Adhesion-dependent rupturing of Saccharomyces cerevisiae on biological antimicrobial nanostructured surfaces

Recent studies have shown that some nanostructured surfaces (NSS), many of which are derived from surfaces found on insect cuticles, rupture and kill adhered prokaryotic microbes. Most important, the nanoscale topography is directly responsible for this effect. Although parameters such as cell adhesion and cell wall rigidity have been suggested to play significant roles in this process, there is little experimental evidence regarding the underlying mechanisms involving NSS-induced microbial rupture. In this work, we report the NSS-induced rupturing of a eukaryotic microorganism, Saccharomyces cerevisiae. We show that the amount of NSS-induced rupture of S. cerevisiae is dependent on both the adhesive qualities of the yeast cell and the nanostructure geometry of the NSS. Thus, we are providing the first empirical evidence that these parameters play a direct role in the rupturing of microbes on NSS. Our observations of this phenomenon with S. cerevisiae, particularly the morphological changes, are strikingly similar to that reported for bacteria despite the differences in the yeast cell wall structure. Consequently, NSS provide a novel approach for the control of microbial growth and development of broad-spectrum microbicidal surfaces.

[1]  K. Kwon-Chung,et al.  Aneuploidy and Drug Resistance in Pathogenic Fungi , 2012, PLoS pathogens.

[2]  C. Nombela,et al.  Genome-wide survey of yeast mutations leading to activation of the yeast cell integrity MAPK pathway: Novel insights into diverse MAPK outcomes , 2011, BMC Genomics.

[3]  Elena P Ivanova,et al.  Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. , 2013, Biophysical journal.

[4]  J. Israelachvili.  Intermolecular and surface forces , 1985 .

[5]  Thierry Fontaine,et al.  Screening of Escherichia coli Species Biodiversity Reveals New Biofilm-Associated Antiadhesion Polysaccharides , 2011, mBio.

[6]  M. Kainer,et al.  Fungal infections associated with contaminated methylprednisolone in Tennessee. , 2012, The New England journal of medicine.

[7]  G. Fink,et al.  Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. , 1996, Genetics.

[8]  Olaf Kniemeyer,et al.  Systems Biology of Fungal Infection , 2012, Front. Microbio..

[9]  Hideaki Matsuoka,et al.  Single-cell viability assessment with a novel spectro-imaging system. , 2002, Journal of biotechnology.

[10]  Hospital faces uncertainty as it copes with surge of patients with fungal meningitis. , 2013, JAMA.

[11]  F. Breinig,et al.  Yeast Kre1p is GPI-anchored and involved in both cell wall assembly and architecture. , 2004, Microbiology.

[12]  E. Hoek,et al.  Extended DLVO interactions between spherical particles and rough surfaces. , 2006, Journal of colloid and interface science.

[13]  L. Bergman,et al.  Growth and maintenance of yeast. , 2001, Methods in molecular biology.

[14]  H. Harms,et al.  Analysis of living S. cerevisiae cell states—A three color approach , 2006, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[15]  H. C. van der Mei,et al.  Forces involved in bacterial adhesion to hydrophilic and hydrophobic surfaces. , 2008, Microbiology.

[16]  M. Ghannoum,et al.  Antifungal Agents: Mode of Action, Mechanisms of Resistance, and Correlation of These Mechanisms with Bacterial Resistance , 1999, Clinical Microbiology Reviews.

[17]  D. Law,et al.  Flo11p adhesin required for meiotic differentiation in Saccharomyces cerevisiae minicolonies grown on plastic surfaces. , 2011, FEMS yeast research.

[18]  E. Ivanova,et al.  Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces , 2012, Applied Microbiology and Biotechnology.

[19]  Seoktae Kang,et al.  Effect of surface hydrophobicity on the adhesion of S. cerevisiae onto modified surfaces by poly(styrene-ran-sulfonic acid) random copolymers. , 2005, Colloids and surfaces. B, Biointerfaces.

[20]  C. Pradier,et al.  Grafting of lysozyme and/or poly(ethylene glycol) to prevent biofilm growth on stainless steel surfaces. , 2009, The journal of physical chemistry. B.

[21]  P. Schmitz,et al.  Study of bioadhesion on a flat plate with a yeast/glass model system. , 2004, Journal of colloid and interface science.

[22]  G. Fink,et al.  Bakers' yeast, a model for fungal biofilm formation. , 2001, Science.

[23]  J. Vincent,et al.  Design and mechanical properties of insect cuticle. , 2004, Arthropod structure & development.

[24]  K. Hellingwerf,et al.  Mass spectrometric quantification of the adaptations in the wall proteome of Candida albicans in response to ambient pH. , 2011, Microbiology.

[25]  L. Saraíva,et al.  New insights into cancer‐related proteins provided by the yeast model , 2012, The FEBS journal.

[26]  K. Verstrepen,et al.  Phenotypic diversity of Flo protein family-mediated adhesion in Saccharomyces cerevisiae. , 2009, FEMS yeast research.

[27]  Elena P Ivanova,et al.  Natural bactericidal surfaces: mechanical rupture of Pseudomonas aeruginosa cells by cicada wings. , 2012, Small.

[28]  B. Regenberg,et al.  Saccharomyces cerevisiae--a model to uncover molecular mechanisms for yeast biofilm biology. , 2012, FEMS immunology and medical microbiology.

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

[30]  Saulius Juodkazis,et al.  Bactericidal activity of black silicon , 2013, Nature Communications.

[31]  L. Fojt,et al.  Effects of low-frequency magnetic fields on the viability of yeast Saccharomyces cerevisiae. , 2007, Bioelectrochemistry.

[32]  P. Lipke,et al.  Yeast Cell Adhesion Molecules Have Functional Amyloid-Forming Sequences , 2009, Eukaryotic Cell.

[33]  Malte Hermansson,et al.  The DLVO theory in microbial adhesion , 1999 .

[34]  G. Watson,et al.  Wetting properties on nanostructured surfaces of cicada wings , 2009, Journal of Experimental Biology.

[35]  J. François,et al.  An atomic force microscopy analysis of yeast mutants defective in cell wall architecture , 2010, Yeast.

[36]  T. C. White,et al.  Genetic basis of antifungal drug resistance , 2009, Current fungal infection reports.

[37]  A. Cochis,et al.  Biosurfactants prevent in vitro Candida albicans biofilm formation on resins and silicon materials for prosthetic devices. , 2012, Oral surgery, oral medicine, oral pathology and oral radiology.

[38]  W. Peukert,et al.  Effect of roughness on particle adhesion in aqueous solutions: a study of Saccharomyces cerevisiae and a silica particle. , 2007, Colloids and surfaces. B, Biointerfaces.

[39]  A. Curtis,et al.  DLVO interaction energy between a sphere and a nano-patterned plate , 2008 .

[40]  C. Nombela,et al.  The 'yeast cell wall chip' - a tool to analyse the regulation of cell wall biogenesis in Saccharomyces cerevisiae. , 2005, Microbiology.

[41]  D. LaJeunesse,et al.  Ultrastructural analysis of wild type and mutant Drosophila melanogaster using helium ion microscopy. , 2013, Micron.

[42]  Ronald W. Davis,et al.  Systematic screen for human disease genes in yeast , 2002, Nature Genetics.