Weakening Effect of Cell Permeabilizers on Gram-Negative Bacteria Causing Biodeterioration
Open accessAbstract
Gram-negative bacteria play an important role in the formation and stabilization of biofilm structures on stone surfaces. Therefore, the control of growth of gram-negative bacteria offers a way to diminish biodeterioration of stone materials. The effect of potential permeabilizers on the outer membrane (OM) properties of gram-negative bacteria was investigated and further characterized. In addition, efficacy of the agents in enhancing the activity of a biocide (benzalkonium chloride) was assessed. EDTA, polyethylenimine (PEI), and succimer (meso-2,3-dimercaptosuccinic) were shown to be efficient permeabilizers of the members of Pseudomonas and Stenotrophomonas genera, as indicated by an increase in the uptake of a hydrophobic probe (1-N-phenylnaphthylamine) and sensitization to hydrophobic antibiotics. Visualization of Pseudomonas cells treated with EDTA or PEI by atomic force microscopy revealed damage in the outer membrane structure. PEI especially increased the surface area and bulges of the cells. Topographic images of EDTA-treated cells were compatible with events assigned for the effect of EDTA on outer membranes, i.e., release of lipopolysaccharide and disintegration of OM structure. In addition, the effect of EDTA treatment was visualized in phase-contrast images as large areas with varying hydrophilicity on cell surfaces. In liquid culture tests, EDTA and PEI supplementation enhanced the activity of benzalkonium chloride toward the target strains. Use of permeabilizers in biocide formulations would enable the use of decreased concentrations of the active biocide ingredient, thereby providing environmentally friendlier products.
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Structural changes in the membrane, such as fluidity alteration, could lead to a slight modification in the external surface of the Gram-positive cell wall such that they appear less rough but more bumpy than Gram-negative bacteria.
“The structural changes in the membrane, such as fluidity alteration, could lead to a slight modification in the external surface of the Gram-positive cell wall such that they appears less rough but more bumpy than Gram-negative bacteria [120].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [120]
In Gram-positive bacteria, carvacrol moves through the peptidoglycan layer and then acts on the cytoplasmic membrane.
“However, in Gram-positive bacteria, carvacrol moves through the peptidoglycan layer and then acts on the cytoplasmic membrane.”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [120]
Cites
Molecular Basis of Bacterial Outer Membrane Permeability Revisited
Nikaido, H. (2003) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.67.4.593-656.2003 · Cited by 4,316 · see citing works
IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans
Carter, R. L. (1980) · Journal of Clinical Pathology · doi:10.1136/jcp.33.1.98-b · Cited by 3,455 · see citing works
Microbial Biofilms: from Ecology to Molecular Genetics
Davey, M. E., & O’Toole, G. A. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.4.847-867.2000 · Cited by 3,072 · see citing works
Agents that increase the permeability of the outer membrane
Vaara, M. (1992) · Microbiological Reviews · doi:10.1128/mr.56.3.395-411.1992 · Cited by 1,879 · see citing works
Lactic Acid Permeabilizes Gram-Negative Bacteria by Disrupting the Outer Membrane
Alakomi, H.-L., Skyttä, E., Saarela, M., Mattila-Sandholm, T., Latva-Kala, K., & Helander, I. M. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.5.2001-2005.2000 · Cited by 1,093 · see citing works
Self-citationBiodeterioration of stone: a review
Warscheid, T., & Braams, J. (2000) · International Biodeterioration & Biodegradation · doi:10.1016/s0964-8305(00)00109-8 · Cited by 1,065 · see citing works
Relationship between Desiccation and Exopolysaccharide Production in a Soil Pseudomonas sp
Roberson, E. B., & Firestone, M. K. (1992) · Applied and Environmental Microbiology · doi:10.1128/aem.58.4.1284-1291.1992 · Cited by 633 · see citing works
Efflux-mediated multiresistance in Gram-negative bacteria
Poole, K. (2004) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2004.00763.x · Cited by 612 · see citing works
Fluorometric assessment of Gram-negative bacterial permeabilization
Helander, I. M., & Mattila, T. (2000) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2000.00971.x · Cited by 532 · see citing works
Self-citationChelator-Induced Dispersal and Killing of Pseudomonas aeruginosa Cells in a Biofilm
Banin, E., Brady, K. M., & Greenberg, E. P. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.3.2064-2069.2006 · Cited by 473 · see citing works
Bacterial target sites for biocide action
Maillard, J. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.92.5s1.3.x · Cited by 469 · see citing works
Endotoxin in Health and Disease
(2020) · CRC Press eBooks · doi:10.1201/9781003064961 · Cited by 398 · see citing works
Similarities and differences in the responses of microorganisms to biocides
Russell, A. D. (2003) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkg422 · Cited by 394 · see citing works
Gilbert, P., & McBain, A. J. (2003) · Clinical Microbiology Reviews · doi:10.1128/cmr.16.2.189-208.2003 · Cited by 335 · see citing works
Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria
Nikaido, H. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0247 · Cited by 319 · see citing works
Cyanobacteria and Biodeterioration of Cultural Heritage: A Review
Crispim, C. A., & Gaylarde, C. C. (2004) · Microbial Ecology · doi:10.1007/s00248-003-1052-5 · Cited by 318 · see citing works
Cellular impermeability and uptake of biocides and antibiotics in Gram-negative bacteria
Denyer, S. P., & Maillard, J. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.92.5s1.19.x · Cited by 278 · see citing works
Interactions between Biocide Cationic Agents and Bacterial Biofilms
Campanac, C., Pineau, L., Payard, A., Baziard, G., & Roques, C. G. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.5.1469-1474.2002 · Cited by 265 · see citing works
Polyethyleneimine is an effective permeabilizer of Gram negative bacteria
Helander, I. M., Alakomi, H.-L., Latva-Kala, K., & Koski, P. (1997) · Microbiology · doi:10.1099/00221287-143-10-3193 · Cited by 237 · see citing works
Self-citationGeobiology of a microbial endolithic community in the Yellowstone geothermal environment
Walker, J. J., Spear, J. R., & Pace, N. R. (2005) · Nature · doi:10.1038/nature03447 · Cited by 225 · see citing works
Outer Membranes and Efflux: The Path to Multidrug Resistance in Gram- Negative Bacteria
Poole, K. (2002) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201023378454 · Cited by 198 · see citing works
Meincken, M., Holroyd, D. L., & Rautenbach, M. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.10.4085-4092.2005 · Cited by 192 · see citing works
Antibiotic and biocide resistance in bacteria: Introduction
Russell, A. D. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.92.5s1.14.x · Cited by 177 · see citing works
Flora, S. J. S., Pande, M., & Mehta, A. K. (2003) · Chemico-Biological Interactions · doi:10.1016/s0009-2797(03)00025-5 · Cited by 171 · see citing works
Polyethyleneimine in immobilization of biocatalysts
Bahulekar, R., AYYANGAR, N. R., & Ponrathnam, S. (1991) · Enzyme and Microbial Technology · doi:10.1016/0141-0229(91)90101-f · Cited by 157 · see citing works
Algal and Cyanobacterial Biofilms on Calcareous Historic Buildings
Crispim, C. A., Gaylarde, P. M., & Gaylarde, C. C. (2003) · Current Microbiology · doi:10.1007/s00284-002-3815-5 · Cited by 152 · see citing works
Loughlin, M. F., Jones, M. V., & Lambert, P. A. (2002) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/49.4.631 · Cited by 148 · see citing works
Saarela, M., Alakomi, H., Suihko, M., et al. (2004) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2003.12.003 · Cited by 136 · see citing works
Self-citationHelander, I. M., Latva‐Kala, K., & Lounatmaa, K. (1998) · Microbiology · doi:10.1099/00221287-144-2-385 · Cited by 119 · see citing works
Self-citationBacterial target sites for biocide action.
Maillard, J.-Y. (2002) · PubMed · Cited by 118 · see citing works
Dornieden, T., Gorbushina, A. A., & Krumbein, W. E. (2000) · International Biodeterioration & Biodegradation · doi:10.1016/s0964-8305(00)00107-4 · Cited by 104 · see citing works
Modification of the interaction betweenEscherichia coli and bacteriophage in saline sediment
Roper, M. M., & Marshall, K. C. (1974) · Microbial Ecology · doi:10.1007/bf02512375 · Cited by 97 · see citing works
Microbial Surfaces Investigated Using Atomic Force Microscopy
Bolshakova, A. V., Kiselyova, O. I., & Yaminsky, I. V. (2004) · Biotechnology Progress · doi:10.1021/bp049742c · Cited by 93 · see citing works
Walsh, A. G., Matewish, M. J., Burrows, L. L., et al. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01741.x · Cited by 91 · see citing works
Microbial mats and the search for minimal ecosystems
Guerrero, R., Piqueras, M., & Berlanga, M. (2002) · International Microbiology · doi:10.1007/s10123-002-0094-8 · Cited by 87 · see citing works
Biodeterioration of natural stone with special reference to nitrifying bacteria
Mansch, R., & Bock, E. (1998) · Biodegradation · doi:10.1023/a:1008381525192 · Cited by 80 · see citing works
Colored moderately thermophilic bacteria in paper-machine biofilms
Kolari, M., Nuutinen, J., Rainey, F. A., et al. (2003) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-003-0047-z · Cited by 74 · see citing works
Alakomi, H., Saarela, M., & Helander, I. M. (2003) · Microbiology · doi:10.1099/mic.0.26312-0 · Cited by 74 · see citing works
Self-citationWang, E. T., Tan, Z., Willems, A. L., et al. (2002) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/00207713-52-5-1687 · Cited by 74 · see citing works
Salt, D. E., Hay, S., Thomas, O. R. T., et al. (1995) · Enzyme and Microbial Technology · doi:10.1016/0141-0229(94)00043-q · Cited by 53 · see citing works
Bansal‐Mutalik, R., & Gaikar, V. G. (2002) · Enzyme and Microbial Technology · doi:10.1016/s0141-0229(02)00178-3 · Cited by 38 · see citing works
Comparative Studies of Microbial Communities on Stone Monuments in Temperate and Semi-Arid Climates
May, E., Papida, S., Abdulla, H., et al. (2000) · Springer eBooks · doi:10.1007/978-1-4615-4239-1_4 · Cited by 29 · see citing works
Small Heat Shock Proteins (sHSPs) As Potential Drug Targets
Crabbe, M. J. C., & Hepburne‐Scott, H. W. (2001) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201013378833 · Cited by 25 · see citing works
Ayres, Payne, Furr, J. R., et al. (1998) · Letters in Applied Microbiology · doi:10.1046/j.1472-765x.1998.00364.x · Cited by 18 · see citing works
Raaska, L., Alakomi, H., Salkinoja-Salonen, M. S., et al. (1999) · Journal of Industrial Microbiology & Biotechnology · doi:10.1038/sj.jim.2900596 · Cited by 7 · see citing works
Self-citationAnti microbial activity of dimercaptosuccinic acid (DMSA): a new chelating agent.
Vineeta, N., Singh, V., & Makkar, S. (2001) · PubMed · Cited by 5 · see citing works
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Ouwehand, A. C., Forssten, S., Hibberd, A. A., Lyra, A., & Stahl, B. (2016) · Annals of Medicine · doi:10.3109/07853890.2016.1161232 · Cited by 216 · see citing works
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- Authors
- Alakomi, H.-L., Paananen, A., Suihko, M.-L., Helander, I. M., & Saarela, M.
- Affiliations
- VTT Technical Research Centre of Finland (FI)
- University of Helsinki (FI)
- Corresponding author
- Alakomi, H.-L.
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2006-07
- Volume
- 72
- Issue
- 7
- Pages
- 4695-4703
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- OpenAlex
- W2171028011
- Cited by
- 141
- References
- 46
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 6 · 2023: 5 · 2022: 6 · 2021: 14 · 2020: 14 · 2019: 11 · 2018: 8 · 2017: 7 · 2016: 9 · 2015: 9 · 2014: 4 · 2013: 8 · 2012: 10
- FWCI
- 1.80
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Chemistry › Organic Chemistry › Antimicrobial agents and applications
- Physical Sciences › Earth and Planetary Sciences › Earth-Surface Processes › Building materials and conservation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Keywords
- Gram-negative bacteria, stone biodeterioration, outer membrane disruption, EDTA, polyethyleneimine, succimer, benzalkonium chloride, Pseudomonas, Stenotrophomonas, lipopolysaccharide release, hydrophobic antibiotics
- MeSH terms
- Anti-Bacterial Agents, Calcium Carbonate, Cell Membrane, Cell Membrane Permeability, Edetic Acid, Gram-Negative Bacteria, Microbial Sensitivity Tests, Molecular Sequence Data, Polyethyleneimine, Pseudomonas, Silicon Dioxide, Sequence Analysis, DNA, Microscopy, Atomic Force, Sinorhizobium, Stenotrophomonas
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