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Characterization and virulence potential of phenotypically diverse Aeromonas veronii isolates recovered from moribund freshwater ornamental fishes of Kerala, India

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Abstract

In the present study, we investigated the involvement of Aeromonas spp. in eliciting disease outbreaks in freshwater ornamental fishes across the state of Kerala, India. We investigated three incidences of disease, in which the moribund fishes exhibited clinical signs such as haemorrhagic septicemia (in gouramy, Trichogaster sp.), dropsy (in Oscar, Astronotus ocellatus) and tail rot/fin rot (in gold fish, Carassius carassius). Pure cultures (n = 20 from each fish; 60 in total) of Aeromonas spp. were recovered from the abdominal fluid as well as from internal organs of affected fishes, although they could not be identified to species level because of the variations in their phenotypic characters. The molecular fingerprinting of the isolates using Enterobacterial Repetitive Intergenic Consensus PCR proved the genetic diversity of the isolates from the three sites. The phylogenetic trees constructed using concatenated sequences (using 16S rRNA, gyrA, gyrB and rpoD genes) indicated that they were related to Aeromonas veronii. They exhibited marked cytotoxic and haemolytic activity, which were responsible for the pathogenic potential of the isolates. The isolates possessed multiple virulence genes such as enterotoxins (act and alt), haemolytic toxins (aerA and hlyA), genes involved in type III secretion system (ascV, aexT and ascF–ascG), glycerophospholipid-cholesterol acyltransferase (gcat) and a type IV pilus (tapA) gene, as determined by PCR. Virulence of representative isolates to goldfish was also tested, and we found LD50 values of 104.07–105.35 cfu/fish. Furthermore, the organisms could be recovered as pure cultures from the lesions as well as from the internal organs.

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References

  • Abbott SL, Wendy KW, Cheung, Janda JM (2003) The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J Clin Microbiol 41(6):2348–2357

    Article  PubMed  CAS  Google Scholar 

  • Aguilera-Arreola MG, Hernández-Rodriguez C, Zúňiga G, Figueras MJ, Garduňo RA, Castro-Escarpulli G (2007) Virulence potential and genetic diversity of Aeromonas caviae, A. veronii and A. hydrophila clinical isolates from Mexico and Spain: a comparative study. Can J Microbiol 53:877–887

    Article  PubMed  CAS  Google Scholar 

  • Albert MJ, Ansaruzzaman M, Talukder KA, Chopra AK, Rahman KM, Faruque AS, Islam MS, Sack RB, Mollby R (2000) Prevalence of enterotoxin genes in Aeromonas spp. isolated from children with diarrhea, healthy controls, and the environment. J Clin Microbiol 38(10):3785–3790

    PubMed  CAS  Google Scholar 

  • Alperi A, Martınez-Murcia AJ, Ko WC, Monera A, Saavedra MJ, Figueras MJ (2010) Aeromonas taiwanensis sp. nov. and Aeromonas sanarellii sp. nov., two new clinical species from Taiwan. Int J Syst Evol Microbiol 60:2048–2055

    Article  PubMed  CAS  Google Scholar 

  • Altwegg M, Steigerwalt AG, Altwegg-Bissig R, Luthy-Hottenstein J, Brenner DJ (1990) Biochemical identification of Aeromonas genospecies isolated from humans. J Clin Microbiol 28:258–264

    PubMed  CAS  Google Scholar 

  • Ando E, Monden K, Mitsuhata R, Kariyama R, Kumon H (2004) Biofilm formation among methicillin-resistant Staphylococcus aureus isolates from patients with urinary tract infection. Acta Med Okayama 58(4):207–214

    PubMed  CAS  Google Scholar 

  • APHA (1995) Standard Methods for the Examination of Water and Wastewater, 20th edn. American Public Health Association/American Water Works Association/Water Environment Federation, Washington, DC

    Google Scholar 

  • Ballal M, Rajeswari A, Bindu M, Shivananda C (2001) Correlation of the suicide phenomenon in Aeromonas species with virulence and enteropathogenicity. Indian J Pathol Microbiol 44(4):421–425

    PubMed  CAS  Google Scholar 

  • Barnett TC, Kirov SM, Strom MS, Sanderson K (1997) Aeromonas spp. possesses at least two distinct type IV pilus families. Microb Pathog 23:241–247

    Article  PubMed  CAS  Google Scholar 

  • Bar-Or Y (1990) Hydrophobicity in the aquatic environment. In: Doyle RJ, Rosenberg M (eds) Microbial cell surface hydrophobicity. American Society for Microbiology, Washington, DC, pp 211–228

    Google Scholar 

  • Bates JM, Mittge E, Kuhlman J, Baden KN, Cheesman SE (2006) Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297:374–386

    Article  PubMed  CAS  Google Scholar 

  • Beaz-Hidalgo R, Alperi R, Buján N, Romalde JL, Figueras MJ (2010) Comparison of phenotypical and genetic identification of Aeromonas strains isolated from diseased fish. Syst Appl Microbiol 33:149–153

    Article  PubMed  Google Scholar 

  • Boyd JM, Dacanay A, Knickle LC, Touhami A, Brown LL, Jericho MH, Johnson SC, Reith M (2008) Contribution of type IV pili to the virulence of Aeromonas salmonicida subsp. salmonicida in Atlantic salmon (Salmo salar L.). Infect Immun 76:1445–1455

    Article  PubMed  CAS  Google Scholar 

  • Burr SE, Frey J (2007) Analysis of type III effector genes in typical and atypical Aeromonas salmonicida. J Fish Dis 30:711–714

    Article  PubMed  CAS  Google Scholar 

  • Burr SE, Pugovkin D, Wahli T, Segner H, Frey J (2005) Attenuated virulence of an Aeromonas salmonicida subsp. salmonicida type III secretion mutant in a rainbow trout model. Microbiology 151:2111–2118

    Article  PubMed  CAS  Google Scholar 

  • Cai SH, Wu ZH, Jian JC, Lu YS, Tang JF (2012) Characterization of pathogenic Aeromonas veronii bv. veronii associated with ulcerative syndrome from Chinese longsnout catfish (Leiocassis longirostris Günther). Braz. J Microbiol 43(1): doi:10.1590/S1517-83822012000100046

  • Carnahan AM, Altwegg M (1996) Taxonomy. In: Austin B, Altwegg M, Gosling PJ, Joseph S (eds) The genus Aeromonas. Wiley, New York, pp 1–38

    Google Scholar 

  • Chopra AK, Xu XJ, Ribardo D, Gonzalez M, Kuhl K, Petersojn JW, Houston CW (2000) The cytotoxic enterotoxic of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infect Immun 68:2808–2818

    Article  PubMed  CAS  Google Scholar 

  • Coquet L, Cosette P, Junter GA, Beucher E, Saiter JM, Jouenne T (2002) Adhesion of Yersinia ruckeri to fish farm materials: influence of cell and material surface properties. Colloids Surf B 26:373–378

    Google Scholar 

  • Dacanay A, Knickle L, Solanky KS, Boyd JM, Walter JA, Brown LL, Johnson SC, Reith M (2006) Contribution of the type III secretion system (TTSS) to virulence of Aeromonas salmonicida subsp. salmonicida. Microbiology 152:1847–1856

    Article  PubMed  CAS  Google Scholar 

  • Dooley JSG, Trust TJ (1988) Surface protein composition of Aeromonas hydrophila strains virulent for fish: identification of a surface array protein. J Bacteriol 170:499–506

    PubMed  CAS  Google Scholar 

  • Esteve C, Alcaide E, Canals R, Merino S, Blasco D, Figueras MJ, Tomas JM (2004) Pathogenic Aeromonas hydrophila Serogroup O:14 and O:81 strains with an S layer. Appl Environ Microbiol 70(10):5898–5904

    Article  PubMed  CAS  Google Scholar 

  • Fehr D, Burr SE, Gilbert M, Alayer J, Frey J, Popoff MR (2007) Aeromonas exoenzyme T of Aeromonas salmonicida is a bifunctional protein that targets the host cytoskeleton. J Biol Chem 282(39):28843–28852

    Article  PubMed  CAS  Google Scholar 

  • Figueras MJ, Alperi A, Beaz-Hidalgo R, Stackebrandt E, Brambilla E, Monera A, Martinez-Murcia AJ (2011) Aeromonas rivuli sp. nov., isolated from the upstream region of a karst water rivulet. Int J Syst Evol Microbiol 61:242–248

    Article  PubMed  CAS  Google Scholar 

  • Freeman DJ, Elakliner FR, Keane CT (1989) New method for detecting slime producing by coagulase negative Staphylococci. J Clin Pathol 42:872–874

    Article  PubMed  CAS  Google Scholar 

  • Ghosh P (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68:771–795

    Article  PubMed  CAS  Google Scholar 

  • Golden NJ, Acheson DWK (2002) Identification of motility and auto agglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect Immun 70(4):1761–1771

    Article  PubMed  CAS  Google Scholar 

  • Goni-Urriza M, Arpin C, Capdepuy M, Dubois V, Caumette P, Quentin C (2002) Type II topoisomerase quinolone resistance-determining regions of Aeromonas caviae, A. hydrophila, and A. sobria complexes and mutations associated with quinolone resistance. Antimicrob Agents Chemother 46:350–359

    Article  PubMed  CAS  Google Scholar 

  • Graf J, Kikuchi Y, Rio RV (2006) Leeches and their microbiota: naturally simple symbiosis models. Trends Microbiol 14:365–371

    Article  PubMed  CAS  Google Scholar 

  • Graham S, Jeffries AH, Secombes CJ (1988) A novel assay to detect macrophage bactericidal activity in fish: factors influencing the killing of Aeromonas salmonicida. J Fish Dis 11:389–396

    Article  Google Scholar 

  • Greenman SB, Rutten MJ, Fowler WM, Scheffler L, Shortridge LA, Brown B, Sheppard BC, Deveney KE, Deveney CW, Trunkey DD (1997) Herbicide/pesticide effects on intestinal epithelial growth. Environ Res 75:85–93

    Article  PubMed  CAS  Google Scholar 

  • Han HJ, Taki T, Kondo H, Hirono I, Aoki T (2008) Pathogenic potential of a collagenase gene from Aeromonas veronii. Can J Microbiol 54:1–10

    Article  PubMed  CAS  Google Scholar 

  • Heuzenroeder MW, Wong CYF, Flower RLP (1999) Distribution of two hemolytic toxin genes in clinical and environmental isolates of Aeromonas spp.: correlation with virulence in a suckling mouse model. FEMS Microbiol Lett 174(1):131–136

    Article  PubMed  CAS  Google Scholar 

  • Hossain M (2008) Isolation of pathogenic bacteria from the skin ulcerous symptomatic gourami (Colisa lalia) through 16S rDNA analysis. Univ J Zool Rajshahi Univ 27:21–24

    Google Scholar 

  • Hulton CSJ, Higgins CF, Sharp PM (1991) ERIC sequences: a novel family of repetitive elements in the genomes of Escherichia coli, Salmonella typhimurium and other enterobacteria. Mol Microbiol 5:825–834

    Article  PubMed  CAS  Google Scholar 

  • Janda JM (1987) Aeromonas and Plesiomonas infections. In: Wentworth BB (ed) Diagnostic procedures for bacterial infection. American Public Health Association, Washington, DC, pp 37–44

    Google Scholar 

  • Janda JM, Abbott SL (2010) The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23:35–73

    Article  PubMed  CAS  Google Scholar 

  • Karunasagar I, Karunasagar I, Otta SK (2003) Disease problems affecting fish in tropical environments. J Appl Aquacult 13(3/4):231–249

    Article  Google Scholar 

  • Kingombe CIB, Huys G, Tonolla M, Albert MJ, Swings J, Peduzzi R (1999) PCR detection, characterization and distribution of virulence genes in Aeromonas spp. Appl Environ Microbiol 65:5293–5302

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Krovacek K, Faris A, Ahne W, Mansson I (1987) Adhesion of Aeromonas hydrophila and Vibrio anguillarum to fish cells and to mucus coated slides. FEMS Microbiol Lett 42:85–89

    Article  CAS  Google Scholar 

  • Krzyminska S, Mokracka J, Koczura R, Cwiertnia A, Kaznowski A (2012) Aeromonas spp.-mediated cell-contact cytotoxicity is associated with the presence of type III secretion system. Antonie van Leeuwenhoek 101(2):243–251

    Article  PubMed  CAS  Google Scholar 

  • Lallier R, Daigneault P (1984) Antigenic differentiation of pili from non-virulent fish pathogenic strains of Aeromonas hydrophila. J Fish Dis 7:509–572

    Article  Google Scholar 

  • Lavender HF, Jagnow JR, Clegg S (2004) Biofilm formation in vitro and virulence in vivo of mutants of Klebsiella pneumoniae. Infect Immun 72:4888–4890

    Article  PubMed  CAS  Google Scholar 

  • Lee KK, Yii KC (1996) A comparison of three methods for assaying hydrophobicity of pathogenic vibrios. Lett Appl Microbiol 23:343–346

    Article  CAS  Google Scholar 

  • Lilenbaum W, Nunes ELC, Azeredo MAI (1998) Prevalence and antimicrobial susceptibility of Staphylococci isolated from the skin surface of clinically normal cats. Lett Appl Microbiol 27:224–228

    Article  PubMed  CAS  Google Scholar 

  • Ma Z, Yang H, Li T, Luo L, Gao J (2009) Isolation and identification of pathogenic Aeromonas veronii isolated from infected Siberian sturgeon (Acipenser baerii). Wei Sheng Wu Xue Bao 49(10):1289–1294

    PubMed  CAS  Google Scholar 

  • Masada CL, LaPatra SE, Morton AW, Strom MS (2002) An Aeromonas salmonicida type IV pilin is required for virulence in rainbow trout Oncorhynchus mykiss. Dis Aqua Organ 15:13–25

    Article  Google Scholar 

  • Masignani V, Pizza M, Rappuoli R (2006) Molecular, functional, and evolutionary aspects of ADP ribosylating toxins. In: Alouf JE, Popoff MR (eds) The comprehensive sourcebook of bacterial protein toxins. Elsevier, Amsterdam

    Google Scholar 

  • Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56:289–314

    Article  PubMed  CAS  Google Scholar 

  • Misawa N, Blaser MJ (2000) Detection and characterization of auto agglutination activity by Campylobacter jejuni. Infect Immun 68(11):6168–6175

    Article  PubMed  CAS  Google Scholar 

  • Mittal KR, Lalonde G, Leblanc D, Olivier G, Lallier GR (1980) Aeromonas hydrophila in rainbow trout: relation between virulence and surface characteristics. Can J Microbiol 26:1501–1503

    Article  PubMed  CAS  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival, application to proliferation and cytotoxicity assays. J Immun Methods 65:55–63

    Article  CAS  Google Scholar 

  • Namdari H, Bottone EJ (1988) Correlation of the suicide phenomenon in Aeromonas species with virulence and enteropathogenicity. J Clin Microbiol 26(12):2615–2619

    PubMed  CAS  Google Scholar 

  • Nerland AH (1996) The nucleotide sequence of the gene encoding GCAT from Aeromonas salmonicida ssp. salmonicida. J Fish Dis 19:145–150

    Article  CAS  Google Scholar 

  • Ormen O, Ostensvik O (2001) The occurrence of aerolysin-positive Aeromonas spp. and their cytotoxicity in Norwegian water sources. J Appl Microbiol 90:797–802

    Article  PubMed  CAS  Google Scholar 

  • Paniagua C, Rivero O, Anguita J, Naharro G (1990) Pathogenicity factors and virulence for rainbow trout (Salmo gairdneri) of motile Aeromonas sp. isolates from river. J Clin Microbiol 28:350–355

    PubMed  CAS  Google Scholar 

  • Parker JL, Shaw JG (2011) Aeromonas spp. clinical microbiology and disease. J Infect 62:109–118

    Article  PubMed  Google Scholar 

  • Paula SJ, Duffey PS, Abbott SL, Kokka RP, Oshiro LS, Janda JM, Shimada T, Sakazaki R (1988) Surface properties of auto agglutinating mesophilic aeromonads. Infect Immun 56:2658–2665

    PubMed  CAS  Google Scholar 

  • Peeters E, Nelis HJ, Coenye T (2008) Comparison of multiple methods for quantification of microbial biofilms grown in microtitre plates. J Microbiol Methods 72(2):157–165

    Article  PubMed  CAS  Google Scholar 

  • Pemberton JM, Kidd SP, Schmidt R (1997) Secreted enzymes of Aeromonas. FEMS Microbiol Lett 152:1–10

    Article  PubMed  CAS  Google Scholar 

  • Plumb JA, Hanson LH (2010) Health maintenance and principal microbial diseases of cultured fishes, 3rd edn. Wiley, New York

    Book  Google Scholar 

  • Puthucheary SD, Puah SM, Chua KH (2012) Molecular characterization of clinical isolates of aeromonas species from Malaysia. PLoS ONE 7(2):e30205

    Article  PubMed  CAS  Google Scholar 

  • Rahman M, Navarro CP, 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. Pak J Biol Sci 68(2):650–655

    CAS  Google Scholar 

  • Reddy GSM, Aggarwal RK, Matsumotto GI, Sivaji SI (2000) Arthrobacter flavus sp.nov., a psychrophilic bacterium isolated from a pond in McMurdo dry vally, Antarctica. Int J Syst Evol Microbiol 50:1553–1561

    Article  PubMed  CAS  Google Scholar 

  • Reed MJ, Muench M (1938) A simple method for estimating fifty percent endpoints. Am J Hyg 27:493–497

    Google Scholar 

  • Rosenberg K, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons, a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33

    Article  CAS  Google Scholar 

  • Sakai DK (1986) Electrostatic mechanism of survival of virulent Aeromonas salmonicida strains in river water. Appl Environ Microbiol 51:1343–1349

    PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Santos JA, Gonzalez CJ, Otero A, Garcia-Lopez ML (1999) Hemolytic and siderophore production in different Aeromonas species isolated from fish. Appl Environ Microbiol 65:5612–5614

    PubMed  CAS  Google Scholar 

  • Scoaris DDO, Colacite J, Nakamura CV, Nakamura TU, Filho BAA, Filho BPD (2008) Virulence and antibiotic susceptibility of Aeromonas spp. isolated from drinking water. Antonie van Leeuwenhoek 93:111–122

    Article  CAS  Google Scholar 

  • Senderovich Y, Ken-Dror S, Vainblat I, Blau D, Izhaki I, Halpern M (2012) A molecular study on the prevalence and virulence potential of aeromonas spp. recovered from patients suffering from diarrhea in Israel. PLoS ONE 7(2):e30070

    Article  PubMed  CAS  Google Scholar 

  • 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(4):1924–1935

    Article  PubMed  CAS  Google Scholar 

  • Sha J, Pillae 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

    Article  PubMed  CAS  Google Scholar 

  • Shames SR, Finlay BB (2010) Breaking the stereotypes: virulence factor-mediated protection of host cells in bacterial pathogenesis. PLoS Pathog 6:1–3

    Article  Google Scholar 

  • Silver AC, Graf J (2009) Prevalence of genes encoding the type three secretion system and the effectors aexT and aexU in the Aeromonas veronii group. DNA Cell Biol 28(8):383–388

    Article  PubMed  CAS  Google Scholar 

  • Silver AC, Williams D, Faucher J, Horneman AJ, Gogarten P, Graf J (2011) Complex evolutionary history of the Aeromonas veronii group revealed by host interaction and DNA sequence data. PLoS ONE 6(2):e1675

    Article  Google Scholar 

  • Singh DV, Sanyal SC (1992) Enterotoxicity of clinical and environmental isolates of Aeromonas spp. J Med Microbiol 36(4):269–272

    Article  PubMed  CAS  Google Scholar 

  • Smith P (2006) Breakpoints for disc diffusion susceptibility testing of bacteria associated with fish diseases, a review of current practice. Aquaculture 261(4):1113–1121

    Article  CAS  Google Scholar 

  • Strauss EJ, Falkow S (1997) Microbial pathogenesis: genomic and beyond. Science 276:707–712

    Article  PubMed  CAS  Google Scholar 

  • Stuber K, Frey J, Burnens AP, Kuhnert P (2003) Detection of type III secretion genes as a general indicator of bacterial virulence. Mol Cell Probes 17:25–32

    Article  PubMed  CAS  Google Scholar 

  • Swift S, Lynch JM, Fish L, Kirke DF, Tomas JM, Stewart GSAB, Williams P (1999) Quarum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect Immun 67(10):5192–5199

    PubMed  CAS  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tenover FC, Lancaster MV, Hill BC (1988) Characterization of staphylococci with reduced susceptibilities to vancomycin and other glycopeptides. J Clin Microbiol 36:1020–1027

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequences weighting, position - specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Trower CJ, Abo S, Majeed KN, von Itzstein M (2000) Production of an enterotoxin by a gastro-enteritis-associated Aeromonas strain. J Med Microbiol 49:121–126

    PubMed  CAS  Google Scholar 

  • van der Marel M, Schroers V, Neuhaus H, Steinhagen D (2008) Chemotaxis towards, adhesion to, and growth in carp gut mucus of two Aeromonas hydrophila strains with different pathogenicity for common carp, Cyprinus carpio L. J Fish Dis 31:321–330

    Article  PubMed  Google Scholar 

  • Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831

    Article  PubMed  CAS  Google Scholar 

  • Von Gravenitz A (2007) The role of Aeromonas in diarrhea: a review. Infection 35:59–64

    Article  Google Scholar 

  • Wang G, Clark CG, Liu C, Pucknell C, Munro CK, Kruk TMAC, Caldeira R, Woodward DL, Rodgers FG (2003) Detection and characterization of the hemolysin genes in Aeromonas hydrophila and Aeromonas sobria by multiplex PCR. J Clin Microbiol 41(3):31048–31054

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wu CJ, Wu JJ, Yan JJ, Lee HC, Lee NY, Chang CM, Shih HI, Wu HM, Wang LR, Ko WC (2007) Clinical significance and distribution of putative virulence markers of 116 consecutive clinical Aeromonas isolates in southern Taiwan. J Infect 54:151–158

    Article  PubMed  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto S, Kasai H, Arnold DL, Jackson RW, Vivian A, Harayama S (2000) Phylogeny of the genus Pseudomonas: intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiology 146:2385–2394

    PubMed  CAS  Google Scholar 

  • Yanez MA, Catalan V, Apraiz D, Figueras MJ, Martınez-Murcia AJ (2003) Phylogenetic analysis of members of the genus Aeromonas based on gyrB gene sequences. Int J Syst Evol Microbiol 53:875–883

    Article  PubMed  CAS  Google Scholar 

  • Yesmin S, Rahman MH, Hussain AM, Khan AR, Pervin F, Hossain MA (2004) Aeromonas hydrophila infection in fish of swamps in Bangladesh. Pak J Biol Sci 7(3):409–411

    Article  Google Scholar 

  • Yucel N, Erdem B, Kaya D (2005) Some virulence properties and characterization of motile Aeromonas species from milk and white cheese. Int J Dairy Technol 58(2):106–110

    Article  Google Scholar 

  • Zmantar T, Kouidhi B, Miladi H, Mahdouani K, Bakhrouf A (2010) A Microtiter plate assay for Staphylococcus aureus biofilm quantification at various pH levels and hydrogen peroxide supplementation. New Microbiol 33:137–145

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge The Marine Products Export Development Authority (MPEDA), Ministry of Commerce & Industry, Govt. of India (Project code: 3/3/OFD/HO/2003 dated 25-02-2004), and Department of Biotechnology (DBT), Govt. of India (Project Code: BT/PR4012/AAQ/03/204/2003), for financial support. The first author thanks MPEDA for Fellowship.

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  1. National Centre for Aquatic Animal Health, Cochin University of Science and Technology, Fine Arts Avenue, Cochin, 682 016, Kerala, India

    Krishnan Sreedharan & Isaac Sarojani Bright Singh

  2. Department of Marine Biology, Microbiology and Biochemistry, School of Marine Sciences, Cochin University of Science and Technology, Fine Arts Avenue, Cochin, 682 016, Kerala, India

    Rosamma Philip

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Sreedharan, K., Philip, R. & Singh, I.S.B. Characterization and virulence potential of phenotypically diverse Aeromonas veronii isolates recovered from moribund freshwater ornamental fishes of Kerala, India. Antonie van Leeuwenhoek 103, 53–67 (2013). https://doi.org/10.1007/s10482-012-9786-z

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