Virulence characteristics and antimicrobial resistance of Aeromonas veronii biovar sobria 312M, a clinical isolate

  • Karoline de C. Prediger
  • Cibelle B. Dallagassa
  • Bárbara Moriel
  • Bruno Stefanello Vizzotto
  • Waldemar Volanski
  • Emanuel M. Souza
  • Fábio O. Pedrosa
  • Vinícius Weiss
  • Dayane Alberton
  • Dieval Guizelini
  • Cyntia M. T. Fadel-PichethEmail author
Bacterial Fungal and Virus Molecular Biology - Research Paper


Aeromonas are bacteria widely distributed in the environment, and some species are able to cause infections in humans, of which diarrhea is the most common. The objective of this study was to evaluate the presence of virulence and antimicrobial resistance associated characteristics in A. veronii biovar sobria strain 312M isolated from diarrheal stools. For this, the genome sequencing and phenotypical tests were performed. The draft genome annotation revealed several complete pathways associated with carbon metabolism and a mucin-desulfating sulfatase which may contribute to intestine colonization, and a large number of virulence-associated genes encoding structures associated with adhesion, toxins, and secretion systems. The strain exhibited swimming and swarming motility, biofilm formation, and hemolytic activity. It was resistant to ampicillin, ampicillin/sulbactam, and amoxicillin-clavulanic acid. Although a cphA gene encoding a narrow-spectrum carbapenase was identified in the strain genome, no carbapenemase activity was detected in the antimicrobial susceptibility test. When compared with other A. veronii with complete genomes, the main differences in virulence characteristics are related to lateral flagella and type III and VI secretion systems; the antimicrobial resistance spectrum also varied among strains. The results indicated that A. veronii biovar sobria 312M presents high virulence potential and resistance to limited classes of antimicrobials.


A. veronii biovar sobria Genome Virulence Resistance 



This work was supported by the Brazilian Program of National Institutes of Science and Technology - INCT/Brazilian Research Council - CNPq/MCT and Fundação Araucária. We thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for scholarships.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Janda JM, Abbott SL (2010) The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23:35–73. CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Grim CJ, Kozlova EV, Ponnusamy D, Fitts EC, Sha J, Kirtley ML, van Lier CJ, Tiner BL, Erova TE, Joseph SJ, Read TD, Shak JR, Joseph SW, Singletary E, Felland T, Baze WB, Horneman AJ, Chopra AK (2014) Functional genomic characterization of virulence factors from necrotizing fasciitis-causing strains of Aeromonas hydrophila. Appl Environ Microbiol 80:4162–4183. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Rasmussen-Ivey CR, Figueras MJ, McGarey D, Liles MR (2016) Virulence factors of Aeromonas hydrophila: in the wake of reclassification. Front Microbiol 7:1337. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Seshadri R, Joseph SW, Chopra AK, Sha J, Shaw J, Graf J, Haft D, Wu M, Ren Q, Rosovitz MJ, Madapu 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. CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Reith ME, Singh RK, Curtis B, Boyd JM, Bouevitch A, Kimball J, Munholland J, Murphy C, Sarty D, Williams J, Nash JHE, 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. CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    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. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Hadi N, Yang Q, Barnett TC, Tabei SMB, Kirov SM, Shaw JG (2012) Bundle-forming pilus locus of Aeromonas veronii bv. sobria. Infect Immun 80:1351–1360. CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Surek M, Vizzotto BS, Souza EM, Pedrosa FO, Dallagassa CB, Farah SMSS, Fadel-Picheth CMT (2010) Identification and antimicrobial susceptibility of Aeromonas spp. isolated from stool samples of Brazilian subjects with diarrhoea and healthy controls. J Med Microbiol 59:373–374. CrossRefPubMedGoogle Scholar
  9. 9.
    Abbott SL, Cheung WKW, Janda JM (2003) The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J Clin Microbiol 41:2348–2357.–2357.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Borrell N, Acinas SG, Figueras MJ, Martínez-Murcia AJ (1997) Identification of Aeromonas clinical isolates by restriction fragment length polymorphism of PCR-amplified 16S rRNA genes. J Clin Microbiol 35:1671–1674PubMedPubMedCentralGoogle Scholar
  11. 11.
    Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Guizelini D, Raittz RT, Cruz LM, Souza EM, Steffens MBR, Pedrosa FO (2016) GFinisher: a new strategy to refine and finish bacterial genome assemblies. Sci Rep 6:34963. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. CrossRefPubMedGoogle Scholar
  15. 15.
    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. CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16. CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    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. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Chopra AK, Peterson JW, Xu XJ, Coppenhaver DH, Houston CW (1996) Molecular and biochemical characterization of a heat-labile cytotonic enterotoxin from Aeromonas hydrophila. Microb Pathog 21:357–377. CrossRefPubMedGoogle Scholar
  21. 21.
    Bomar L, Stephens WZ, Nelson MC, Velle K, Guillemin K, Graf J (2013) Draft genome sequence of Aeromonas veronii Hm21, a symbiotic isolate from the medicinal leech digestive tract. Genome Announc 1:e00800–e00813. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    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. CrossRefPubMedGoogle Scholar
  23. 23.
    Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Clinical and laboratory standards institute (CLSI) (2008) Performance standards for antimicrobial susceptibility testing: eighteenth informational supplement M100-S18, vol 28. CLSI, WayneGoogle Scholar
  25. 25.
    Clinical and laboratory standards institute (CLSI) (2011) Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria: approved guideline 2nd edn, M45–A2, vol 30, n 19. CLSI, WayneGoogle Scholar
  26. 26.
    Carter MQ, Louie JW, Feng D, Zhong W, Brandl MT (2016) Curli fimbriae are conditionally required in Escherichia coli O157:H7 for initial attachment and biofilm formation. Food Microbiol 57:81–89. CrossRefPubMedGoogle Scholar
  27. 27.
    Jagoda SSSDS, Honein K, Arulkanthan A, Ushio H, Asakawa S (2017) Genome sequencing and annotation of Aeromonas veronii strain Ae52, a multidrug-resistant isolate from septicaemic gold fish (Carassius auratus) in Sri Lanka. Genomics Data 11:46–48. CrossRefGoogle Scholar
  28. 28.
    Abdelhamed H, Lawrence ML, Waldbieser G (2019) Complete genome sequence data of multidrug-resistant Aeromonas veronii strain MS-18-37. Data in Brief 23:103689. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Kang Y, Pan X, Xu Y, Siddiqui SA, Wang C, Shan X, Qian A (2016) Complete genome sequence of the fish pathogen Aeromonas veronii TH0426 with potential application in biosynthesis of pullulanase and chitinase. J Biotechnol 227:81–82. CrossRefPubMedGoogle Scholar
  30. 30.
    Fuchs TM, Eisenreich W, Heesemann J, Goebel W (2012) Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats. FEMS Microbiol Rev 36:435–462. CrossRefPubMedGoogle Scholar
  31. 31.
    Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, Smalley D, McHargue JW, Hightower GA, Smith JT, Autieri SM, Leatham MP, Lins JJ, Allen RL, Laux DC, Cohen PS, Conway T (2008) Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 76:1143–1152. CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Prediger KC, Surek M, Dallagassa CB, Assis FEA, Piantavini MS, Souza EM, Pedrosa FO, Farah SMSS, Alberton D, Fadel-Picheth CMT (2017) Utilization of carbon sources by clinical isolates of Aeromonas. Can J Microbiol 63:359–364. CrossRefPubMedGoogle Scholar
  33. 33.
    Dacanay A, Boyd JM, Fast MD, Knickle LC, Reith ME (2010) Aeromonas salmonicida type I pilus system contributes to host colonization but not invasion. Dis Aquat Org 88:199–206. CrossRefPubMedGoogle Scholar
  34. 34.
    Kirov SM, Barnett TC, Pepe CM, Strom MS, Albert MJ (2000) Investigation of the role of type IV Aeromonas pilus (Tap) in the pathogenesis of Aeromonas gastrointestinal infection. Infect Immun 68:4040–4048. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    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. CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Fosse T (2010) Aeromonas, Vibrio and Plesiomonas. In: Courvalin P, Leclercq R, Rice LB (eds) Antibiogram. ESKA Publishing, ASM Press, Portland, pp 509–518Google Scholar
  37. 37.
    Wu CJ, Chen PL, Wu JJ, Yan JJ, Lee CC, Lee HC, Lee NY, Chang CM, Lin YT, Chiu YC, Ko WC (2012) Distribution and phenotypic and genotypic detection of a metallo-b-lactamase, CphA, among bacteraemic Aeromonas isolates. J Med Microbiol 61:712–719. CrossRefPubMedGoogle Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Karoline de C. Prediger
    • 1
  • Cibelle B. Dallagassa
    • 1
  • Bárbara Moriel
    • 1
  • Bruno Stefanello Vizzotto
    • 1
    • 2
  • Waldemar Volanski
    • 1
  • Emanuel M. Souza
    • 3
  • Fábio O. Pedrosa
    • 3
  • Vinícius Weiss
    • 4
  • Dayane Alberton
    • 1
  • Dieval Guizelini
    • 4
  • Cyntia M. T. Fadel-Picheth
    • 1
    Email author
  1. 1.Departamento de Análises ClínicasUniversidade Federal do ParanáCuritibaBrazil
  2. 2.Universidade FranciscanaSanta MariaBrazil
  3. 3.Departamento de Bioquímica e Biologia MolecularUniversidade Federal do ParanáCuritibaBrazil
  4. 4.Programa de Pós-Graduação em BioinformáticaUniversidade Federal do ParanáCuritibaBrazil

Personalised recommendations