Cell Wall-Related Bionumbers and Bioestimates of Saccharomyces cerevisiae and Candida albicans

ABSTRACT Bionumbers and bioestimates are valuable tools in biological research. Here we focus on cell wall-related bionumbers and bioestimates of the budding yeast Saccharomyces cerevisiae and the polymorphic, pathogenic fungus Candida albicans. We discuss the linear relationship between cell size and cell ploidy, the correlation between cell size and specific growth rate, the effect of turgor pressure on cell size, and the reason why using fixed cells for measuring cellular dimensions can result in serious underestimation of in vivo values. We further consider the evidence that individual buds and hyphae grow linearly and that exponential growth of the population results from regular formation of new daughter cells and regular hyphal branching. Our calculations show that hyphal growth allows C. albicans to cover much larger distances per unit of time than the yeast mode of growth and that this is accompanied by strongly increased surface expansion rates. We therefore predict that the transcript levels of genes involved in wall formation increase during hyphal growth. Interestingly, wall proteins and polysaccharides seem barely, if at all, subject to turnover and replacement. A general lesson is how strongly most bionumbers and bioestimates depend on environmental conditions and genetic background, thus reemphasizing the importance of well-defined and carefully chosen culture conditions and experimental approaches. Finally, we propose that the numbers and estimates described here offer a solid starting point for similar studies of other cell compartments and other yeast species.

[1]  S. Oliver,et al.  Genome-wide analysis of yeast stress survival and tolerance acquisition to analyze the central trade-off between growth rate and cellular robustness , 2011, Molecular biology of the cell.

[2]  G. Gooday The dynamics of hyphal growth , 1995 .

[3]  C. D. de Koster,et al.  Iron restriction-induced adaptations in the wall proteome of Candida albicans. , 2013, Microbiology.

[4]  J. Mitchison,et al.  The growth of single cells. I. Schizosaccharomyces pombe. , 1957, Experimental cell research.

[5]  Andre Boorsma,et al.  Cell wall construction in Saccharomyces cerevisiae , 2006, Yeast.

[6]  N. Gow,et al.  Vacuolation, branch production and linear growth of germ tubes in Candida albicans. , 1982, Journal of general microbiology.

[7]  F. Odds,et al.  Development of Candida albicans hyphae in different growth media--variations in growth rates, cell dimensions and timing of morphogenetic events. , 1986, Journal of general microbiology.

[8]  C. Boone,et al.  Yeast KRE genes provide evidence for a pathway of cell wall beta-glucan assembly , 1990, The Journal of cell biology.

[9]  C. Munro,et al.  The Cell Wall: Glycoproteins, Remodeling, and Regulation , 2012 .

[10]  Xiaomin Zhao,et al.  Heterogeneous distribution of Candida albicans cell-surface antigens demonstrated with an Als1-specific monoclonal antibody , 2010, Microbiology.

[11]  P. Lord,et al.  Dependency of size of Saccharomyces cerevisiae cells on growth rate , 1979, Journal of bacteriology.

[12]  C. D. de Koster,et al.  Mass spectrometric quantitation of covalently bound cell wall proteins in Saccharomyces cerevisiae , 2007, FEMS yeast research.

[13]  G C Johnston,et al.  Regulation of cell size in the yeast Saccharomyces cerevisiae , 1979, Journal of bacteriology.

[14]  N. Chauhan,et al.  Adhesins in Human Fungal Pathogens: Glue with Plenty of Stick , 2013, Eukaryotic Cell.

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

[16]  P. Biely,et al.  Wall mannan of Saccharomyces cerevisiae. Metabolic stability and release into growth medium. , 1975, Biochimica et biophysica acta.

[17]  Griffin M. Weber,et al.  BioNumbers—the database of key numbers in molecular and cell biology , 2009, Nucleic Acids Res..

[18]  W. L. Chaffin The relationship between yeast cell size and cell division in Candida albicans. , 1984, Canadian journal of microbiology.

[19]  C. D. de Koster,et al.  Hyphal induction in the human fungal pathogen Candida albicans reveals a characteristic wall protein profile. , 2011, Microbiology.

[20]  H. Erickson Size and Shape of Protein Molecules at the Nanometer Level Determined by Sedimentation, Gel Filtration, and Electron Microscopy , 2009, Biological Procedures Online.

[21]  Samara L. Reck-Peterson,et al.  Role of actin and Myo2p in polarized secretion and growth of Saccharomyces cerevisiae. , 2000, Molecular biology of the cell.

[22]  Chaffin Wl The relationship between yeast cell size and cell division in Candida albicans , 1984 .

[23]  F. Klis,et al.  Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. , 2009, FEMS yeast research.

[24]  K. Sigler,et al.  Yeasts and Yeast-Like Organisms , 1990 .

[25]  J. Adams,et al.  Population studies in microorganisms. I. Evolution of diploidy in Saccharomyces cerevisiae. , 1974, Genetics.

[26]  F. Klis,et al.  An assay of relative cell wall porosity in Saccharomyces cerevisiae, Kluyveromyces lactis and Schizosaccharomyces pombe , 1990, Yeast.

[27]  P. Gerhardt,et al.  Porosity of the Yeast Cell Wall and Membrane , 1974, Journal of bacteriology.

[28]  M. Sipiczki,et al.  Characterization of Ccw12p, a major key player in cell wall stability of Saccharomyces cerevisiae , 2007, Yeast.

[29]  P. Gervais,et al.  Passive response of Saccharomyces cerevisiae to osmotic shifts: cell volume variations depending on the physiological state. , 1996, Biochemical and biophysical research communications.

[30]  Yves F Dufrêne,et al.  Measuring cell wall thickness in living yeast cells using single molecular rulers. , 2010, ACS nano.

[31]  J. Broach Nutritional Control of Growth and Development in Yeast , 2012, Genetics.

[32]  C. D. de Koster,et al.  Of Novel Adhesin-like Wall Proteins : Differential Incorporation Candida Glabrata Supplemental Material , 2008 .

[33]  A. H. Rose,et al.  Effect of growth rate and substrate limitation on the composition and structure of the cell wall of Saccharomyces cerevisiae. , 1967, The Biochemical journal.

[34]  K. J. Clarke,et al.  Effect of osmotic stress on the ultrastructure and viability of the yeast Saccharomyces cerevisiae. , 1986, Journal of general microbiology.

[35]  L. Hartwell,et al.  Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division , 1977, The Journal of cell biology.

[36]  W N Arnold,et al.  Permeability of the Cell Envelope and Osmotic Behavior in Saccharomyces cerevisiae , 1977, Journal of bacteriology.

[37]  Thierry Fontaine,et al.  Glycosylphosphatidylinositol-anchored Glucanosyltransferases Play an Active Role in the Biosynthesis of the Fungal Cell Wall* , 2000, The Journal of Biological Chemistry.

[38]  E. O’Shea,et al.  Global analysis of protein expression in yeast , 2003, Nature.

[39]  F. Klis,et al.  News from the Fungal Front: Wall Proteome Dynamics and Host–Pathogen Interplay , 2012, PLoS pathogens.

[40]  J. Michalski,et al.  β-1,2 Oligomannose Adhesin Epitopes Are Widely Distributed over the Different Families of Candida albicans Cell Wall Mannoproteins and Are Associated through both N- and O-Glycosylation Processes , 2008, Infection and Immunity.

[41]  N. Gow,et al.  A model of the hyphal septum ofCandida albicans , 1983 .

[42]  N. Gow,et al.  Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen , 2012, Cellular microbiology.

[43]  Stanley Brul,et al.  Role of cell cycle-regulated expression in the localized incorporation of cell wall proteins in yeast. , 2006, Molecular biology of the cell.

[44]  K. Takeo,et al.  Three-dimensional reconstruction of a pathogenic yeast Exophiala dermatitidis cell by freeze-substitution and serial sectioning electron microscopy. , 2003, FEMS microbiology letters.

[45]  D. Soll,et al.  A comparison of volume growth during bud and mycelium formation in Candida albicans: a single cell analysis. , 1984, Journal of general microbiology.

[46]  Richard G. W. Anderson,et al.  Lipid rafts: at a crossroad between cell biology and physics , 2007, Nature Cell Biology.

[47]  M. Mann,et al.  Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast , 2008, Nature.

[48]  J. François A simple method for quantitative determination of polysaccharides in fungal cell walls , 2006, Nature Protocols.

[49]  A. Cassone,et al.  Ultrastructural changes in the wall during germ-tube formation from blastospores of Candida albicans. , 1973, Journal of general microbiology.

[50]  Gerald R. Fink,et al.  Transcriptional Response of Candida albicans upon Internalization by Macrophages , 2004, Eukaryotic Cell.

[51]  P. Robbins,et al.  A glucanase-driven fractionation allows redefinition of Schizosaccharomyces pombe cell wall composition and structure: assignment of diglucan. , 2005, Analytical biochemistry.

[52]  R. Mortimer Radiobiological and genetic studies on a polyploid series (haploid to hexaploid) of Saccharomyces cerevisiae. , 1958, Radiation research.

[53]  H. Hamamcı,et al.  Continuous cultivation of bakers' yeast: Change in cell composition at different dilution rates and effect of heat stress on trehalose level , 2008, Folia Microbiologica.

[54]  Alistair J. P. Brown,et al.  The PKC, HOG and Ca2+ signalling pathways co‐ordinately regulate chitin synthesis in Candida albicans , 2007, Molecular microbiology.

[55]  C. Bracker,et al.  Pulsed growth of fungal hyphal tips. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[56]  J. Berman,et al.  The distinct morphogenic states of Candida albicans. , 2004, Trends in microbiology.

[57]  J. Tkacz,et al.  Wall replication in saccharomyces species: use of fluorescein-conjugated concanavalin A to reveal the site of mannan insertion. , 1972, Journal of general microbiology.

[58]  J. Michalski,et al.  Adhesin Epitopes Are Widely Distributed over the Different Families of Candida albicans Cell Wall Mannoproteins and Are Associated through both Nand O-Glycosylation Processes , 2008 .

[59]  C. D. de Koster,et al.  Mass spectrometric identification of covalently bound cell wall proteins from the fission yeast Schizosaccharomyces pombe , 2007, Yeast.

[60]  F. Klis,et al.  Covalently linked wall proteins in ascomycetous fungi , 2009, Yeast.

[61]  Richard J. Bennett,et al.  The ‘obligate diploid’ Candida albicans forms mating-competent haploids , 2013, Nature.

[62]  C. D. de Koster,et al.  Beyond the wall: Candida albicans secret(e)s to survive. , 2013, FEMS microbiology letters.

[63]  C. D. de Koster,et al.  Surface stress induces a conserved cell wall stress response in the patho- genic fungus Candida albicans , 2013 .

[64]  Rob Phillips,et al.  A feeling for the numbers in biology , 2009, Proceedings of the National Academy of Sciences.

[65]  D. E. Levin,et al.  Regulation of Cell Wall Biogenesis in Saccharomyces cerevisiae: The Cell Wall Integrity Signaling Pathway , 2011, Genetics.

[66]  Enrico Cabib,et al.  How carbohydrates sculpt cells: chemical control of morphogenesis in the yeast cell wall , 2013, Nature Reviews Microbiology.

[67]  K. Takeo,et al.  Quantitative three-dimensional structural analysis of Exophiala dermatitidis yeast cells by freeze-substitution and serial ultrathin sectioning. , 2003, Journal of electron microscopy.

[68]  B. Daignan-Fornier,et al.  A pharmaco‐epistasis strategy reveals a new cell size controlling pathway in yeast , 2022 .

[69]  W. Chaffin,et al.  Candida albicans Cell Wall Proteins , 2008, Microbiology and Molecular Biology Reviews.

[70]  Edda Klipp,et al.  Biophysical properties of Saccharomyces cerevisiae and their relationship with HOG pathway activation , 2010, European Biophysics Journal.

[71]  K. Hellingwerf,et al.  Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. , 2008, Microbiology.

[72]  J. Mitchison The growth of single cells. II. Saccharomyces cerevisiae. , 1958, Experimental cell research.

[73]  A. Verkleij,et al.  The cell wall architecture of Candida albicans wild‐type cells and cell wall‐defective mutants , 2000, Molecular microbiology.

[74]  C. D. de Koster,et al.  A systematic study of the cell wall composition of Kluyveromyces lactis , 2010, Yeast.

[75]  H. E. Kubitschek,et al.  Buoyant density variation during the cell cycle of Saccharomyces cerevisiae , 1984, Journal of bacteriology.

[76]  D. Soll,et al.  Growth and the inducibility of mycelium formation in Candida albicans: a single-cell analysis using a perfusion chamber. , 1983, Journal of general microbiology.

[77]  F. Klis,et al.  The glucanase‐soluble mannoproteins limit cell wall porosity in Saccharomyces cerevisiae , 1990, Yeast.

[78]  C. D. de Koster,et al.  Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans , 2012, Proteomics.

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

[80]  M. Prevost,et al.  The GPI-modified proteins Pga59 and Pga62 of Candida albicans are required for cell wall integrity. , 2009, Microbiology.

[81]  J. Cope The porosity of the cell wall of Candida albicans. , 1980, Journal of general microbiology.

[82]  K. Parker,et al.  Multiplexed Protein Quantitation in Saccharomyces cerevisiae Using Amine-reactive Isobaric Tagging Reagents*S , 2004, Molecular & Cellular Proteomics.

[83]  E. Herrero,et al.  Metabolism of Saccharomyces cerevisiae envelope mannoproteins , 1982, Archives of Microbiology.

[84]  Mike Tyers,et al.  Systematic Identification of Pathways That Couple Cell Growth and Division in Yeast , 2002, Science.

[85]  A. Beaussart,et al.  Atomic Force Microscopy: A New Look at Pathogens , 2013, PLoS pathogens.

[86]  N. Gow,et al.  Growth kinetics and morphology of colonies of the filamentous form of Candida albicans. , 1982, Journal of general microbiology.

[87]  A. Casadevall,et al.  Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans‐cell wall transfer of proteins and lipids in ascomycetes , 2008, Cellular microbiology.

[88]  F. Klis,et al.  Increased Cell Wall Porosity in Saccharomyces cerevisiae after Treatment with Dithiothreitol or EDTA , 1989 .

[89]  C. Powell,et al.  Chitin scar breaks in aged Saccharomyces cerevisiae. , 2003, Microbiology.

[90]  D. Manners,et al.  Isolation and composition of an alkali-soluble glucan from the cell walls of Saccharomyces cerevisiae. , 1976, Journal of general microbiology.

[91]  C. D. de Koster,et al.  The effects of fluconazole on the secretome, the wall proteome and wall integrity of the clinical fungus Candida albicans , 2013 .

[92]  P. Orlean Architecture and Biosynthesis of the Saccharomyces cerevisiae Cell Wall , 2012, Genetics.