Atomic force microscopy studies of bioprocess engineering surfaces – imaging, interactions and mechanical properties mediating bacterial adhesion

The detrimental effect of bacterial biofilms on process engineering surfaces is well documented. Thus, interest in the early stages of bacterial biofilm formation; in particular bacterial adhesion and the production of anti‐fouling coatings has grown exponentially as a field. During this time, Atomic force microscopy (AFM) has emerged as a critical tool for the evaluation of bacterial adhesion. Due to its versatility AFM offers not only insight into the topographical landscape and mechanical properties of the engineering surfaces, but elucidates, through direct quantification the topographical and biomechnical properties of the foulants The aim of this review is to collate the current research on bacterial adhesion, both theoretical and practical, and outline how AFM as a technique is uniquely equipped to provide further insight into the nanoscale world at the bioprocess engineering surface.

[1]  R. Neihof Dissolved Organic Matter in Seawater and the Electric Charge of Immersed Surfaces ' , 2019 .

[2]  N. Gadegaard,et al.  Influence of biomaterial nanotopography on the adhesive and elastic properties of Staphylococcus aureus cells , 2016 .

[3]  K. Bohinc,et al.  Metal surface characteristics dictate bacterial adhesion capacity , 2016 .

[4]  Stephen M Martin,et al.  Novel zwitterion functionalized carbon nanotube nanocomposite membranes for improved RO performance and surface anti-biofouling resistance , 2016 .

[5]  A. Fane,et al.  The effect of different surface conditioning layers on bacterial adhesion on reverse osmosis membranes , 2016 .

[6]  D. Vanhecke,et al.  Synthesis, characterization, antibacterial activity and cytotoxicity of hollow TiO2-coated CeO2 nanocontainers encapsulating silver nanoparticles for controlled silver release. , 2016, Journal of materials chemistry. B.

[7]  W. Sand,et al.  Proteins dominate in the surface layers formed on materials exposed to extracellular polymeric substances from bacterial cultures , 2016, Biofouling.

[8]  Susanne Hertz,et al.  Statistical Mechanics Of Chain Molecules , 2016 .

[9]  C. Wright,et al.  Atomic Force Microscopy of Biofilms—Imaging, Interactions, and Mechanics , 2016 .

[10]  T. Webster,et al.  The influence of nanostructured features on bacterial adhesion and bone cell functions on severely shot peened 316L stainless steel. , 2015, Biomaterials.

[11]  C. Rodriguez-Emmenegger,et al.  Quantifying bacterial adhesion on antifouling polymer brushes via single-cell force spectroscopy , 2015 .

[12]  Ronn S. Friedlander,et al.  Role of Flagella in Adhesion of Escherichia coli to Abiotic Surfaces. , 2015, Langmuir : the ACS journal of surfaces and colloids.

[13]  Cristina Solano,et al.  Evaluation of Surface Microtopography Engineered by Direct Laser Interference for Bacterial Anti-Biofouling. , 2015, Macromolecular bioscience.

[14]  S. Radford,et al.  Extraction of accurate biomolecular parameters from single-molecule force spectroscopy experiments. , 2015, ACS nano.

[15]  M. Shemesh,et al.  Bioinspired passive anti-biofouling surfaces preventing biofilm formation. , 2015, Journal of materials chemistry. B.

[16]  N. Hilal,et al.  Characterisation and quantification of membrane surface properties using atomic force microscopy: A comprehensive review , 2015 .

[17]  N. Hilal,et al.  A comprehensive review on surface modified polymer membranes for biofouling mitigation , 2015 .

[18]  Flavien Pillet,et al.  Generation of living cell arrays for atomic force microscopy studies , 2014, Nature Protocols.

[19]  A. Beaussart,et al.  Quantifying the forces guiding microbial cell adhesion using single-cell force spectroscopy , 2014, Nature Protocols.

[20]  C. Wright,et al.  A nanoscale characterization of the interaction of a novel alginate oligomer with the cell surface and motility of Pseudomonas aeruginosa. , 2014, American journal of respiratory cell and molecular biology.

[21]  A. Nguyen,et al.  Quantifying adhesion of acidophilic bioleaching bacteria to silica and pyrite by atomic force microscopy with a bacterial probe. , 2014, Colloids and surfaces. B, Biointerfaces.

[22]  Yaolin Liu,et al.  Effects of organic macromolecular conditioning on gypsum scaling of forward osmosis membranes , 2014 .

[23]  S. Setayeshgar,et al.  Physiochemical properties of Caulobacter crescentus holdfast: a localized bacterial adhesive. , 2013, The journal of physical chemistry. B.

[24]  K. Jandt,et al.  Physical vapor deposited titanium thin films for biomedical applications: Reproducibility of nanoscale surface roughness and microbial adhesion properties , 2013 .

[25]  Seoktae Kang,et al.  The role of conditioning film formation in Pseudomonas aeruginosa PAO1 adhesion to inert surfaces in aquatic environments , 2013 .

[26]  A. Beaussart,et al.  Single-cell force spectroscopy of probiotic bacteria. , 2013, Biophysical journal.

[27]  Ajay-Vikram Singh,et al.  Interaction of bacterial cells with cluster-assembled nanostructured titania surfaces: an atomic force microscopy study. , 2013, Journal of nanoscience and nanotechnology.

[28]  Seoktae Kang,et al.  Impact of an extracellular polymeric substance (EPS) precoating on the initial adhesion of Burkholderia cepacia and Pseudomonas aeruginosa , 2012, Biofouling.

[29]  H. Busscher,et al.  Force microscopic and thermodynamic analysis of the adhesion between Pseudomonas aeruginosa and Candida albicans , 2012 .

[30]  Seoktae Kang,et al.  Impact of conditioning films on the initial adhesion of Burkholderia cepacia. , 2012, Colloids and surfaces. B, Biointerfaces.

[31]  N. Hilal,et al.  Atomic force microscopy of nanofiltration membranes: Effect of imaging mode and environment , 2012 .

[32]  C. Gruden,et al.  Determining the influence of active cells and conditioning layer on early stage biofilm formation using cellulose acetate ultrafiltration membranes , 2012 .

[33]  P. Loubière,et al.  Measuring kinetic dissociation/association constants between Lactococcus lactis bacteria and mucins using living cell probes. , 2011, Biophysical journal.

[34]  Feng Wang,et al.  Differential attraction and repulsion of Staphylococcus aureus and Pseudomonas aeruginosa on molecularly smooth titanium films , 2011, Scientific reports.

[35]  Vimal Sharma,et al.  Quantitative Characterization of the Influence of the Nanoscale Morphology of Nanostructured Surfaces on Bacterial Adhesion and Biofilm Formation , 2011, PloS one.

[36]  H. Flemming,et al.  The biofilm matrix , 2010, Nature Reviews Microbiology.

[37]  Georg Papastavrou,et al.  Importance of charge regulation in attractive double-layer forces between dissimilar surfaces. , 2010, Physical review letters.

[38]  Elena P Ivanova,et al.  The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. , 2010, Biomaterials.

[39]  Elena P Ivanova,et al.  Impact of nanoscale roughness of titanium thin film surfaces on bacterial retention. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[40]  Thomas J Webster,et al.  The relationship between the nanostructure of titanium surfaces and bacterial attachment. , 2010, Biomaterials.

[41]  Seoktae Kang,et al.  Bioinspired single bacterial cell force spectroscopy. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[42]  Jingyuan Li,et al.  Single homopolypeptide chains collapse into mechanically rigid conformations , 2009, Proceedings of the National Academy of Sciences.

[43]  J. White,et al.  Progesterone induces nano‐scale molecular modifications on endometrial epithelial cell surfaces , 2009, Biology of the cell.

[44]  E. Ivanova,et al.  Differences in colonisation of five marine bacteria on two types of glass surfaces , 2009, Biofouling.

[45]  Guillaume Andre,et al.  Fishing single molecules on live cells , 2009 .

[46]  M G Walker,et al.  Immobilizing live bacteria for AFM imaging of cellular processes. , 2009, Ultramicroscopy.

[47]  Christophe Vieu,et al.  Nanomechanical properties of dead or alive single-patterned bacteria. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[48]  Elena P. Ivanova,et al.  Effect of ultrafine-grained titanium surfaces on adhesion of bacteria , 2009, Applied Microbiology and Biotechnology.

[49]  P. C. dos Santos Claro,et al.  Submicron trenches reduce the Pseudomonas fluorescens colonization rate on solid surfaces. , 2009, ACS applied materials & interfaces.

[50]  M. Borkovec,et al.  Interactions between solid surfaces with adsorbed polyelectrolytes of opposite charge , 2008 .

[51]  T. Webster,et al.  Influence of nanophase titania topography on bacterial attachment and metabolism , 2008, International journal of nanomedicine.

[52]  E. Ivanova,et al.  Nano-structured surfaces control bacterial attachment , 2008, 2008 International Conference on Nanoscience and Nanotechnology.

[53]  Daniel J. Muller,et al.  Single-cell force spectroscopy , 2008, Journal of Cell Science.

[54]  E. Bergantino,et al.  Conformational Equilibria in Monomeric α-Synuclein at the Single-Molecule Level , 2008, PLoS biology.

[55]  Marco Brucale,et al.  Conformational equilibria in monomeric alpha-synuclein at the single molecule level , 2007, 0712.1973.

[56]  Terri A. Camesano,et al.  Measuring bacterial adhesion at environmental interfaces with single-cell and single-molecule techniques , 2007 .

[57]  C. V. Oss,et al.  Energetics of cell-cell and cell-biopolymer interactions , 1989, Cell Biophysics.

[58]  Yatao Liu,et al.  Microscale correlation between surface chemistry, texture, and the adhesive strength of Staphylococcus epidermidis. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[59]  J. Chorover,et al.  ATR-FTIR spectroscopy reveals bond formation during bacterial adhesion to iron oxide. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[60]  Laurence Mansuy-Huault,et al.  Fatty acids of lipid fractions in extracellular polymeric substances of activated sludge flocs , 2003, Lipids.

[61]  J. Duval,et al.  Analysis of the interfacial properties of fibrillated and nonfibrillated oral streptococcal strains from electrophoretic mobility and titration measurements: evidence for the shortcomings of the 'classical soft-particle approach'. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[62]  Joanna Verran,et al.  Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. , 2005, Colloids and surfaces. B, Biointerfaces.

[63]  H. Busscher,et al.  On a relation between interfacial free energy-dependent and noninterfacial free energy-dependent adherence of oral streptococci to solid substrata , 1988, Current Microbiology.

[64]  H. C. van der Mei,et al.  Comparison of Atomic Force Microscopy Interaction Forces between Bacteria and Silicon Nitride Substrata for Three Commonly Used Immobilization Methods , 2004, Applied and Environmental Microbiology.

[65]  Manfred H. Jericho,et al.  Atomic Force Microscopy of Cell Growth and Division in Staphylococcus aureus , 2004, Journal of bacteriology.

[66]  Dehong Hu,et al.  Correlated atomic force microscopy and fluorescence lifetime imaging of live bacterial cells. , 2004, Colloids and surfaces. B, Biointerfaces.

[67]  Job Ubbink,et al.  Imaging of lactic acid bacteria with AFM--elasticity and adhesion maps and their relationship to biological and structural data. , 2003, Ultramicroscopy.

[68]  M J Doktycz,et al.  AFM imaging of bacteria in liquid media immobilized on gelatin coated mica surfaces. , 2003, Ultramicroscopy.

[69]  Yves F Dufrêne,et al.  Recent progress in the application of atomic force microscopy imaging and force spectroscopy to microbiology. , 2003, Current opinion in microbiology.

[70]  Bernard Nysten,et al.  Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy , 2003 .

[71]  H. Flemming,et al.  Extracellular Polymeric Substances (EPS): Structural, Ecological and Technical Aspects , 2003 .

[72]  R. Schneider,et al.  Conditioning Films in Aquatic Environments , 2003 .

[73]  A. Touhami,et al.  Real‐time imaging of the surface topography of living yeast cells by atomic force microscopy , 2003, Yeast.

[74]  N. Dan The effect of charge regulation on cell adhesion to substrates: salt-induced repulsion , 2003 .

[75]  Rolf Bos,et al.  Electric double layer interactions in bacterial adhesion to surfaces , 2002 .

[76]  T. Camesano,et al.  Elasticity of Pseudomonas putida KT2442 Surface Polymers Probed with Single-Molecule Force Microscopy , 2002 .

[77]  Jost Wingender,et al.  Influence of extracellular polymeric substances on deposition and redeposition of Pseudomonas aeruginosa to surfaces. , 2002, Microbiology.

[78]  Robert D. Boyd,et al.  Use of the atomic force microscope to determine the effect of substratum surface topography on bacterial adhesion , 2002 .

[79]  Manfred H. Jericho,et al.  Atomic force microscopy and theoretical considerations of surface properties and turgor pressures of bacteria , 2002 .

[80]  C. Bowman,et al.  Effects of ultrafiltration membrane surface properties on Pseudomonas aeruginosa biofilm initiation for the purpose of reducing biofouling , 2001 .

[81]  Chris J. Wright,et al.  Atomic Force Microscopy Study of the Adhesion of Saccharomyces cerevisiae. , 2001, Journal of colloid and interface science.

[82]  R. Lovitt,et al.  Atomic force microscope studies of stainless steel: Surface morphology and colloidal particle adhesion , 2001 .

[83]  Y. Lyubchenko,et al.  Comparative studies of bacteria with an atomic force microscopy operating in different modes. , 2001, Ultramicroscopy.

[84]  A. Leis,et al.  Isolation and biochemical characterization of extracellular polymeric substances from Pseudomonas aeruginosa. , 2001, Methods in enzymology.

[85]  G. W. Bailey,et al.  Surface finishes on stainless steel reduce bacterial attachment and early biofilm formation: scanning electron and atomic force microscopy study. , 2000, Poultry science.

[86]  Daniel J. Müller,et al.  Observing single biomolecules at work with the atomic force microscope , 2000, Nature Structural Biology.

[87]  M. Radmacher,et al.  Bacterial turgor pressure can be measured by atomic force microscopy. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[88]  I. Beech,et al.  Chemical and structural characterization of exopolymers produced by Pseudomonas sp. NCIMB 2021 in continuous culture. , 1999, Microbiology.

[89]  Daniel J. Müller,et al.  Atomic force microscopy: A forceful way with single molecules , 1999, Current Biology.

[90]  G. Georgiou,et al.  Molecular determinants of bacterial adhesion monitored by atomic force microscopy. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Nidal Hilal,et al.  Direct measurement of the force of adhesion of a single biological cell using an atomic force microscope , 1998 .

[92]  L. Makowski,et al.  Bacterial adhesion pili are heterologous assemblies of similar subunits. , 1998, Biophysical journal.

[93]  G. Fredrickson The theory of polymer dynamics , 1996 .

[94]  J. Vanderleyden,et al.  Direct evidence for the involvement of extracellular proteins in the adhesion of Azospirillum brasilense. , 1996, Microbiology.

[95]  M. Fletcher,et al.  Pseudomonas fluorescens adhesion and transport through porous media are affected by lipopolysaccharide composition , 1996, Applied and environmental microbiology.

[96]  A. Ikai,et al.  Method for immobilizing microbial cells on gel surface for dynamic AFM studies. , 1995, Biophysical journal.

[97]  A Ikai,et al.  A method for anchoring round shaped cells for atomic force microscope imaging. , 1995, Biophysical journal.

[98]  H. Busscher,et al.  Adhesion of oral streptococci from a flowing suspension to uncoated and albumin-coated surfaces. , 1987, Journal of general microbiology.

[99]  Gerber,et al.  Atomic Force Microscope , 2020, Definitions.

[100]  E. Kellenberger,et al.  Capsule of Escherichia coli K29: ultrastructural preservation and immunoelectron microscopy , 1985, Journal of bacteriology.

[101]  J. Pringle,et al.  The effect of surface free energy and medium surface tension on bacterial attachment to solid surfaces , 1985 .

[102]  P. Rutter,et al.  Physicochemical Interactions of the Substratum, Microorganisms, and the Fluid Phase , 1984 .

[103]  Ralph Mitchell,et al.  Mechanism of the Initial Events in the Sorption of Marine Bacteria to Surfaces , 1970 .

[104]  C. Overberger Book reviews. Encyclopedia of polymer science and technology. Volume 10. Herman F. Murk, Norman G. Gaylord, and Norbert M. Bikales, eds. Wiley (Interscience), New York, 1969 , 1969 .

[105]  E. Verwey,et al.  Theory of the stability of lyophobic colloids. , 1955, The Journal of physical and colloid chemistry.

[106]  B. Derjaguin,et al.  Theory of the stability of strongly charged lyophobic sols and of the adhesion of strongly charged particles in solutions of electrolytes , 1993 .