Skip to main content
Science Progress logoLink to Science Progress
. 2019 Feb 27;86(4):283–312. doi: 10.3184/003685003783238608

Bacterial Outer Membrane and Cell Wall Penetration and Cell Destruction by Polluting Chemical Agents and Physical Conditions

AD Russell 1
PMCID: PMC10367465  PMID: 15508894

Abstract

In the environment, bacteria and other microorganisms are subjected to a variety of constantly changing chemical and physical agencies. Chemical ones include antimicrobial compounds (both biocides and antibiotics), pollutants, drugs, cosmetic and pharmaceutical ingredients and pesticides. The physical agents include desiccation and drying, osmotic pressure, hydrostatic pressure, temperature and pH changes and radiations (ultraviolet, sunlight, ionizing). Bacteria must thus adapt to survive these inimicable conditions. Organisms such as bacterial spores usually survive, whereas other types of microorganisms may be much more susceptible.

Depending on the type of organism, the bacterial cell wall, outer membrane or the spore outer layers may act as permeability barriers to the intracellular uptake of antibiotics and biocides. Some antibacterial agents interact with, and damage or modify, the outer components. Physical agencies are known to damage the cytoplasmic membrane or to produce alterations in DNA or proteins or enzymes. Nevertheless, significant damage to the cell wall or outer membrane may also occur.

Four types of organisms are considered: cocci, mycobactria, Gram-negative bacteria and bacterial spores. The nature of the damage inflicted on, or in some cases prevented by, their outer cell layers is discussed for each type of organism.

Keywords: biocides, chemical pollutants, physical processes, outer cell damage

Full Text

The Full Text of this article is available as a PDF (221.3 KB).

References

  • 1.Russell A.D. (2004) Microbial susceptibility and resistance to chemical and physical agents. In: Topley & Wilson's Microbiology and Microbial Infections, 10th edn. Bacteriology Volume. Arnold Health Sciences, London: (in press). [Google Scholar]
  • 2.Russell A.D. (2003) Lethal effects of heat on bacterial physiology and structure. Sci. Progr., 86, 115–137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Russell A.D. (2003) Similarities and differences in the responses of micro-organisms to biocides. J. Antimicrob. Chemother., 52, 750–763. [DOI] [PubMed] [Google Scholar]
  • 4.Russell A.D. (2003) Biocide usage and antibiotic usage: the relevance of laboratory findings to clinical and environmental situations. Lancet Infectious Diseases, 3, 794–803. [DOI] [PubMed] [Google Scholar]
  • 5.Perry J.J., Staley J.T., and Lory S. (2002) Microbial Life. Sinauer Associates, Sunderland, Mass., USA. [Google Scholar]
  • 6.Wayne R.P. (2000) Chemistry of Atmospheres, 3rd edn. Oxford University Press, Oxford. [Google Scholar]
  • 7.Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., & Buxton H.T. (2002) Pharmaceuticals, hormones and other organic wastewater contaminants in U.S. streams, 1999–2000: a national recon-naissance. Environ. Sci. Technol., 36, 1202–1211. [DOI] [PubMed] [Google Scholar]
  • 8.Kummerer K., & Henninger A. (2003) Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin. Micribiol. Infect., 12, 1203–1211. [DOI] [PubMed] [Google Scholar]
  • 9.Daughton C.D., & Ternes T.A. (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ. Health Perspect., 107(Supplement 6), 907–938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Russell A.D. (2002) Biocides and pharmacologically active drugs as residues in the environment: is there a correlation with antibiotic resistance? Am. J. Infect. Control, 30, 495–498. [DOI] [PubMed] [Google Scholar]
  • 11.Bordas A.C., Brady M.S., Siewierski M., & Katz S.E. (1997) In vitro enhancement of antibiotic resistance development–interaction of residue levels of pesticides and antibiotics. J. Food Protect, 60, 531–536. [DOI] [PubMed] [Google Scholar]
  • 12.Falkingham J.O. III (2002) Nontuberculous mycobacteria in the environment. Clin. Chest Med., 23, 529–551. [DOI] [PubMed] [Google Scholar]
  • 13.Primm T.P., Lucero C.A., & Falkinham J.O. III (2004) Health impacts of environmental mycobacteria. Clin. Microbiol. Rev., 17, 98–106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Nicholson W.I. (2002) Roles of Bacillus endospores in the environment. Cell. Molecul. Life Sci., 59, 410–416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Atrib A., & Foster S.J. (2002) Bacterial endospores the ultimate survivors. Int. Dairy J., 12, 217–223. [Google Scholar]
  • 16.Scherrer R., & Gerhardt P. (1971) Molecular sirving by the Bacillus megateriunm cell wall and protoplast. J. Bacteriol., 107, 718–735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Koch A.L. (2000) The exoskeleton of bacterial cells (the sacculus): still a highly attractive target for antibacterial agents that will last for a long time. Crit. Rev. Microbiol., 26, 1–35. [DOI] [PubMed] [Google Scholar]
  • 18.Neuhaus F.C., & Baddiley J. (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria. Microbiol. Molec. Biol. Rev., 67, 686–723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.O'Riordan K., & Lee J.C. (2004) Staphylococcus aureus capsular polysaccharides. Clin. Microbiol. Rev., 17, 218–234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.McNeil M.R., & Brennan P.J. (1991) Structure, function and biogenesis of the cell envelope of mycobacteria in relation to bacterial physiology, pathogenesis and drug resistance: some thoughts and possibilities arising from recent structural information. Res. Microbiol., 142, 451–463. [DOI] [PubMed] [Google Scholar]
  • 21.Jarlier V., & Nikaido H. (1990) Permeability barrier to hydrophilic solutes in Mycobacterium chelonii. J. Bacteriol., 172, 1418–1423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Nikaido H., Kim S.-H., & Rosenberg E.Y. (1993) Physical organization of lipids in the cell wall of Mycobacterium chelonae. Molecul. Microbiol., 8, 1025–1030. [DOI] [PubMed] [Google Scholar]
  • 23.Besra G.S., Khoo W.K., McNeil M.R., Dell A., Morris H.R., & Brennan P.J. (1995) A new interpretation of the mycolyl-arabinogalactan complex of Mycobacterium tuberculosis as revealed through characterization of oligo-glycosylalditol fragnents by fast-atom bombardment mass spectrometry and 1H nuclear magnetic resonance spectroscopy. Biochemistry, 34 [???], 4257–4266. [DOI] [PubMed] [Google Scholar]
  • 24.Russell A.D. (1996) Activity of biocides against mycobacteria. J. Appl. Bacteriol., 81, 87S–101S. [PubMed] [Google Scholar]
  • 25.Hawkey P.M. (2004) Mycobactericidal agents. In: Fraise A.P., Lambert P.A., & Maillard J-Y. (eds.) Russell, Hugo & Ayliffe's Principles and Practice of Disinfection, Preservation and Sterilization, 4th edn., pp. 191–204. [Google Scholar]
  • 26.DiGuiseppe P.A., & Silhavy T.J. (2004) Pushing the envelope: lessons learned from stressing bacteria. ASM News, 72, 71–70. [Google Scholar]
  • 27.Rizzitello A.E., Harper J.R., & Silhavy T.J. (2001) Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J. Bacteriol., 183, 6794–7000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Behrens S., Maier R., de Cock H., Schmid F.X., & Gross C.A. (2001) The SurA periplasmic PpIase lacking its parvulin domains functions in vivo has chaperone activity. The EMBO J., 20, 285–294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Spiess C., Beil A., & Ehrmann M. (1999) A temperature-dependent switch from chaperone to protease in widely conserved heat shock protein. Cell, 97, 339–347. [DOI] [PubMed] [Google Scholar]
  • 30.Wiese A., Brandenburg K., Ulmer A.J., Seydel U., & Muller-Loennies S. (1999) The dual role of lipopolysaccharide as effector and target molecule. Biol. Chem., 380, 767–784. [DOI] [PubMed] [Google Scholar]
  • 31.Hancock R.E.W. (2001) Pseudomonas aeruginosa outer membrane proteins. http://www.cmdr.ubc.ca/bobh/omps/.
  • 32.Beveridge T.J. (1999) Structures of Gram-negative cell walls and their derived mambrane vesicles. J. Bacteriol., 181, 4725–4733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Trias H., & Nikaido H. (1990) Protein D2 channel of the Pseudomonas aeruginosa outer membrane has a binding site for basic amino acida and peptides. J. Biol. Chem., 265, 15680–15684. [PubMed] [Google Scholar]
  • 34.Siehnel R.J., Egli C., & Hancock R.E.W. (1992) Polyphosphate-selective porin OprO of Pseudomonas aeruginosa: expression, purification and sequence. Molecul. Microbiol., 6, 2319–2326. [DOI] [PubMed] [Google Scholar]
  • 35.Poole K. (2004) Acquired resistance. In Fraise A.P., Lambert P.A., & Maillard J-Y. (eds) Russell, Hugo & Ayliffe's Principles and Practice of Disinfection, Preservation & Sterilization, 4th edn., pp. 170–190. Blackwell Publishing, Oxford. [Google Scholar]
  • 36.Russell A.D. (1990) The bacterial spore and chemical sporicidal agents. Clin. Microbiol. Rev., 3, 99–119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Popham D.I. (2002) Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cell. Molecul. Life Sci., 59, 426–433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Driks A. (2002) Overview: development in bacteria: spore formation in Bacillus subtilis. Cell. Molecul. Life Sci., 59, 389–391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Takamatsu H., & Watabe K. (2002) Assembly and genetics of spore protective structures. Cell. Molecul. Life Sci., 59, 434–444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Young S.B., & Setlow P. (2004) Mechanism of killing of Bacillus subtilis spores by Decon and OxoneTM, two general decontaminants for biological agents. J. Appl. Microbiol., 96, 289–301. [DOI] [PubMed] [Google Scholar]
  • 41.Donlan R.M, & Costerton J.W. (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev., 15, 167–193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Gilbert P., Rickard A.H., & McBain A.J. (2004) Biofilms and antimicrobial resistance. In: Fraise A.P., Lambert P.A., & Maillard J-Y. (eds.) Russell, Hugo & Ayliffe's Principles and Practice of Disinfection, Preservation and Sterilization, 4th edn., pp. 139–153. Blackwell Publishing, Oxford. [Google Scholar]
  • 43.Setlow P. (1994) Mechanisms which contribute to the long-term survival of spores of Bacillus species. J. Appl. Bacteriol., 76, 49S–60S. [DOI] [PubMed] [Google Scholar]
  • 44.Russell A.D. (1999) Bacterial resistance to disinfectants: present knowledge and future problems. J. Hospital Infection, 43(Supplement), S57–S68. [DOI] [PubMed] [Google Scholar]
  • 45.Denyer S.P., & Hugo W.B. (1991) Biocide-induced damage to the cytoplasmic membrane. Soc. Appl. Bacteriol. Techn. Ser., 27, 171–187. [Google Scholar]
  • 46.Denyer S.P., & Chapman G.S.A.B. (1998) Mechanisms of action of disinfectants. International Biodeteriorat. Biodegradat., 41, 261–268. [Google Scholar]
  • 47.Lambert P.A. (2004) Mechanisms of action of biocides. In: Fraise A.P., Lambert P.A., & Maillard J-Y. (eds) Russell, Hugo & Ayliffe's Principles and Practice of Disinfection, Preservation and Sterilization, 4th edn., pp. 139–153. Blackwell Science, Oxford. [Google Scholar]
  • 48.Fitzgerald K.A., Davies A., & Russell A.D. (1992) Sensitivity and resistance of Escherichia coli and Staphylococcus aureus to chlorhexidine. Lett. Appl. Microbiol., 14, 33–36. [Google Scholar]
  • 49.Giles C.H., Smith D., & Huitson A. (1974) A general treatment and classification of the solute adsorption isotherm. 1. Theoretical. J. Coll. Interfac. Sci., 47, 755–765. [Google Scholar]
  • 50.Denyer S.P., & Maillard J-Y. (2002) Cellular impermeability and uptake of biocides and antibiotics in Gram-negative bacteria. J. Appl. Microbiol., 92, 35S–45S. [PubMed] [Google Scholar]
  • 51.Ayres H.M., Payne D.N., Furr J.R., & Russell A.D. (1998) Effect of permeabilizing agents on antibacterial agents against a simple Pseudomonas aeruginosa biofilm. Lett. Appl. Microbiol., 27, 79–82. [DOI] [PubMed] [Google Scholar]
  • 52.Lambert R.J.W., Hanlon G.W., & Denyer S.P. (2004) The synergistic effect of EDTA/antimicrobial combinations on Pseudomonas aeruginosa. J. Appl. Microbiol., 96, 244–253. [DOI] [PubMed] [Google Scholar]
  • 53.Russell A.D., & Chopra I. (1996) Understanding Antibacterial Action and Resistance, 2nd edn Ellis Horwood, Chichester. [Google Scholar]
  • 54.Helander I.M., Alakomi H-L., & Koski P. (1997) Polyethyleneimine is an effective permeabilizer of Gram-negative bacteria. Microbiology, 143, 3193–3199. [DOI] [PubMed] [Google Scholar]
  • 55.Helander I.M., Latva-kala K., & Lonatmaa K. (1998) Pemeabilizing action of polyethyleneimine on Salmonella typhimurium involves disruption of the outer membrane and interactions with lipopolysaccharide. Microbiology, 144, 385–390. [DOI] [PubMed] [Google Scholar]
  • 56.Jiang W., & Schwendeman S.P. (2000) Formaldehyde-mediated aggregation of protein antigens: comparison of untreated and formalinized model antigens. Biotechnol. Bioengng, 70, 507–517. [PubMed] [Google Scholar]
  • 57.Comas J., & Vives-Rego J. (1997) Assessment of gramicidin, formaldehyde and surfactants on Escherichia coli by flow cytometry using nucleic acid and membrane potential dyes. Cytometry, 29, 58–64. [DOI] [PubMed] [Google Scholar]
  • 58.Hughes R.C., & Thurman P.F. (1970) Cross-linking of bacterial cell walls with glutaraldehyde. Biochem. J., 119, 105–115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Munton T.J., & Russell A.D. (1970) Aspects of the action of glutaraldehyde on Escherichia coli. J. Appl. Bacteriol., 33, 410–419. [DOI] [PubMed] [Google Scholar]
  • 60.Munton T.J., & Russell A.D. (1972) Effect of glutaraldehyde on the outer layers of Escherichia coli. J. Appl. Bacteriol., 35, 193–199. [DOI] [PubMed] [Google Scholar]
  • 61.Power E.G.M., & Russell A.D. (1989) Glutaraldehyde: its uptake by sporing and non-sporing bacteria, rubber, plastic and an endoscope. J. Appl. Bacteriol., 67, 329–342. [DOI] [PubMed] [Google Scholar]
  • 62.Walsh S.E., Maillard J-Y., & Russell A.D. (1999) Ortho-phthalaldehyde: a possible alternative to glutaraldehyde for high-level disinfection. J. Appl. Microbiol., 87, 702–710. [DOI] [PubMed] [Google Scholar]
  • 63.Walsh S.E., Maillard J-Y., Russell A.D., & Simons C. (2000) Possible mechanisms for the relative efficacies of ortho-phthalaldehyde and glutaraldehyde against glutaraldehyde-resistant Mycobacterium chelonae. J. Appl. Microbiol., 91, 80–92. [DOI] [PubMed] [Google Scholar]
  • 64.Fraud S., Hann A.C., Maillard J-Y., & Russell A.D. (2003) Effects of ortho-phthalaldehyde, glutaraldehyde and chlorhexidine diacetate on Mycobacterium chelonae and Mycobacterium abscessus strains with modified permeability. J. Antimicrob. Chemother., 51, 575–584. [DOI] [PubMed] [Google Scholar]
  • 65.Hancock R.E.W. (1998) Resistance mechanisms in Pseudomonas aeruginosa and other nonfermentative Gram-negative bacteria. Clinical Infectious Diseases, 27(Supplement), S93–S99. [DOI] [PubMed] [Google Scholar]
  • 66.Preschel A. (2002) How do bacteria resist human antimicrobial peptides? Trends Microbiol., 10, 179–? [DOI] [PubMed] [Google Scholar]
  • 67.Anderson R.C., Hancock R.E.W., and Yu P-K. (2004) Antimicrobial peptides and bacterial- membrane interaction of ovine-derived cathelicidins. Antimicrob. Agents Chemotherapy, 48, 673–676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Pag U., Oedenkoven M., Papo N., Oren Z., Shai Y., and Sahl H.-G. (2004) In vitro activity and mode of action of diastereomeric antimicrobial peptides against bacterial clinical isolates. J. Antimicrob. Chemother., 53, 230–239. [DOI] [PubMed] [Google Scholar]
  • 69.Poxton I.R. (1993) Prokaryote envelope diversity. J. Appl. Bacteriol., 70, 1S–11S. [DOI] [PubMed] [Google Scholar]
  • 70.Nikaido H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Molec. Biol. Rev., 67, 593–656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Brown M.R.W., Collier P.J., & Gilbert P. (1993) Influence of growth rate on susceptibility to antimicrobial agents: modification of the cell envelope and batch and continuous culture studies. Antimicrobial Agents Chemother, 34, 1623–1628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Hugo W.B., & Franklin I. (1968) Cellular lipid and the antistaphylococcal activity of phenols. J. Gen. Microbiol., 52, 365–373. [PubMed] [Google Scholar]
  • 73.Hamilton W.A. (1968) The mechanism of the bacteriostatic action of tetrachlorosalicylanilidr. J. Gen. Microbiol., 50, 441–458. [DOI] [PubMed] [Google Scholar]
  • 74.Kolawole D.O. (1984) Resistance mechanismsof mucoid-grown Staphylococcus aureus to the antibacterial action of some disinfectants and antiseptics. FEMS Microbiol. Lett., 25, 205–209. [Google Scholar]
  • 75.(a) Seaman P.F., Day M., Russell A.D., and Ochs D. Susceptibility of capsuler strains of Staphylococcus aureus to some antibiotics, triclosan and cationic biocides. J. Antimicrob. Chemother. (in press). (b) Akimutsu, N., Hamaomoto, H., Inoue, R., Shohi, M., Akamine, A., Takeemori, K., Hamasaki, N. & Saiekimizu, K. (1999) Increase in resistance of methicillin-resistant Staphylococcus aureus to beta- lactams caused by mutations conferring resistance to benzalkonium chloride, a disinfectant widely used in hospitals. Antimicrob. Agents and Chemother, 43, 3042–3043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Suller M.T.E., & Russell A.D. (2000) Triclosan and antibiotic resistance in Staphylococcus aureus. J. Antimicrob. Chemother., 46, 11–18. [DOI] [PubMed] [Google Scholar]
  • 77.Sondheim G., Langsrud S., Heir E., & Holck A.L. (1998) Bacterial resistance to disinfectants containing quarternary ammonium compounds. Int. Biodeteriorat. Biodegradat., 41, 235–239. [Google Scholar]
  • 78.Gilbert P., Collier P.J., & Brown M.R.W. (1990) Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy and stringent response. Antimicrob. Agents Chemother, 34, 1865–1868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Fraise A.P. (2002) Susceptibility of antibiotic-resistant cocci to biocides. J. Appl. Microbiol., 92, 158S–152S. [PubMed] [Google Scholar]
  • 80.Meregheyyi L., Quentin R., Van Der Mee N.M., & Audurier (2000) Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl. Environ. Microbiol., 66, 5083–5086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.To M.S., Favrin S., Romanova N., & Griffiths M.W. (2002) Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl. Environ. Microbiol., 68, 5258–5264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Shen T.H. (1934) Cited by Croshaw, B. (1971) The destruction of mycobacteria. In: Hugo W.B. (ed.) Inhibition and Destruction of the Microbial Cell, pp. 429–449. Academic Press, London. [Google Scholar]
  • 83.Broadley S.J., Jenkins P.A., Furr J.R., & Russell A.D. (1995) Potentiation of the effects of chlorhexidine diacetate and cetylpyridinium chloride on mycobacteria by ethambutol. J. Med. Microbiol., 43, 458–460. [DOI] [PubMed] [Google Scholar]
  • 84.Manzoor S.E., Lambert P.A., Griffiths P.A., Gill M.J., & Fraise A.P. (1999) Reduced glutaraldehyde susceptibility in Mycobacterium chelonae associated with altered cell wall polysaccharides. J. Antimicrob. Chemother, 43, 759–763. [DOI] [PubMed] [Google Scholar]
  • 85.Viveiros M., Leandro C., & Amaral L. (2003) Mycobacterial efflux pumps and chemotherapeutic implications. Int. J. Antimicrob. Agents, 22, 274–278. [DOI] [PubMed] [Google Scholar]
  • 86.Miltner C.E., & Bermudez L.E. (2000) Mycobacterium avium grown in Acanthamoeba castellanii is protected from the effects of antimicrobials. Antimicrob. Agents Chemother., 44, 1990–1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Nicholson W.L., Munakato N., Horneck G., Melosh H.J., & Setlow P. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Molecul. Biol. Rev., 64, 548–572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88.Knott A.G., Dancer B.N., & Russell A.D. (1995) Development of resistance to biocides during sporulation of Bacillus subtilis. J. Appl. Bacteriol., 79, 492–498. [Google Scholar]
  • 89.Lambert P.A. (2004) Resistance of bacterial spores to chemical agents. In: Fraise A.P., Lambert P.A., & Maillard J-Y (eds.) Russell, Hugo & Ayliffe's Principles and Practice of Disinfection, Preservation and Sterilization, 4th edn., pp. 184–190. Blackwell Publishing, Oxford. [Google Scholar]
  • 90.Bayliss C.E., & Waites W.M. (1976) The effect of hydrogen peroxide on spores of Clostridium bifermentans. J. Gen. Microbiol., 96, 401–407. [DOI] [PubMed] [Google Scholar]
  • 91.Shin S-Y., Calvisi E.G., Beaman T.C., Prankratz H.S., Gerhardt P., & Marquis R.E. (1994) Microscopic and thermal characterization of hydrogen peroxide killing and lysis of spores and protection by transition metal ions, chelators, and antioxidants. Appl. Environ. Microbiol., 60, 3192–3197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Khadre M.A., Yousef A.E., & Kim J.-G. (2001) Microbiological aspects of ozone applications in food: a review. J. Food Sci., 66, 1241–1252. [Google Scholar]
  • 93.Khadre M.A., & Yousef A.E. (2001) Sporicidal action of ozone and hydrogen peroxide: a comparative study. Int. J. Food Microbiol., 71, 131–138. [DOI] [PubMed] [Google Scholar]
  • 94.Young S.B., & Setlow P. (2004) Mechanisms of killing of Bacillus subtilis spores by Decon and OxoneTM, two general decontaminants for biological agents. J. Appl. Microbiol., 96, 289–301. [DOI] [PubMed] [Google Scholar]
  • 95.Moir A., Corfe B.M., & Behravan J. (2002) Spore germination. Cell. Molecul. Life Sci., 59, 403–409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 96.Power E.G.M., & Russell A.D. (1989) Uptake of L-(14C)-alanine to glutaraldehyde-treated and untreated spores of Bacillus subtilis. FEMS Microbiol. Lett., 66, 271–276. [DOI] [PubMed] [Google Scholar]
  • 97.Williams N.D., & Russell A.D. (1003) Injury and repair in biocide-treated spores of Bacillus subtilis. FEMS Microbiol. Lett., 106, 183–186. [DOI] [PubMed] [Google Scholar]
  • 98.Russell A.D. (2003) bacterial resistance to biocides: current knowledge and future problems. In Lens P., Moran A.P., Mahoney T., Stoodley P., & O'Flaherty V. (eds.) Biofilms in Medicine, Industry and Environmental Biotechnology, pp. 512–533. IWA Publishers, London. [Google Scholar]
  • 99.Nikaido H. (1994) Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science, 264, 382–388. [DOI] [PubMed] [Google Scholar]
  • 100.Nikaido H. (1993) Transport across the bacterial outer membrane. J. Bioenergetics Biomembranes, 25, 581–589. [DOI] [PubMed] [Google Scholar]
  • 101.Nakae T. (1995) Role of membrane permeability in determining antibiotic resistance in Pseudomonas aeruginosa. Microbiol. Immunol., 39, 221–229. [DOI] [PubMed] [Google Scholar]
  • 102.Hancock R.E.W. (1997) The bacterial outer membrane as a drug barrier. Trends Microbiol., 5, 37–42. [DOI] [PubMed] [Google Scholar]
  • 103.Nikaido H. (1998) Multiple antibiotic resistance and efflux. Curr. Opin. Microbiol., 1, 516–523. [DOI] [PubMed] [Google Scholar]
  • 104.Nikaido H. (1998) Antibiotic resistance caused by multidrug efflux pumps. Clin. Infect. Dis., 27(Supplement 1), S32–S41. [DOI] [PubMed] [Google Scholar]
  • 105.Stickler D.J. (2004) Intrinsic resistance of Gram-negative bacteria. In: Fraise A.P., Lambert P.A., & Maillard J-Y. (eds.) Russell, Hugo & Ayliffe's Principles and Practice of Disinfection, Preservation and Sterilization, 4th edn., pp. 154–169. Blackwell Publishing, Oxford. [Google Scholar]
  • 106.Russell A.D., Furr J.R., & Pugh J.W. (1985) Susceptibility of porin and lipopolysaccharide- defective strains of Escherichia coli to a homologous series of esters of p-hydroxybenzoic acid. Int. J. Pharmaceut., 27, 163–173. [Google Scholar]
  • 107.Russell A.D., & Furr J.R. (1986) The effects of antiseptics, disinfectants and presewrvatives on smooth, rough and deep rough strains of Salmonella typhimurium. Int. J. Pharmaceut., 34, 115–123. [Google Scholar]
  • 108.Russell A.D., & Furr J.R. (1986) Susceptibility of porin and lipopolysaccharide-defective strains of Escherichia coli to some antiseptics and disinfectants. J. Hospital Infect., 8, 47–56. [DOI] [PubMed] [Google Scholar]
  • 109.Russell A.D., & Furr J.R. (1987) Comaprative sensitivity of smooth, rough and deep rough strains of Escherichia coli to chlorhexidine, quaternary ammoniumn compounds and dibromopropamidine isethionate. Int. J. Pharmaceut., 36, 191–197. [Google Scholar]
  • 110.Russell A.D., Furr J.R., & Pugh J.W. (1987) Sequential loss of outer membrane lipopolysaccharide and sensitivity of Escherichia coli to antibacterial agents. Int. J. Pharmaceut., 35, 227–232. [Google Scholar]
  • 111.Vaara M. (1992) Agents that increase the permeability of the outer membrane. Microbiol. Rev., 56, 395–411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 112.Stickler D.J., Jones G.L., & Russell A.D. (2003) Control of encrustation and blockage of Foley catheters. Lancet, 361, 1435–1437. [DOI] [PubMed] [Google Scholar]
  • 113.Cox A.D., & Wilkinson S.G. (1991) Ionizing groups of lipopolysaccharides of Pseudomonas cepacia in relation to antibiotic resistance. Molec. Microbiol., 5, 641–646. [DOI] [PubMed] [Google Scholar]
  • 114.Fraud S., Rees E.L., Mahenthiralingam E., Russell A.D., & Maillard J-Y. (2003) Aromatic alcohols and their effect on Gram-negative bacteria, cocci and mycobacteria. J. Antimicrob. Chemother, 51, 1435–1436. [DOI] [PubMed] [Google Scholar]
  • 115.Higgins C.S., Murtough S.M., Williams E., Hiom S.J., Payne D.J., Russell A.D., & Walsh T.R. (2001) Resistance to antibiotics and biocides among non-fermenting Gram-negative bacteria. Clin. Microbiol. Infect., 7, 308–315. [DOI] [PubMed] [Google Scholar]
  • 116.Tannert A., Pohl A., Pomorski T., & Herrmann A. (2003) Protein-mediated transbilayer movement of lipids in eukaryotes and prokaryotes: the relevance of ABC transporters. Int. J. Antimicrob. Agents, 22, 177–187. [DOI] [PubMed] [Google Scholar]
  • 117.Lage H. (2003) ABC-transporters: implications on drug resistance from microorganisms to human cancers. Int. J. Antimicrob.l Agents, 22, 188–199. [DOI] [PubMed] [Google Scholar]
  • 118.Butaye P., Cloeckaert A., & Schwarz S. (2003) Mobile genes coding for efflux-mediated antimicrobial resistance in Gram-positive and Gram-negative bacteria. Int. J. Antimicrob. Agents, 22, 205–210. [DOI] [PubMed] [Google Scholar]
  • 119.Fernandes P., Ferreira B.S., & Cabral J.M.S. (2003) Solvent tolerance in bacteria: the role of efflux pumps and cross-resistance with antibiotics. Int. J. Antimicrob. Agents, 22, 211–216. [DOI] [PubMed] [Google Scholar]
  • 120.Poole K. (2002) Mechanisms of bacterial and biocide resistance. J. Appl. Microb., 92, 55S–64S. [PubMed] [Google Scholar]
  • 121.Welker N.E. (1976) Microbial endurance and resistance to heat stress. In: Gray T.G.R, & Postgate J.R. (eds.) The Survival of Vegetative Microbes. 26th Symposium of the Society for General Microbiology, pp. 241–247. Cambridge University Press, Cambridge. [Google Scholar]
  • 122.Bradley C.R., & Fraise A.P. (1996) Heat and chemical resistance of entero-cocci. J. Hospital Infect., 34, 191–196. [DOI] [PubMed] [Google Scholar]
  • 123.Hitchener B.J., & Egan J.F. (1977) Outer membrane damage in sublethally heated Escherichia coli K-12. Can. J. Microbiol., 23, 311–318. [DOI] [PubMed] [Google Scholar]
  • 124.Katsui S., Tsuchido T., Hiramatsu R., Fujikawa S., Takano M., & Shibasaki I. (1982) Heat- induced blebbing and vesiculation of the outer membrabe of Escherichia coli. J. Bacteriol., 151, 1523–1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 125.Mackey B.M. (1983) Changes in antibiotic sensitivity and hydrophobicity in Escherichia coli injured by heating, freezing, drying or gamma radiation. FEMS Microbiol. Lett., 20, 395–399. [Google Scholar]
  • 126.Tsuchido T., Katsui T., Takeuchi A., Takano M., & Shibasaki I. (1985) Destruction of the outer membrane permeability barrier of Escherichia coli by heat treatment. Appl. Environ. Microbiol., 50, 298–303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 127.Tsuchido T., Aoki I., & Takano M. (1989) Interaction of the fluorescent dye, 1-N- phenylnaphthylamine with Escherichia coli cells during heat stress and recovery of heat stress. J. Gen. Microbiol., 135, 1941–1947. [DOI] [PubMed] [Google Scholar]
  • 128.Boziaris I.S., & Adams M.R. (2001) Temperature shock, injury and transient sensitivity to nisin in Gram-negatives. J. Appl. Microbiol., 91, 715–724. [DOI] [PubMed] [Google Scholar]
  • 129.Rowbury R.J. (2001) Extracellular sensing components and extracellular induction component alarrmones give early warning against stress in Escherichia coli. Adv. Microb. Physiol., 44, 215–257. [DOI] [PubMed] [Google Scholar]
  • 130.Polissi A., Goffin L., & Georgopoulos C. (1995) The Escherichia coli heat shock response and bacteriophage lambda development. FEMS Microbiol. Rev., 17, 159–169. [DOI] [PubMed] [Google Scholar]
  • 131.Yura T., Kanemori M., & Morita M.T. (2000) The heat shock response: regulation and function. In: Stortz G., & Hengge-Aronis R. (eds.) Bacterial Stress Responses, pp. 3–18. ASM Press, Washington, D.C. [Google Scholar]
  • 132.Setlow B., & Setlow P. (1996) Role of DNA repair in Bacillus subtilis spore resistance. J. Bacteriol., 178, 3486–3495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 133.Zamenhof S. (1960) Effects of heating dry bacteria and spores on their phenotype and genotype. Proc. Natl Acad. Sci. USA, 46, 101–105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 134.Rowe A.J., & Silverman G.J. (1970) The absorption-desorption of water by bacterial spores and its relation to dry heat resistance. Develop. Indust. Microbiol., 11, 311–326. [Google Scholar]
  • 135.MacLeod R.A., & Calcott P.H. (1976) Cold shock and freezing damage to microbes. In: Gray T.R.G, & Postgate J.R. (eds.) The Survival of vegetative Microbes, 26th Symposium of the Society for General Microbiology, pp. 81–109. Cambridge University Press, Cambridge. [Google Scholar]
  • 136.Rose A.H. (1976) Osmotic stress and microbial survival. In: Gray T.R.G., & Postgate J.R. (eds.) The Survival of Vegetative Microbes. 26th Symposium of the Society for General Microbiology, pp. 155–182. Cambridge University Press, Cambridge. [Google Scholar]
  • 137.Russell N.J. (1984) Mechanisms of thermal adaptation in bacteria: blueprints for survival. Trends Biochem. Sci., 9, 108–112. [Google Scholar]
  • 138.Neu H.C., & Heppel L.A. (1965) The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J. Biol. Chem., 240, 3685–3692. [PubMed] [Google Scholar]
  • 139.Asada S., Takano M., & Shibasaki I. (1979) Deoxyribonucleic acid strand breaks during drying of Escherichia coli on a hydrophoboc filter membrane. Appl. Environ. Microbiol., 37, 266–273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 140.Mackey B.M. (1984) Lethal and sublethal effects of refrigeration, freezing and freeze-drying on microorganisms. In: Andrew M.H.E., & Russell A.D. (eds.) The Revival of injured Microbes. Society for Applied Bacteriology Symposium Series No. 12, pp. 45–75. Academic Press, London. [PubMed] [Google Scholar]
  • 141.Hugo W.B. (1999) Historical introduction. In: Russell A.D., Hugo W.B., & Ayliffe G.A.J. (eds.) Principles and Practice of Disinfection, Preservation and Sterilization, 3rd edn., pp. 1–4. Blackwell Science, Oxford [Google Scholar]
  • 142.Gould G.W. (1989) Drying, raised osmotic pressure and low water activity. In: Gould G.W. (ed.) Mechanisms of Action of Food Preservation, pp. 97–117. Elsevier Applied Science, London. [Google Scholar]
  • 143.Wiggind P.W. (1990) Role of water in some biological processes. Microbiol. Rev., 54, 432–449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 144.Beveridge E.G. (1999) Preservation of medicines and cosmetics. In: Russell A.D., Hugo W.B., & Ayliffe G.A.J. (eds.) Principles and Practice of Disinfection, Preservation and Sterilization, 3rd edn., pp. 457–484. Blackwell Science, Oxford. [Google Scholar]
  • 145.Beveridge E.G. (1998) Microbial spoilage and preservation of pharmaceutical products. In: Hugo W.B., & Russell A.D. (eds.) Pharmaceutical Microbiology, 6th edn., pp. 355–373. Blackwell Science, Oxford. [Google Scholar]
  • 146.Koch A.L. (1995) Bacterial Growth and Form. Chapman and Hall, London. [Google Scholar]
  • 147.Milner J.L., McClennan D.J., & Wood J.M. (1987) Factors reducing and promoting the effectiveness of proline as an osmoprotectant in Escherichia coli. J. Gen. Microbiol., 133, 1851–1860. [DOI] [PubMed] [Google Scholar]
  • 148.Russell N.J., & Kogut M. (1985) Haloadaptation: salt sensing and cell envelope changes. Microbiol. Sci., 2, 345–350. [PubMed] [Google Scholar]
  • 149.Record M.T. Jr., Courtney E.S., Cayley S., & Guttman H.J. (1998) Responses of E.coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci., 23, 143–148. [DOI] [PubMed] [Google Scholar]
  • 150.Record M.T. Jr., Courteney E.S., Cayley S., & Guttman H.J. (1998) Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments. Trends Biochem. Sci., 23, 190–194. [DOI] [PubMed] [Google Scholar]
  • 151.Potts M. (2001) Desiccation tolerance: a simple process? Trends Microbiol., 11, 553–559. [DOI] [PubMed] [Google Scholar]
  • 152.Potts M. (1994) Desiccation tolerance of prokaryotes. Microbiol. Rev., 58, 755–805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 153.Kaletunc G., Lee J., Alpas H., & Bozoglu F. (2004) Evaluation of structural changes induced by high hydrostatic pressure in Leuconostoc mesenteroides. Appl. Environ. Microbiol., 70, 1116–1122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 154.Clery-Barraud C., Gaubert A., Masson P., & Vidal D. (2004) Combined effects of high hydrostatic pressure and temperature for inactivation of Bacillus anthracis spores. Appl. Environ. Microbiol., 70, 635–637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 155.Assar S.K., & Block S.S. (2001) Survival of microorganisms in the environment. In Block S.S. (ed.) Disinfection, Sterilization and Preservation, 5th edn., pp. 1221–1242. [Google Scholar]
  • 156.Krinksky N.I. (1976) Cellular damage initiated by visible light. In: Gray T.G.R., & Postgate J.R. (eds.) The Survival of Vegetative Microbes. 26th Symposium of the society for General Microbiology, pp. 209–239. Cambridge University Press, Cambridge. [Google Scholar]
  • 157.Farkas J. (1994) Tolerance of spores to ionizing radiation: mechanisms of inactivation, injury and repair. J. Appl.d Bacteriol., 76, 81S–90S. [DOI] [PubMed] [Google Scholar]
  • 158.Bridges B.A. (1976) Survival of bacteria following exposure to ultraviolet and ionizing radiation. In: Gray T.R.G., & Postgate J.R. (eds.) The Survival of Vegetative Microbes. 26th Symposium of the Society for General Microbiology, pp. 183–208. Cambridge University Press, Cambridge. [Google Scholar]
  • 159.Setlow R.B., & Carrier K.J. (1972) The disappearance of thymine dimers from DNA: an error- correcting process. Proc. Natl. Acad. Sci. USA, 51, 226–231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 160.Munakata N., & Rupert C.S. (1974) Dark repair of DNA containing ‘spore photoproducts’ in Bacillus subtilis. Molec. Gen. Genetics, 130, 239–250. [DOI] [PubMed] [Google Scholar]
  • 161.Narumi I. (2003) Unlocking radiation resistance mechanisms: still a long way to go. Trends Microbiol., 11, 422–425. [DOI] [PubMed] [Google Scholar]
  • 162.Thomas L., Lambert R.J.W., Maillard J-Y., & Russell A.D. (2000) Development of resistance to chlorhexidine diacetate in Pseudomonas aeruginosa and the effect of a ‘residual’ concentration. J. Hosp. Infect., 46, 297–303. [DOI] [PubMed] [Google Scholar]
  • 163.Adolfsson-Erici M., Petterson M., Parkkonen J., & Sturve J. (2002) Triclosan, a commonly used bactericide found in human milk and in the aquatic environment in Sweden. Chemosphere, 46, 1485–1489. [DOI] [PubMed] [Google Scholar]
  • 164.Sullivan A., Wretlind B., & Nord C.E. (2003) Will triclosan in toothpaste select for resistant oral streptococci? Clin. Microbiol. Infect., 9, 306–309. [DOI] [PubMed] [Google Scholar]
  • 165.Russell A.D. (2004) Whither triclosan? J. Antimicrob. Chemother., 53, 693–695. [DOI] [PubMed] [Google Scholar]
  • 166.Amaral L., & Lothian V. (1991) Effects of chlorpromazine on the envelope proteins of Escherichia coli. Antimicrob. Agents Chemother., 35, 1923–1924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 167.Russell A.D. (2004) Bacterial adaptation to antiseptics, disinfectants and preservatives is not a new phenomenon. J. Hosp. Infect., 57, 97–104. [DOI] [PubMed] [Google Scholar]
  • 168.Lambert P.A. (2002) Cellular impermeability and uptake of biocides and antibiotics in Gram-positive bacteria and mycobactetia. J. Appl. Microbiol., 92, 46S–54S. [PubMed] [Google Scholar]

Articles from Science Progress are provided here courtesy of SAGE Publications

RESOURCES