Skip to main content
Log in

Effect of starvation on survival and virulence expression of Aeromonas hydrophila from different sources

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Aeromonas hydrophila is an aquatic bacterium responsible for several human illnesses. The aim of this work was to investigate the survival ability and virulence expression of two strains from different sources (fish, strain 87 and surface water, strain LS) maintained in a seawater microcosm. The strains were analyzed for the total and viable bacterial counts, adhesion ability to Hep-2 cells and aerA gene expression by qPCR throughout the experiment (35 days). Both strains reached a putative VBNC state and lost adhesive properties but exhibited a different behavior in the expression of aerA. This could be due to the different origin of the two strains; the former adapted to a habitat rich of nutrient and the latter already used to survive in a more hostile environment. Moreover, our results indicate that the quantitative determination of aerA mRNA can be a useful indicator of virulence expression under stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abrami L, Fivaz M, van der Goot FG (2000) Adventures of a pore-forming toxin at the target cell surface. Trends Microbiol 8:168–172

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Aldape K, Ginzinger DG, Godfrey TE (2002) Real-time quantitative polymerase chain reaction: a potential tool for genetic analysis in neuropathology. Brain Pathol 12:54–66

    Article  CAS  PubMed  Google Scholar 

  • Avolio M, La Spisa C, Moscariello F, De Rosa R, Camporese A (2009) Aeromonas hydrophila ecthyma gangrenosum without bacteraemia in a diabetic man: the first case report in Italy. Infez Med 17:184–187

    PubMed  Google Scholar 

  • Braun V, Focareta T (1991) Pore-forming bacterial protein hemolysins (cytolysins). Crit Rev Microbiol 18:115–158

    Article  CAS  PubMed  Google Scholar 

  • Carvalho-Castro GA, Lopes CO, Leal CA, Cardoso PG, Leite RC, Figueiredo HC (2010) Detection of type III secretion system genes in Aeromonas hydrophila and their relationship with virulence in Nile tilapia. Vet Microbiol 26:371–376

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Delamare APL, Costa SOP, Da Silveira MM, Echeverriagary S (2000) Growth of Aeromonas species on increasing concentrations of sodium chloride. Lett Appl Microbiol 30:57–60

    Article  CAS  PubMed  Google Scholar 

  • Dooley JS, Trust TJ (1988) S-layer of high-virulence Aeromonas hydrophila. J Diarrhoeal Dis Res 6:120–123

    CAS  PubMed  Google Scholar 

  • Grim CJ, Kozlova EV, Sha J, Fitts EC, van Lier CJ, Kirtley ML, Joseph SJ, Read TD et al (2013) Characterization of Aeromonas hydrophila wound pathotypes by comparative genomic and functional analyses of virulence genes. MBio 4:e00064-13

    Article  PubMed Central  PubMed  Google Scholar 

  • Heim S, Lleo MDL, Bonato B, Guzman CA, Canepari P (2002) The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J Bacteriol 184:6739–6745

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hudson JA, Mott SJ, Penney N (1994) Growth of Listeria monocytogenes and Aeromonas hydrophila and Yersinia enterocolitica on vacuum and saturated carbon dioxide controlled atmosphere-packaged sliced roast beef. J Food Prot 57:204–208

    Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janda JM, Kokka RP, Guthertz LS (1994) The susceptibility of S-layer-positive and S-layer-negative Aeromonas strains to complement-mediated lysis. Microbiology 140:2899–2905

    Article  CAS  PubMed  Google Scholar 

  • Khaianchi BK, Fad AA, Bochardt MA, Berg RL, Horneman AJ, Stemper ME, Joseph SW, Moyer NP et al (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

    Article  Google Scholar 

  • Kirow SM (1997) Aeromonas and Plesiomonas species. In: Doyle MP, Beauchat LR, Montville TJ (eds) Food microbiology: fundamentals and frontiers. AMS Press, Washington DC, pp 265–267

    Google Scholar 

  • Li J, Ni XD, Liu YJ, Lu CP (2011) Detection of three virulence genes alt, ahp and aerA in Aeromonas hydrophila and their relationship with actual virulence to zebrafish. J Appl Microbiol 110:823–830

    Article  CAS  PubMed  Google Scholar 

  • Maalej S, Gdoura R, Dukan S, Hammami A, Bouain A (2004) Maintenance of pathogenicity during entry into and resuscitation from viable but nonculturable state in Aeromonas hydrophila exposed to natural seawater at low temperature. J Appl Microbiol 97:557–565

    Article  CAS  PubMed  Google Scholar 

  • Mary P, Sautour M, Chihib NE, Tierny Y (2003) Tolerance and starvation induced cross-protection against different stresses in Aeromonas hydrophila. Int J Food Microbiol 87:121–130

    Article  PubMed  Google Scholar 

  • McMahon MAS, Blair IS, McDowell DA (1998) Filamentation in Aeromonas hydrophila. Food Microbiol 15:441–448

    Article  Google Scholar 

  • Messi P, Guerrieri E, Bondi M (2002) Survival of an Aeromonas hydrophila in an artificial mineral water microcosm. Water Res 36:3410–3415

    Article  CAS  PubMed  Google Scholar 

  • Montecucco C, Papini E, Schiavo G (1994) Bacterial protein toxins penetrate cells via a four-step mechanism. FEBS Lett 346:92–98

    Article  CAS  PubMed  Google Scholar 

  • Oliver JD (2009) Recent findings on the viable but non-culturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415–425

    PubMed  Google Scholar 

  • Ottaviani D, Parlani C, Citterio B, Masini L, Leoni F, Canonico C, Sabatini L, Bruscolini F et al (2011) Putative virulence properties of Aeromonas strains isolated from food, environmental and clinical sources in Italy: a comparative study. Int J Food Microbiol 144:538–545

    Article  PubMed  Google Scholar 

  • Palu 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Parker MW, van der Goot FG, Buckley T (1996) Aerolysin—the ins and outs of a model channel-forming toxin. Mol Microbiol 19:205–212

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pianetti A, Manti A, Boi P, Citterio B, Sabatini L, Papa S, Rocchi MB, Bruscolini F (2008) Determination of viability of Aeromonas hydrophila in increasing concentrations of sodium chloride at different temperatures by flow cytometry and plate count technique. Int J Food Microbiol 127:252–560

    Article  CAS  PubMed  Google Scholar 

  • Pianetti A, Battistelli M, Barbieri F, Bruscolini F, Falcieri E, Manti A, Sabatini L, Citterio B (2012) Changes in adhesion ability of Aeromonas hydrophila during long exposure to salt stress conditions. J Appl Microbiol 113:974–982

    Article  CAS  PubMed  Google Scholar 

  • Rahman MH, Suzuki S, Kawai K (2001) Formation of viable but non-culturable state (VBNC) of Aeromonas hydrophila and its virulence in goldfish, Carassius auratus. Microbiol Res 156:103–106

    Article  CAS  PubMed  Google Scholar 

  • Singh V, Somvanshi P, Rathore G, Kapoor D, Mishra BN (2009) Gene cloning, expression and homology modelling of hemolysin gene from Aeromonas hydrophila. Protein Express Purif 65:1–7

    Article  CAS  Google Scholar 

  • Singh V, Chaudhary DK, Mani I, Jain R, Mishra BN (2013) Development of diagnostic and vaccine markers through cloning, expression, and regulation of putative virulence-protein-encoding genes of Aeromonas hydrophila. J Microbiol 51:275–282

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Wai SN, Mizunoe Y, Takade A, Yoshida S (2000) A comparison of solid and liquid media for resuscitation of starvation- and low-temperature-induced nonculturable cells of Aeromonas hydrophila. Arch Microbiol 173:307–310

    Article  CAS  PubMed  Google Scholar 

  • Yu HB, Zhang YL, Lau YL, Yao F, Vilches S, Merino S, Tomas JM, Howard SP et al (2005) Identification and characterization of putative virulence genes and gene clusters in Aeromonas hydrophila PPD134/91. Appl Environ Microbiol 71:4469–4477

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Barbara Citterio.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Casabianca, A., Orlandi, C., Barbieri, F. et al. Effect of starvation on survival and virulence expression of Aeromonas hydrophila from different sources. Arch Microbiol 197, 431–438 (2015). https://doi.org/10.1007/s00203-014-1074-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-014-1074-z

Keywords

Navigation