Skip to main content
SpringerLink
Log in

Phenotypic variation and morphological changes in starved denitrifying Aeromonas hydrophila

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

In this study, an Aeromonas hydrophila identified as a denitrifying bacterium by PCR detection of nitrate reductase (narG) and nitrite reductase (nirK) genes was incubated in seawater microcosms for 8 months at room temperature and at 4 °C. A study of the phenotypic variation demonstrated that A. hydrophila becomes gelatinase-positive after the incubation in sea water. We noted that starved A. hydrophila becomes unable to produce leucine arylamidase, and that the starved strain appears to grow more slowly. Indeed, we also observed a severe decrease in cellular aggregation of Aeromonas after incubation. In addition, atomic force micrographs revealed a reduction in cell size.

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

Access this article

Log in via an institution

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. 4a,b

Similar content being viewed by others

References

  • Alonso JL, Mascellaro S, Moreno Y, Ferrus MA, Hernandez J (2002) Doublestaining method for differentiation of morphological changes and membrane integrity of Campylobacter coli cells. Appl Environ Microbiol 68:5151–5154

    Article  PubMed  CAS  Google Scholar 

  • Alterman E, Buck BL, Cano R, Klaenhammer TR (2004) Identification and phenotypic characterization of the cell-division protein CdpA. Gene 342:189–197

    Article  Google Scholar 

  • Angka SL, Lam TJ, Sin YM (1995) Some virulence characteristics of Aeromonas hydrophila in walking catfish (Clarias gariepinus). Aquaculture 130:103–111

    Article  Google Scholar 

  • Austin B, Adams C (1996) Fish pathogens. In: Austin B, Altwegg M, Gosling PJ, Joseph SW (eds) The genus Aeromonas. Wiley, Chichester, 197–243

    Google Scholar 

  • Austin B, Austin DA (1999) Bacterial fish pathogens. Diseases of farmed and wild fish, 3rd edn. Springer Praxis, Chichester

    Google Scholar 

  • Ben Abdallah F, Chaieb K, Snoussi M et al (2007) Phenotypic variations and molecular identification of Salmonella enteric Serovar Typhimurium cells under starvation in seawater. Curr Microbiol 55:485–491

    Article  PubMed  CAS  Google Scholar 

  • Ben Kahla-Nakbi A, Besbes A, Chaieb K et al (2007) Survival of Vibrio alginolyticus in seawater and retention of virulence of its starved cells. Mar Environ Res 64:469–478

    Article  PubMed  CAS  Google Scholar 

  • Braga PC, Ricci D (1998) Atomic force microscopy: application to investigation of Escherichia coli morphology before and after exposure to cefodizime. Antimicrob Agents Chemother 42:18–22

    PubMed  CAS  Google Scholar 

  • Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775

    PubMed  CAS  Google Scholar 

  • Briandet R, Meylheuc T, Maher C, Bellon-Fontaine MN (1999) Listeria monocytogenes Scott A: cell surface charge, hydrophobicity, and electron donor and acceptor characteristics under different environmental growth conditions. Appl Environ Microbiol 65:5328–5333

    PubMed  CAS  Google Scholar 

  • Chaieb K, Chehab O, Zmantar T et al (2007) In vitro effect of pH and ethanol on biofilm formation by clinical ica positive Staphylococcus epidermidis strains. Ann Microbiol 57:431–437

    Article  CAS  Google Scholar 

  • Costerton JW, Cheng KJ (1975) The role of the bacterial cell envelope in antibiotic resistance. J Antimicrob Chemother 1:363–377

    Article  PubMed  CAS  Google Scholar 

  • Everis L, Betts G (2001) pH stress can cause cell elongation in Bacillus and Clostridium species: a research note. Food Control 12:53–56

    Article  Google Scholar 

  • Farmer JJ III, Arduino MJ, HickmanBrenner FW (1992) The genera Aeromonas and Plesiomonas In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The procaryotes, 2nd edn. Springer, New York, 3012–3028

    Google Scholar 

  • Gauthier MJ, Munro PM, Breittmayer VA (1988) Damage to surface colonisation factors of enters adhesive Escherichia coli during starvation in seawater. Microbiol Lett 38:37–45

    CAS  Google Scholar 

  • Givskov M, Eberl L, Moller S et al (1994) Responses to nutrient starvation in Pseudomonas putida KT2442: analysis of general cross-protection, cell shape, and macromolecular content. J Bacteriol 176:7–14

    PubMed  CAS  Google Scholar 

  • Hamadi F, Latrache H, Elghmari A, Mabrrouki M, Ellouali M, Kuider N (2004) Effect of pH and ionic strength on hydrophobicity and electron donor and acceptor characteristics of Escherichia coli and Staphylococcus aureus. Ann Microbiol 54:213–225

    CAS  Google Scholar 

  • Hazen TC, Fliermans CB, Hirsch RP, Esch GW (1978) Prevalence and distribution of Aeromonas hydrophila in the United States. Appl Environ Microbiol 36:731–738

    PubMed  CAS  Google Scholar 

  • Janda JM, Duffey PS (1988) Mesophilic Aeromonas in human disease: current taxonomy, laboratory identification, and infectious disease spectrum. Rev Infect Dis 10:980–997

    Article  PubMed  CAS  Google Scholar 

  • Jiang X, Chai TJ (1996) Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable nonculturable cells. Appl Environ Microbiol 62:1300–1305

    PubMed  CAS  Google Scholar 

  • Jydegaard-Axelsen AM, Aes-Jorgensen A, Koch AG, Jensen JS, Knochel S (2005) Changes in growth, rRNA content, and cell morphology of Listeria monocytogenes induced by CO2 up and downshift. Int J Food Microbiol 98:145–155

    Article  PubMed  CAS  Google Scholar 

  • Kjelleberg S, Flärdh K, Nyström T et al (1993) Growth limitation and starvation of bacteria In: Ford T (ed) Aquatic microbiology: an ecological approach. Blackwell, Oxford, 289–320

    Google Scholar 

  • Mahdhi A, Harbi B, Esteban MA, Chaieb K, Kamoun F, Bakhrouf A (2010) Using mixture design to construct consortia of potential probiotic Bacillus strains to protect gnotobiotic Artemia against pathogenic Vibrio. Biocontrol Sci Technol 20:983–996

    Article  Google Scholar 

  • Massa S, Altieri C, Angela AD (2001) The occurrence of Aeromonas spp. in natural mineral water and well water. Int J Food Microbiol 63:169–173

    Article  PubMed  CAS  Google Scholar 

  • Mattick KL, Phillips LE, Jorgensen F, Lappin-Scott HM, Humprey TJ (2003a) Filament formation by Salmonella spp. inoculated into liquid food matrices at refrigeration temperatures, and growth pattern when warmed. J Food Protect 66:215–219

    Google Scholar 

  • Mattick KL, Rowbury RJ, Humprey TJ (2003b) Morphological changes to Escherichia coli 0157:H7, commensal E. coli and Salmonella spp. in response to marginal growth conditions, with special reference do mildly stressing temperatures. Sci Prog 96:103–113

    Article  Google Scholar 

  • McMahon MAS, McDowell DA, Blair IS (2007) The pattern of pleomorphism in stressed Salmonella Virchow populations in nutrient and growth phase dependent. Lett Appl Microbiol 0266–8254:1–6

    Google Scholar 

  • Morita RY (1993) Bioavailability of energy and the starvation state In: Kjelleberg S (ed) Starvation in bacteria. Plenum, New York, 1–23

    Chapter  Google Scholar 

  • Nogales B, Timmis KN, Nedwell DB, Osborn AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl Environ Microbiol 68:5017–5025

    Article  PubMed  CAS  Google Scholar 

  • Pathiratne A, Jayasinghe RPPK (2001) Environmental influence on the occurrence of epizootic ulcerative syndrome (EUS) in freshwater fish in Bellanwila-Attidia wetlands Sri Lanka. J Appl Ichthyol 17:30–34

    Article  Google Scholar 

  • Pearson MD, Hirono I, Aoki T, Miranda R, Inglis V (2000) Virulence properties of motile aeromonads isolated from farmed frogs Rana tigerina and R. rugulosa. Dis Aquat Org 40:185–193

    Article  PubMed  CAS  Google Scholar 

  • Piuri M, Sanchez-Rivas C, Ruzal SM (2005) Cell wall modifications during osmotic stress in Lacobacillus casei. J Appl Microbiol 98:84–95

    Article  PubMed  CAS  Google Scholar 

  • Rippey SR, Cabelli VJ (1989) Use of the thermotolerent Aeromonas group for the trophic state classification of freshwaters. Water Res 23:1107–1114

    Article  CAS  Google Scholar 

  • Rosen R, Buttner K, Schmid R, Hecker M, Ron EZ (2001) Stressinduced proteins of Agrobacterium tumefaciens. FEMS Microbiol Ecol 35:277–285

    Article  PubMed  CAS  Google Scholar 

  • Russell NJ, Fukanaga N (1990) A comparison of thermal adaptation of membrane lipids in psychrophilic and thermophilic bacteria. FEMS Microbiol Rev 75:171–182

    Article  CAS  Google Scholar 

  • Russell NJ, Evans RI, ter Steg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28:255–261

    Article  PubMed  CAS  Google Scholar 

  • Shi B, Xia X (2003) Morphological changes of Pesudomonas pseudoalcaligenes in response to temperature selection. Curr Microbiol 46:120–123

    Article  PubMed  CAS  Google Scholar 

  • Shotts EB, Gaines JL, Martin L, Prestwood AK (1972) Aeromonas- induced deaths among fish and reptiles in an eutrophic inland lake. J Am Vet Med Assoc 161:603–607

    PubMed  Google Scholar 

  • Thornley JP, Shaw IE, Gryllos IA, Eley A (1997) Virulence properties of clinically significant Aeromonas species: evidence for pathogenicity. Rev Med Microbiol 8:61–72

    Article  Google Scholar 

  • Torella F, Morita RY (1981) Microcultural study of bacterial size change and microcolony and ultramicroclony formation by hetrotrophic bacteria in sea water. Appl Environ Microbiol 41:518–527

    Google Scholar 

  • Wang Y, Corrieu G, Beal C (2005) Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. J Dairy Sci 88:21–29

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Analysis, Treatment and Valorization of Environment Polluants and Product, Faculty of Pharmacy, Monastir, Tunisia

    Besma Harbi, Chédia Jabeur, Ali Ellafi & Amina Bakhrouf

Authors
  1. Besma Harbi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chédia Jabeur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ali Ellafi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amina Bakhrouf
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Besma Harbi.

Additional information

Besma Harbi and Chédia Jabeur contributed equally to this manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harbi, B., Jabeur, C., Ellafi, A. et al. Phenotypic variation and morphological changes in starved denitrifying Aeromonas hydrophila . Ann Microbiol 63, 1039–1045 (2013). https://doi.org/10.1007/s13213-012-0560-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-012-0560-2

Keywords

Search

Navigation