Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Home
  • Home
Hostname: page-component-559fc8cf4f-qpj69 Total loading time: 0.567 Render date: 2021-03-04T00:27:05.900Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }
EnglishFrançais
Microscopy and Microanalysis Microscopy and Microanalysis

Article contents

The Effects of β-Lactam Antibiotics on Surface Modifications of Multidrug-Resistant Escherichia coli: A Multiscale Approach

Published online by Cambridge University Press:  14 March 2019

Samuel C. Uzoechi  and
Nehal I. Abu-Lail [Opens in a new window]
Samuel C. Uzoechi
Affiliation:
Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, WA 99164, USA
Nehal I. Abu-Lail
Affiliation:
Department of Biomedical Engineering, The University of Texas at San Antonio, San Antonio, TX 78249, USA
Corresponding
E-mail address:
nehal.abu-lail@utsa.edu
Get access
Rights & Permissions[Opens in a new window]

Abstract

Possible multidrug-resistant (MDR) mechanisms of four resistant strains of Escherichia coli to a model β-lactam, ampicillin, were investigated using contact angle measurements of wettability, crystal violet assays of permeability, biofilm formation, fluorescence imaging, and nanoscale analyses of dimensions, adherence, and roughness. Upon exposure to ampicillin, one of the resistant strains, E. coli A5, changed its phenotype from elliptical to spherical, maintained its roughness and biofilm formation abilities, decreased its length and surface area, maintained its cell wall integrity, increased its hydrophobicity, and decreased its nanoscale adhesion to a model surface of silicon nitride. Such modifications are suggested to allow these cells to conserve energy during metabolic dormancy. In comparison, resistant strains E. coli D4, A9, and H5 elongated their cells, increased their roughness, increased their nanoscale adhesion forces, became more hydrophilic, and increased their biofilm formation upon exposure to ampicillin. These results suggest that these strains resisted ampicillin through biofilm formation that possibly introduces diffusion limitations to antibiotics. Investigations of how MDR bacterial cells modify their surfaces in response to antibiotics can guide research efforts aimed at designing more effective antibiotics and new treatment strategies for MDR bacterial infections.

Keywords

adhesion force AFM antibiotics β-lactam biofilms dimensions E. coli multidrug-resistance (MDR) permeability roughness
Type
Biological Science Applications
Information
Microscopy and Microanalysis , Volume 25 , Issue 1 , February 2019 , pp. 135 - 150
Copyright
Copyright © Microscopy Society of America 2019 

Access options

Get access to the full version of this content by using one of the access options below.
If you should have access and can't see this content please contact technical support.

References

Absolom, DR et al. (1983). Surface thermodynamics of bacterial adhesion. Appl Environ Microbiol 46(1), 90–97.CrossRefGoogle ScholarPubMed
Abu-Lail, L (2012). Using atomic force microscopy to measure anti-adhesion effects on uropathogenic bacteria, observed in urine after cranberry juice consumption. J Biomater Nanobiotechnol 03(04), 533–540.CrossRefGoogle Scholar
Abu-Lail, NI & Camesano, TA (2003). Role of ionic strength on the relationship of biopolymer conformation, DLVO contributions, and steric interactions to bioadhesion of pseudomonas putida KT2442. Biomacromolecules 4(4), 1000–1012.CrossRefGoogle ScholarPubMed
Abu-Lail, NI & Camesano, TA (2006). The effect of solvent polarity on the molecular surface properties and adhesion of Escherichia coli. Colloids Surf B 51(1), 62–70.CrossRefGoogle ScholarPubMed
Aeschlimann, JR (2003). The role of multidrug efflux pumps in the antibiotic resistance of Pseudomonas aeruginosa and other gram-negative bacteria. Pharmacotherapy 23(7), 916–924.CrossRefGoogle ScholarPubMed
Aguayo, S et al. (2015). Single-bacterium nanomechanics in biomedicine: Unravelling the dynamics of bacterial cells. Nanotechnology. 26(6), 062001.CrossRefGoogle ScholarPubMed
Ali, R et al. (2014). Role of polymerase chain reaction (PCR) in the detection of antibiotic-resistant Staphylococcus aureus. Egyptian Journal of Medical Human Genetics 15(3), 293–298.CrossRefGoogle Scholar
Allen, HK et al. (2010). Call of the wild: Antibiotic resistance genes in natural environments. Nature Reviews Microbiology 8(4), 251–259.CrossRefGoogle ScholarPubMed
Allison, DP et al. (2011). Bacterial immobilization for imaging by atomic force microscopy. J Visualized Exp (54), 5–7. doi: 10.3791/2880.Google ScholarPubMed
Alves, CS et al. (2010). Escherichia coli cell surface perturbation and disruption induced by antimicrobial peptides BP100 and pepR. J Biol Chem 285(36), 27536–27544.CrossRefGoogle ScholarPubMed
Arslan, B et al. (2018). Characterizing interaction forces between actin and proteins of the tropomodulin family reveals the presence of the N-terminal actin-binding site in leiomodin. Arch Biochem Biophys. Elsevier, 638(October 2017), 18–26.CrossRefGoogle ScholarPubMed
Babic, M & Bonomo, RA (2006). What's new in antibiotic resistance? Focus on beta-lactamases. Drug Resist Updates 9(3), 142–156.CrossRefGoogle ScholarPubMed
Bendezú, FO & De Boer, PAJ (2008). Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli. J Bacteriol 190(5), 1792–1811.CrossRefGoogle ScholarPubMed
Bhatti, AR, DeVoe, IW & Ingram, JM (1976). Cell division in Pseudomonas aeruginosa: Participation of alkaline phosphatase. J Bacteriol 126(1), 400–409.CrossRefGoogle ScholarPubMed
Bonomo, RA (2018). Multiple antibiotic-resistant bacteria in long-term-care facilities: An emerging problem in the practice of infectious diseases author (s): Robert A. Bonomo Published by: Oxford University Press Stable. Available at http://www.jstor.org/stable/4482385SPECIA. 31(6), 1414–1422.Google Scholar
Bou, G et al. (2012). Fast assessment of resistance to carbapenems and ciprofloxacin of clinical strains of Acinetobacter baumannii. J Clin Microbiol 50(11), 3609–3613.CrossRefGoogle ScholarPubMed
Braga, PC & Ricci, D (1998). Atomic force microscopy: Application to investigation of Escherichia coli morphology before and after exposure to cefodizime. Dow. Antimicrob Agent Chemother 42(1), 1–6.CrossRefGoogle Scholar
Brown, AN et al. (2012). Nanoparticles functionalized with ampicillin destroy multiple-antibiotic-resistant isolates of Pseudomonas aeruginosa and Enterobacter aerogenes and methicillin-resistant Staphylococcus aureus. Appl Environ Microbiol 78(8), 2768–2774.CrossRefGoogle ScholarPubMed
Brown, CA & Harold, RP (1979). In Vitro Synthesis of Peptidoglycan by/β-Lactam-Sensitive and -Resistant Strains of Neisseria gonorrhoeae: Effects of/BLactam and Other Antibiotics.CrossRefGoogle Scholar
Camesano, TA & Abu-Lail, NI (2002). Heterogeneity in bacterial surface polysaccharides, probed on a single-molecule basis. Biomacromolecules 3(4), 661–667.CrossRefGoogle ScholarPubMed
Camesano, TA, Liu, Y & Pinzon-Arango, PA (2007). Cranberry prevents the adhesion of bacteria: Overview of relevant health benefits. Agro Food Ind Hi Tech 18(1, S), 24–27.Google Scholar
Chen, YY et al. (2009). Surface rigidity change of Escherichia coli after filamentous bacteriophage infection. Langmuir 25(8), 4607–4614.CrossRefGoogle ScholarPubMed
Cho, H & Bernhardt, TG (2014). Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell 159(6), 1310–1311.CrossRefGoogle ScholarPubMed
Chroma, M & Kolar, M (2010). Genetic methods for detection of antibiotic resistance: Focus on extended-spectrum β-lactamases. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 154(4), 289–396. Available at http://www.ncbi.nlm.nih.gov/pubmed/21293539.CrossRefGoogle ScholarPubMed
CLSI (2017). Performance standards for antimicrobial susceptibility testing. 27th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute, Performance standards for antimicrobial susceptibility testing. 27th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute.Google Scholar
Coleman, K (2011). Diazabicyclooctanes (DBOs): A potent new class of non-β-lactam β-lactamase inhibitors. Curr Opin Microbiol 14(5), 550–555.CrossRefGoogle ScholarPubMed
Costerton, J et al. (1995). Microbial biofilms. Annu Rev Microbiol 49, 711–745.CrossRefGoogle ScholarPubMed
Daffonchio, D & Verstraete, W (1995). Contact angle measurement and cell hydrophobicity of granular sludge from upflow anaerobic sludge bed reactors. Appl Environ Microbiol 61(10), 3676–3680.CrossRefGoogle ScholarPubMed
Dasgupta, T et al. (1994). Characterization of lipopolysaccharide-deficient mutants of Pseudomonas aeruginosa derived from serotypes O3, O5, and O6. Infect Immun 62(3), 809–817.CrossRefGoogle ScholarPubMed
Delcour, AH (2009). Outer membrane permeability and antibiotic resistance. Biochim Biophys Acta 1794(5), 808–816.CrossRefGoogle ScholarPubMed
Devi, KP et al. (2010). Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J Ethnopharmacol 130(1), 107–115.CrossRefGoogle ScholarPubMed
Doktycz, MJ et al. (2003). AFM imaging of bacteria in liquid media immobilized on gelatin coated mica surfaces. Ultramicroscopy 97(1–4), 209–216.CrossRefGoogle ScholarPubMed
Dong, H et al. (2004). Growing group of extended spectrum: The CTX-M enzymes. Antimicrob Agent Chemother 48(1), 1–14.Google Scholar
Donlan, RM (2002). Biofilms: Microbial life on surfaces. Emerg Infect Diseases. Available at http://www.cdc.gov/ncidod/EID/vol8no9/02-0063.htm, 8(9), 881–890.CrossRefGoogle ScholarPubMed
Dufrêne, YF (2002). Atomic force microscopy, a powerful tool in microbiology. J Bacteriol 184(19), 5205–5213.CrossRefGoogle ScholarPubMed
Durodie, J et al. (1995). Rapid detection of antimicrobial activity using flow cytometry. Cytometry 21(4), 374–377.CrossRefGoogle ScholarPubMed
Eastman, T & Zhu, D (1996). Adhesion forces between surface-modified AFM tips and a mica surface. Langmuir 12(11), 2859–2862.CrossRefGoogle Scholar
Eriksson, M, Nielsen, PE & Good, L (2002). Cell permeabilization and uptake of antisense peptide-peptide nucleic acid (PNA) into Escherichia coli. J Biol Chem 277(9), 7144–7147.CrossRefGoogle ScholarPubMed
Filho, RP et al. (2010). Prodrugs available on the Brazilian pharmaceutical market and their corresponding bioactivation pathways. Brazilian J Pharmaceutical Sci 46(3), 393–420.CrossRefGoogle Scholar
Fruci, M & Poole, K (2016). Bacterial stress responses as determinants of antimicrobial resistance. Stress Environ Regul Gene Expression Adaptation Bacteria 1(April), 115–136.CrossRefGoogle Scholar
Garrett, TR & Zhang, Z (2008). Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 18(9), 1049–1056.CrossRefGoogle Scholar
Ghuysen, J-M (1994). Molecular structures of penicillin-binding proteins and β-lactamases. Trends Microbiol 2(10), 372–80.CrossRefGoogle Scholar
Golding, CG et al. (2016). The scanning electron microscope in microbiology and diagnosis of infectious disease. Sci Rep 6(February), 1–8.CrossRefGoogle ScholarPubMed
Gordesli, FP & Abu-Lail, NI (2012). The role of growth temperature in the adhesion and mechanics of pathogenic L. monocytogenes: An AFM study. Langmuir 28(2), 1360–1373.CrossRefGoogle Scholar
Grant, LM & Ducker, WA (1997). Effect of substrate hydrophobicity on surface − aggregate geometry: Zwitterionic and nonionic surfactants. J Phys Chem B 101(27), 5337–5345.CrossRefGoogle Scholar
Gupta, A (2015). Original research article biofilm quantification and comparative analysis of MIC (minimum inhibitory concentration) & MBIC (minimum biofilm inhibitory concentration) value for different antibiotics against E. coli. 4(2), 198–224.Google Scholar
Halder, S et al. (2015). Alteration of Zeta potential and membrane permeability in bacteria: A study with cationic agents. Springer Plus 4(1), 672.CrossRefGoogle ScholarPubMed
Hawkey, PM et al. (2018). Treatment of infections caused by multidrug-resistant gram-negative bacteria: Report of the British society for antimicrobial chemotherapy/healthcare infection society/British infection association joint working party. J Antimicrob Chemother 73(March 2015), iii2-iii78.CrossRefGoogle ScholarPubMed
Hoffman, LR et al. (2005). Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436(7054), 1171–1175.CrossRefGoogle ScholarPubMed
Huang, Q et al. (2015). Atomic force microscopy measurements of bacterial adhesion and biofilm formation onto clay-sized particles. Sci Rep 5(November), 1–12.Google ScholarPubMed
Hutter, JL & Bechhoefer, J (1993). Calibration of atomic-force microscope tips. Rev Sci Instrum 64(7), 1868–1873.CrossRefGoogle Scholar
Ito, A et al. (2009). Increased antibiotic resistance of Escherichia coli in mature biofilms. Appl Environ Microbiol 75(12), 4093–4100.CrossRefGoogle ScholarPubMed
Jacoby, GA & Medeiros, AA (1991). More extended-spectrum beta-lactamases. Antimicrob Agents Chemother 35(9), 1697–1704.CrossRefGoogle ScholarPubMed
Jenkins, SG & Schuetz, AN (2012). Current concepts in laboratory testing to guide antimicrobial therapy. Mayo Clin Proc 87(3), 290–308.CrossRefGoogle ScholarPubMed
Justice, SS et al. (2007). Morphological plasticity as a bacterial survival strategy. Nat Rev Micro, advanced o. Available at file:///c:/pdf/rfd6662.pdf%5Cnfile:///home/ford/Documents/PDF/rfd6662.pdf.Google Scholar
Kaplan, JB (2011). Antibiotic-induced biofilm formation. Int J Artif Organs 34(9), 737–751.CrossRefGoogle ScholarPubMed
Kennedy, WPU & Murdoch, JMC (1963). Ampicillin in treatment of certain gram-negative bacterial infections. BMJ 2(5363), 962–965.CrossRefGoogle ScholarPubMed
Khalili, AA & Ahmad, MR (2015). A review of cell adhesion studies for biomedical and biological applications. Int J Mol Sci 16(8), 18149–18184.CrossRefGoogle ScholarPubMed
Krasowska, A & Sigler, K (2014). How microorganisms use hydrophobicity and what does this mean for human needs? Front Cell Infect Microbiol 4(August), 1–7.CrossRefGoogle ScholarPubMed
Kumarasamy, KK et al. (2010). Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study. Lancet Infect Dis 10(9), 597–602.CrossRefGoogle ScholarPubMed
Lambert, PA (2002). Cellular impermeability and uptake of biocides and antibiotics in Gram-positive bacteria and mycobacteria. J Appl Microbiol 92(s1), 46S–54S.CrossRefGoogle ScholarPubMed
Lee, H et al. (2017). Competitive adsorption of polyelectrolytes onto and into pellicle-coated hydroxyapatite investigated by QCM–D and force spectroscopy. doi: 10.1021/acsami.7b02774.CrossRefGoogle Scholar
Lewis, K (2007). Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5(1), 48–56.CrossRefGoogle ScholarPubMed
Limoli, DH et al. (2015). Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol Spectr 3(3), 1–30.CrossRefGoogle ScholarPubMed
Liu, Y et al. (2006). Role of cranberry juice on molecular-scale surface characteristics and adhesion behavior of Escherichia coli. Biotechnol Bioeng 93(2), 297–305.CrossRefGoogle ScholarPubMed
Livermore, DM (2004). The need for new antibiotics. Clin Microbiol Infect 10(Suppl 4), 1–9.CrossRefGoogle ScholarPubMed
Longo, G et al. (2013). Antibiotic-induced modifications of the stiffness of bacterial membranes. J Microbiol Methods 93(2), 80–84.CrossRefGoogle ScholarPubMed
Luyt, C-E et al. (2014). Antibiotic stewardship in the intensive care unit. Crit Care 18(5), 480.CrossRefGoogle ScholarPubMed
Ma, L, Conover, M, Lu, H, Parsek, MR, Bayles, K & Wozniak, DJ (2009). Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5(3). e1000354. doi: 10.1371/journal.ppat.1000354.CrossRefGoogle ScholarPubMed
Mei, L et al. (2011). Influence of surface roughness on streptococcal adhesion forces to composite resins. Dent Mater 27(8), 770–778.CrossRefGoogle ScholarPubMed
Meincken, M, Holroyd, DL & Rautenbach, M (2005). Atomic force microscopy study of the effect of antimicrobial peptides on the cell envelope of Escherichia coli. Society 49(10), 4085–4092.Google ScholarPubMed
Mohammad, H et al. (2015) Anti-biofilm activity and synergism of novel thiazole compounds with glycopeptide antibiotics against multidrug-resistant Staphylococci. J Antibiot 68(4), 259–266.CrossRefGoogle ScholarPubMed
Mohanty, S et al. (2012). An investigation on the antibacterial, cytotoxic, and antibiofilm efficacy of starch-stabilized silver nanoparticles. Nanomedicine 8(6), 916–924.CrossRefGoogle ScholarPubMed
Munita, JM & Arias, CA (2016). Mechanisms of antibiotic resistance. Microbiol Spectr 4(2), 80–87.CrossRefGoogle ScholarPubMed
Nikaido, H (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev: MMBR 67(4), 593–656.CrossRefGoogle ScholarPubMed
O'Brien, S (2015). Meeting the societal need for new antibiotics: The challenges for the pharmaceutical industry. Br J Clin Pharmacol 79(2), 168–172.CrossRefGoogle ScholarPubMed
O'Toole, GA (2011). Microtiter dish biofilm formation assay. J Visualized Exp (47), 10–11. doi: 10.3791/2437.Google ScholarPubMed
Oliveira, R et al. (2001). The role of hydrophobicity in bacterial adhesion. Bioline (October 2016), 11–22. Available at http://repositorium.sdum.uminho.pt/handle/1822/6706.Google Scholar
Pagès, JM & Winterhalter, M (2008). The porin and the permeating antibiotic: A selective diffusion barrier in gram-negative bacteria. Nat Rev Microbiol 6(12), 893–903.CrossRefGoogle ScholarPubMed
Pantanella, F et al. (2008). Biotimer assay, a new method for counting Staphylococcus spp. in biofilm without sample manipulation applied to evaluate antibiotic susceptibility of biofilm. J Microbiol Methods 75(3), 478–484.CrossRefGoogle ScholarPubMed
Park, BJ & Abu-Lail, NI (2009). A correlation between the virulence and the adhesion of Listeria monocytogenes to silicon nitride: An atomic force microscopy study. Colloids Surf B 73(2), 237–243.CrossRefGoogle Scholar
Park, BJ & Abu-Lail, NI (2011 a) The role of the pH conditions of growth on the bioadhesion of individual and lawns of pathogenic Listeria monocytogenes cells. J Colloid Interface Sci 358(2), 611–620.CrossRefGoogle Scholar
Park, BJ & Abu-Lail, NI (2011 b) Variations in the nanomechanical propertis of virulent and avirulent Listeria monocytogenes. Soft Matter 6(16), 3898–3909.CrossRefGoogle Scholar
Park, B-J and Abu-Lail, NI (2011 c). Atomic force microscopy investigations of heterogeneities in the adhesion energies measured between pathogenic and non-pathogenic Listeria species and silicon nitride as they correlate to virulence and adherence. Biofouling 27(5), 543–559.CrossRefGoogle ScholarPubMed
Perry, CC et al. (2009). Atomic force microscopy study of the antimicrobial activity of aqueous garlic versus ampicillin against Escherichia coli and Staphylococcus aureus. J Sci Food Agric 89(6), 958–964.CrossRefGoogle Scholar
Pickering, SAW, Bayston, R & Scammell, BE (2003). Electromagnetic augmentation of antibiotic efficacy in infection of orthopaedic implants. J Bone Joint Surg 85(4), 588–593.CrossRefGoogle ScholarPubMed
Read, AF & Woods, RJ (2014). Antibiotic resistance management. Evol Med Public Health 2014(1), 147–147.CrossRefGoogle ScholarPubMed
Renner, LD & Weibel, DB (2011). Physiochemical regulation of biofilm formation. MRS Bull 36(5), 347–355.CrossRefGoogle Scholar
Rolinson, GN (1980). Effect of lactam antibiotics on bacterial cell growth rate. Microbiology 120(2), 317–323.CrossRefGoogle ScholarPubMed
Rology, VI et al. (1993). MEDICAL quality control of the polymerase chain reaction. 3, 107–114.Google Scholar
Römling, U & Balsalobre, C (2012). Biofilm infections, their resilience to therapy and innovative treatment strategies. J Intern Med 272(6), 541–561.CrossRefGoogle ScholarPubMed
Roosjen, A et al. (2006). Bacterial factors influencing adhesion of Pseudomonas aeruginosa strains to a poly(ethylene oxide) brush. Microbiology 152(9), 2673–2682.CrossRefGoogle ScholarPubMed
Rossolini, GM et al. (2014). Update on the antibiotic resistance crisis. Curr Opin Pharmacol 18, 56–60.CrossRefGoogle ScholarPubMed
Russell, AD (1999). Bacterial resistance to disinfectants: Present knowledge and future problems. J Hosp Infect 43(Suppl. 1), 57–68.CrossRefGoogle ScholarPubMed
Sailer, FC & Young, KD (2003). β-lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol Lett 226(2), 245–249.CrossRefGoogle ScholarPubMed
Satta, G & Canepari, P (1979). Peptidoglycan synthesis in cocci and rods of a morphologically conditional mutant of Klebsiella pneumoniae peptidoglycan synthesis in cocci and rods of a pH- dependent, morphologically conditional mutant of Klebsiella pneumoniae. 137(2), 727–734.Google Scholar
Shah, D et al. (2006). Persisters: A distinct physiological state of E. coli. BMC Microbiol 6, 1–9.CrossRefGoogle ScholarPubMed
Shaikh, S et al. (2015). Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Saudi J Biol Sci 22(1), 90–101.CrossRefGoogle ScholarPubMed
Solomon, SL & Oliver, KB (2014). Antibiotic resistance threats in the United States: Stepping back from the brink. Am Fam Physician 89(12), 938–941.Google ScholarPubMed
Stenstrom, TA (1989). Bacterial hydrophobicity, an overall parameter for the measurement of adhesion potential to soil particles. Microbiology 55(1), 142–147.Google ScholarPubMed
Stepanovic, S et al. (2007). Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Apmis 115(3), 891–899.CrossRefGoogle ScholarPubMed
Stewart, PS (2002). Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292(2), 107–113.CrossRefGoogle ScholarPubMed
Sundari, S & Balasubramanian, D (1991). Are amphiphilic chains. Methods 1065, 35–41.Google ScholarPubMed
Thomson, JM & Bonomo, RA (2005). The threat of antibiotic resistance in gram-negative pathogenic bacteria: Β-lactams in peril!. Curr Opin Microbiol 8(5), 518–524.CrossRefGoogle ScholarPubMed
Touhami, A, Jericho, MH, Boyd, JM & Beveridge, TJ (2006). Nanoscale characterization and determination of adhesion forces of Pseudomonas aeruginosa pili by using atomic force microscopy nanoscale characterization and determination of adhesion forces of Pseudomonas aeruginosa pili by using atomic force microscopy. Am Soc Microbiol. 188(2), 370–377.Google ScholarPubMed
Typas, A et al. (2012). From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10(2), 123–136.CrossRefGoogle Scholar
van Loosdrecht, MC et al. (1987). The role of bacterial cell wall hydrophobicity in adhesion. Appl Environ Microbiol 53(8), 1893–1897.CrossRefGoogle ScholarPubMed
Vashishtha, VM (2010). Growing antibiotics resistance and the need for new antibiotics. Indian Pediatr 47(6), 505–506.CrossRefGoogle ScholarPubMed
Vollmer, W & Seligman, SJ (2010). Architecture of peptidoglycan: More data and more models. Trends Microbiol 18(2), 59–66.CrossRefGoogle ScholarPubMed
Wang, H et al. (2015 a). Role of capsular polysaccharides in biofilm formation: An AFM nanomechanics study. ACS Appl Mater Interfaces 7(23), 13007–13013.CrossRefGoogle ScholarPubMed
Wang, Z et al. (2015 b). Influence of core oligosaccharide of lipopolysaccharide to outer membrane behavior of Escherichia coli. Mar Drugs 13(6), 3325–3339.CrossRefGoogle ScholarPubMed
Welch, K & Strømme, M (2012). A method for quantitative determination of biofilm viability. J Funct Biomater 3(4), 418–431.CrossRefGoogle ScholarPubMed
WHO (2015). Model List of Essential Medicines––Explanatory notes—19th List. (April), p. 55. Available at http://www.who.int/medicines/publications/essentialmedicines/en/.Google Scholar
Wong, AHM, Wenzel, RP & Edmond, MB (2000). Epidemiology of bacteriuria caused by vancomycin-resistant enterococci––A retrospective study. Am J Infect Control 28(4), 277–281.CrossRefGoogle Scholar
Worthington, RJ & Melander, C (2013). Overcoming resistance to β-lactam antibiotics. J Org Chem 78(9), 4207–4213.CrossRefGoogle ScholarPubMed
Wright, CJ et al. (2010). Application of AFM from microbial cell to biofilm. Scanning 32(3), 134–149.CrossRefGoogle Scholar
Yang, L et al. (2006). Atomic force microscopy study of different effects of natural and semisynthetic β-lactam on the cell envelope of Escherichia coli. Anal Chem 78(20), 7341–7345.CrossRefGoogle ScholarPubMed
Yao, X et al. (2016). Combating antimicrobial resistance: Policy recommendations to save lives. Sci Rep. Nature Publishing Group, 22(2), 410–415.Google Scholar
Yoon, MY et al. (2011). Contribution of cell elongation to the biofilm formation of Pseudomonas aeruginosa during anaerobic respiration. PLoS ONE 6(1), 1–11.CrossRefGoogle ScholarPubMed
Young, KD (2006). The selective value of bacterial shape. Microbiol Mol Biol Rev 70(3), 660–703.CrossRefGoogle ScholarPubMed
Zeng, X & Lin, J (2013). Beta-lactamase induction and cell wall metabolism in Gram-negative bacteria. Front Microbiol 4(May), 1–9.CrossRefGoogle ScholarPubMed

Uzoechi and Abu-Lail supplementary material

Uzoechi and Abu-Lail supplementary material 1

File 848 KB

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 14
Total number of PDF views: 77 *
View data table for this chart

* Views captured on Cambridge Core between 14th March 2019 - 4th March 2021. This data will be updated every 24 hours.

7 Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

The Effects of β-Lactam Antibiotics on Surface Modifications of Multidrug-Resistant Escherichia coli: A Multiscale Approach
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

The Effects of β-Lactam Antibiotics on Surface Modifications of Multidrug-Resistant Escherichia coli: A Multiscale Approach
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

The Effects of β-Lactam Antibiotics on Surface Modifications of Multidrug-Resistant Escherichia coli: A Multiscale Approach
Available formats
×
×

Reply to: Submit a response

Your details

Conflicting interests

Do you have any conflicting interests? *