Abstract
The marine bacteria Vibrio parahaemolyticus and V. alginolyticus were incubated in seawater for 8 months to evaluate their adaptative responses to starvation. The starved cells showed an altered biochemical and enzymatic profiles, respectively, on Api 20E and Api ZYM systems and an evolution to the filterable minicells state capable to pass membrane pore size 0.45 μm. Outer membrane proteins patterns of stressed bacteria were also altered. Indeed, these modifications were manifested by the appearance and/or disappearance of bands as well as in the level of expression of certain proteins. Plasmids profiles analysis showed that V. alginolyticus ATCC 33787 lost three plasmids, whereas other tested strains conserved their initial profiles.
Similar content being viewed by others
References
Bakhrouf A, Jeddi M, Bouddabous A, Gauthier MJ (1989) Evolution of Pseudomonas aeruginosa cells towards a filterable stage in seawater. FEMS Microbiol Lett 50:187–190
Bakhrouf A, Jeddi M, Gauthier MJ (1992) Modifications des caractères culturaux et biochimiques du Salmonella paratyphi B après incubation dans l’eau de mer. Can J Microbiol 55:871–874
Bakhrouf-Ben Fedhila A, Jeddi M, Bouddabous A, Gauthier MJ (1990) Production of filterable minicells by Salmonella paratyphi B in seawater. Microbiol Lett 43:123–129
Ben Abdallah F, Chaieb K, Snoussi M, Bakhrouf A, Gaddour K (2007) Phenotypic variations and molecular identification of Salmonella enterica serovar Typhimurium cells under starvation in seawater. Curr Microbiol 55:485–491
Ben Abdallah F, Chaieb K, Kallel H, Bakhrouf A (2009) RT-PCR assays for in vivo expression of Vibrio alginolyticus virulence genes in cultured gilthead Dicentrarchus labrax and Sparus aurata. Ann Microbiol 59:1–5
Ben Kahla NA, Besbes A, Chaieb K, Rouabhia M, Bakhrouf A (2007) Survival of Vibrio alginolyticus in seawater and retention of virulence of its starved cells. Mar Environ Res 64:469–478
Ben Kahla NA, Besbes A, Bakhrouf A (2008) Survival of Vibrio fluvialis in seawater under starvation conditions. Microbiol Res 163:323–328
Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523
Cai SJ, Inouye M (2002) EnvZ–OmpR interaction and osmoregulation in Escherichia coli. J Biol Chem 277:24155–24161
Carroll JA, Garon CF, Schwan TG (1999) Effects of environmental pH on membrane proteins in Borrelia burgdorferi. Infect Immun 67:3181–3187
Chen HY, Livermore DM (1993) Activity of cefepime and other beta-lactam antibiotics against permeability mutants of Escherichia coli and Klebsiella pneumoniae. J Antimicrob Chemother 32(Suppl B):63–74
Contreras I, Muñoz L, Toro CS, Mora GC (1995) Heterologous expression of Escherichia coli porin genes in Salmonella typhi Ty2: regulation by medium osmolarity, temperature and oxygen availability. FEMS Microbiol Lett 133:105–111
Costerton JW, Cheng K (1975) The role of the bacterial cell envelope in antibiotic resistance. J Antimicrob Chemother 1:363–377
Cullen PA, Cordwell SJ, Bulach DM, Haake DA, Adler B (2002) Global analysis of outer membrane proteins from Leptospira interrogans serovar Lai. Infect Immun 70:2311–2318
Dedieu L, Pages JM, Bolla JM (2002) Environmental regulation of Campylobacter jejuni major outer membrane protein porin expression in Escherichia coli monitored by using green fluorescent protein. Appl Environ Microbiol 68:4209–4215
Denner EBM, Vybiral D, Fischer UR, Velimirov B, Busse HJ (2002) Vibrio calviensis sp. nov., a halophilic, facultatively oligotrophic 0.2 μm-filterable marine bacterium. Int J Syst Bacteriol 52:549–553
Feodorova VA, Devdariani ZL (2001) Expression of acid-stable proteins and modified lipopolysaccharide of Yersinia pestis in acidic growth medium. J Med Microbiol 50:979–985
Gauthier MJ, Munro PM, Breittmayer VA (1988) Damage to surface colonisation factors of enters adhesive Escherichia coli for starvation in seawater. Microbios Lett 38:37–45
Hernandez-Alles S, Albert S, Alvarez D, Domenech-Sanchez A, Martinez-Martinez L, Gil J, Tomas JM, Bendi VJ (1999) Porin expression in clinical isolates of Klebsiella pneumoniae. Microbiology 145:673–679
Hwang PM, Choy WY, Lo EI, Chen L, Forman-Kay JD, Raetz CR, Privé GG, Bishop RE, Kay LE (2002) Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc Natl Acad Sci USA 99:13560–13565
Jiang X, Chai T (1996) Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl Environ Microb 62:1300–1305
Kjelleberg S (1993) Starvation in bacteria. Plenum, New York
Kjelleberg S, Hermannson M, Marden P, Jones GW (1987) The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment. Annu Rev Microbiol 41:25–49
Kustos I, Kocsis B, Kilár F (2007) Bacterial outer membrane protein analysis by electrophoresis and microchip technology. Expert Rev Proteomics 4:91–106
Laemmli UK (1970) Cleavage of structural proteins for the assembly of the head of bacteriophage T4. Nature 227:680–685
Leal-Balbino TC, Leal NC, Lopes CV, de Almeida AMP (2004) Differences in the stability of the plasmids of Yersinia pestis cultures in vitro: Impact on virulence. Mem Inst Oswaldo Cruz 99:727–732
Liu PV (1957) Survey of hemolysin production among species of Pseudomonas. J Bacteriol 74:718–727
Martinez MB, Flickinger M, Higgins L, Krick T, Nelsestuen GL (2001) Reduced outer membrane permeability of Escherichia coli O157:H7: suggested role of modified outer membrane porins and theoretical function in resistance to antimicrobial agents. Biochemistry 40:11965–11974
Molloy MP, Herbert BR, Slade MB, Rabilloud T, Nouwens AS, Williams KL, Gooley AA (2000) Proteomic analysis of the Escherichia coli outer membrane. Eur J Biochem 267:2871–2881
Morita RY (1997) Bacteria in oligotrophic environments: starvation-survival lifestyle. Chapman & Hall, New York
Mushtaq S, Ge Y, Livermore DM (2004) Doripenem versus Pseudomonas aeruginosa in vitro: activity against characterized isolates, mutants, and transconjugants and resistance selection potential. Antimicrob Agents Chemother 8:3086–3092
Obonyo M, Munderloh UG, Sam TN, Kurtti TJ (2002) Cultivation at 37 degrees C enhances Borrelia burgdorferi sensu stricto infectivity for hamsters. Med Microbiol Immunol 191:33–39
Provenzano D, Lauriano CM, Klose KE (2001) Characterization of the role of the ToxR-modulated outer membrane porins OmpU and OmpT in Vibrio cholerae virulence. J Bacteriol 183:3652–3662
Puig M, Fusté C, Viñas M (1993) Outer membrane proteins from Serratia marcescens. Can J Microbiol 39:108–111
Rahmati-Bahram A, Magee JT, Jackson SK (1996) Temperature-dependent aminoglycoside resistance in Stenotrophomonas (Xanthomonas) maltophilia; alterations in protein and lipopolysaccharide with growth temperature. J Antimicrob Chemother 37:665–676
Rosen R, Buttner K, Schmid R, Hecker M, Ron EZ (2001) Stress-induced proteins of Agrobacterium tumefaciens. FEMS Microbiol Ecol 35:277–285
Sabri MY, Zamri-Saad M, Mutalib AR, Israf DA, Muniandy N (2000) Efficacy of an outer membrane protein of Pasteurella haemolytica A2, A7 or A9-enriched vaccine against intratracheal challenge exposure in sheep. Vet Microbiol 73:13–23
Sambrook PL, Peterson BC, Gerding DN, Cleary PP (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor
Shand GH, Anwar H, Brown MR (1988) Outer membrane proteins of polymyxin resistant Pseudomonas aeruginosa: effect of magnesium depletion. J Antimicrob Chemother 22:811–821
Siegele DA, Kolter R (1992) Life after log. J Bacteriol 174:345–348
Srinivasan S, Kjellberg S (1998) Cycles of famine and feast: the starvation and outgrowth strategies of a marine Vibrio. J Biosci 23:501–511
Sunde M, Sorum H (2001) Self-transmissible multidrug resistance plasmids in Escherichia coli of the normal intestinal flora of healthy swine. Microbial Drug Resistance 7:191–196
Tabor PS, Ohwada K, Colwell RR (1981) Filterable marine bacteria found in the deep sea distribution, taxonomy, and response to starvation. Microb Ecol 7:67–83
Van Gemerden H, Kuen JG (1984) Strategies for growth and evolution of microorganisms in oligotrophic habitats. In: Hobbie JE, Williams PJB (eds) Heterotrophic activity in the sea. Nato Conference series IV. Plenum Press, New York, pp 25–54
Vybiral D, Denner EBM, Haller CM, Busse HJ, Witte A, Hofle MG, Velimirov B (1999) Polyphasic classification of 0.2 μm filterable bacteria from the Western Mediterranean Sea. Syst Appl Microbiol 22:635–646
Wibbenmeyer JA, Provenzano D, Landry CF, Klose KE, Delcour AH (2002) Vibrio cholerae OmpU and OmpT Porins are differentially affected by bile. Infect Immun 70:121–126
Wu L, Lin X, Wang F, Ye D, Xiao X, Wang S, Peng X (2006) OmpW and OmpV are required for NaCl regulation in Photobacterium damsela. J Proteome Res 5:2250–2257
Xu C, Ren H, Wang S, Peng X (2004) Proteomic analysis of salt-sensitive outer membrane proteins of Vibrio parahaemolyticus. Res Microbiol 155:835–842
Xu C, Wang S, Ren H, Lin X, Wu L, Peng X (2005) Proteomic analysis on the expression of outer membrane proteins of Vibrio alginolyticus at different sodium concentrations. Proteomics 5:3142–3152
Yoshida T, Qin L, Inouye M (2002) Formation of the stoichiometric complex of EnvZ, a histidine kinase, with its response regulator, OmpR. Mol Microbiol 46:1273–1282
Acknowledgments
We are grateful to M’SELMI Abdelhamid principal technical; USCR: Unité des Services Communs de Recherche, Faculté des Sciences de Tunis. Campus Universitaire. Tunisia.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jorge Membrillo-Hernández.
Rights and permissions
About this article
Cite this article
Abdallah, F.B., Kallel, H. & Bakhrouf, A. Enzymatic, outer membrane proteins and plasmid alterations of starved Vibrio parahaemolyticus and Vibrio alginolyticus cells in seawater. Arch Microbiol 191, 493–500 (2009). https://doi.org/10.1007/s00203-009-0477-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-009-0477-8