacteriol. 184: 5966-5970. http://dx.doi.org/10.1128/JB.184.21.5966-5970.2002.
43. 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.
44. 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.
45. Leung KY, Siame BA, Snowball H, Mok YK. 2011. Type VI secretion regulation: crosstalk and intracellular communication. Curr. Opin. Microbiol. 14:9-15. http://dx.doi.org/10.1016/j.mib.2010.09.017.
46. Maltz M, Graf J. 2011. The type II secretion system is essential for erythrocyte lysis and gut colonization by the leech digestive tract symbiont Aeromonas veronii. Appl. Environ. Microbiol. 77:597-603. http://dx.doi.org/10.1128/AEM.01621-10.
47. Sha J, Pillai L, Fadl AA, Galindo CL, Erova TE, Chopra AK. 2005. The type III secretion system and cytotoxic enterotoxin alter the virulence of Aeromonas hydrophila. Infect. Immun. 73:6446-6457. http://dx.doi.org /10.1128/IAI.73.10.6446-6457.2005.
48. 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.
49. Swift S, Lynch MJ, Fish L, Kirke DF, Tomas JM, Stewart GS, Williams P. 1999. Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect. Immun. 67:5192-5199.
50. Rodriguez LA, Ellis AE, Nieto TP. 1992. Purification and characterisation of an extracellular metalloprotease, serine protease and haemolysin of Aeromonas hydrophila strain B32: all are lethal for fish. Microb. Pathog. 13:17-24. http://dx.doi.org/10.1016/0882-4010(92)90028-M.
51. Wong CY, Heuzenroeder MW, Flower RL. 1998. Inactivation of two haemolytic toxin genes in Aeromonas hydrophila attenuates virulence in a suckling mouse model. Microbiology 144:291-298. http://dx.doi.org/10.1099/00221287-144-2-291.
52. Hu M, Wang N, Pan ZH, Lu CP, Liu YJ. 2012. Identity and virulence properties of Aeromonas isolates from diseased fish, healthy controls and water environment in China. Lett. Appl. Microbiol. 55:224-233. http://dx.doi.org/10.1111/j.1472-765X.2012.03281.x.
53. Vipond R, Bricknell IR, Durant E, Bowden TJ, Ellis AE, Smith M, MacIntyre S. 1998. Defined deletion mutants demonstrate that the major secreted toxins are not essential for the virulence of Aeromonas salmonicida. Infect. Immun. 66:1990-1998.