The influence of microgravity on invasive growth in Saccharomyces cerevisiae.

This study investigates the effects of microgravity on colony growth and the morphological transition from single cells to short invasive filaments in the model eukaryotic organism Saccharomyces cerevisiae. Two-dimensional spreading of the yeast colonies grown on semi-solid agar medium was reduced under microgravity in the Σ1278b laboratory strain but not in the CMBSESA1 industrial strain. This was supported by the Σ1278b proteome map under microgravity conditions, which revealed upregulation of proteins linked to anaerobic conditions. The Σ1278b strain showed a reduced invasive growth in the center of the yeast colony. Bud scar distribution was slightly affected, with a switch toward more random budding. Together, microgravity conditions disturb spatially programmed budding patterns and generate strain-dependent growth differences in yeast colonies on semi-solid medium.

[1]  G. Fink,et al.  Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. , 1994, Genes & development.

[2]  J. Chant,et al.  Analysis of budding patterns. , 2002, Methods in enzymology.

[3]  E S Lander,et al.  Ploidy regulation of gene expression. , 1999, Science.

[4]  Sara D. Altenburg,et al.  Yeast genomic expression patterns in response to low-shear modeled microgravity , 2007, BMC Genomics.

[5]  D. Pierson,et al.  Microbial Responses to Microgravity and Other Low-Shear Environments , 2004, Microbiology and Molecular Biology Reviews.

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

[7]  Hong-zhi Liu,et al.  Effects of spaceflight on polysaccharides of Saccharomyces cerevisiae cell wall , 2008, Applied Microbiology and Biotechnology.

[8]  C Graf,et al.  Saccharomyces cerevisiae fungemia in an immunocompromised patient not treated with Saccharomyces boulardii preparation. , 2007, The Journal of infection.

[9]  C. Mark Ott,et al.  Microgravity as a Novel Environmental Signal Affecting Salmonella enterica Serovar Typhimurium Virulence , 2000, Infection and Immunity.

[10]  K. Verstrepen,et al.  Flocculation, adhesion and biofilm formation in yeasts , 2006, Molecular microbiology.

[11]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[12]  Gerald Sonnenfeld,et al.  The immune system in space and microgravity. , 2002, Medicine and science in sports and exercise.

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

[14]  L. Stodieck,et al.  Haploid deletion strains of Saccharomyces cerevisiae that determine survival during space flight , 2007 .

[15]  J. Mccusker,et al.  Development of Saccharomyces Cerevisiae as a Model Pathogen: a System for the Genetic Identification of Gene Products Required for Survival in the Mammalian Host Environment Tion and Therefore Simultaneously Exposed to the Same , 2001 .

[16]  D M Klaus,et al.  Microgravity and its implication for fermentation biotechnology. , 1998, Trends in biotechnology.

[17]  A Cogoli,et al.  Cultivation of Saccharomyces cerevisiae in a bioreactor in microgravity. , 1996, Journal of biotechnology.

[18]  P J Cullen,et al.  Glucose depletion causes haploid invasive growth in yeast. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Gershwin,et al.  Microgravity and immune responsiveness: implications for space travel. , 2002, Nutrition.

[20]  G Sonnenfeld,et al.  Changes in the immune system during and after spaceflight. , 1997, Advances in space biology and medicine.

[21]  S. Potier,et al.  Two-dimensional protein map of an "ale"-brewing yeast strain: proteome dynamics during fermentation. , 2004, FEMS yeast research.

[22]  R. Kuroki,et al.  Region of Flo1 Proteins Responsible for Sugar Recognition , 1998, Journal of bacteriology.

[23]  G Sonnenfeld,et al.  Space flight, microgravity, stress, and immune responses. , 1999, Advances in space research : the official journal of the Committee on Space Research.

[24]  Ronald W. Davis,et al.  Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. , 1994, Genetics.

[25]  P. Lipke,et al.  A Biochemical Guide to Yeast Adhesins: Glycoproteins for Social and Antisocial Occasions , 2007, Microbiology and Molecular Biology Reviews.

[26]  J. W. Wilson,et al.  Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq , 2007, Proceedings of the National Academy of Sciences.

[27]  M. Kacena,et al.  Effects of space flight and mixing on bacterial growth in low volume cultures. , 1999, Microgravity science and technology.

[28]  Marcelo D. Vinces,et al.  Contributions of hyphae and hypha‐co‐regulated genes to Candida albicans virulence , 2005, Cellular microbiology.

[29]  I. S. Pretorius,et al.  Characteristics of Flo11-dependent flocculation in Saccharomyces cerevisiae. , 2005, FEMS yeast research.

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

[31]  E G Yukihara,et al.  Radiation dosimetry for microbial experiments in the International Space Station using different etched track and luminescent detectors. , 2006, Radiation protection dosimetry.

[32]  G. Fink,et al.  Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. , 1994, Molecular biology of the cell.

[33]  O. Jejelowo,et al.  Spaceflight and modeled microgravity effects on microbial growth and virulence , 2009, Applied Microbiology and Biotechnology.

[34]  G. Fink,et al.  A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. Lo,et al.  FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin , 1996, Journal of bacteriology.

[36]  A. Jansen,et al.  Mat Formation in Saccharomyces cerevisiae Requires Nutrient and pH Gradients , 2007, Eukaryotic Cell.

[37]  G. Fink,et al.  The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Ghigo,et al.  Escherichia coli biofilms. , 2008, Current topics in microbiology and immunology.

[39]  Natalie Leys,et al.  The response of Cupriavidus metallidurans CH34 to spaceflight in the international space station , 2009, Antonie van Leeuwenhoek.

[40]  I. S. Pretorius,et al.  Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[41]  D. Engelberg,et al.  The Yeast Ras/Cyclic AMP Pathway Induces Invasive Growth by Suppressing the Cellular Stress Response , 1999, Molecular and Cellular Biology.

[42]  Zdena Palková,et al.  Life within a community: benefit to yeast long-term survival. , 2006, FEMS microbiology reviews.

[43]  A. Mitchell,et al.  How to build a biofilm: a fungal perspective. , 2006, Current opinion in microbiology.

[44]  Stefan Brückner,et al.  Amino acid starvation and Gcn4p regulate adhesive growth and FLO11 gene expression in Saccharomyces cerevisiae. , 2003, Molecular biology of the cell.

[45]  A. Dranginis,et al.  Expression and Characterization of the Flocculin Flo11/Muc1, a Saccharomyces cerevisiae Mannoprotein with Homotypic Properties of Adhesion , 2007, Eukaryotic Cell.

[46]  S. Evans Coping with Candida infections. , 2010, Proceedings of the American Thoracic Society.

[47]  J. Pringle Staining of bud scars and other cell wall chitin with calcofluor. , 1991, Methods in enzymology.

[48]  D. Klaus,et al.  Microgravity, bacteria, and the influence of motility , 2007 .

[49]  A. Teunissen,et al.  The dominant flocculation genes of Saccharomyces cerevisiae constitute a new subtelomeric gene family , 1995, Yeast.

[50]  R. Korona,et al.  Mutational Load and the Transition between Diploidy and Haploidy in Experimental Populations of the Yeast Saccharomyces cerevisiae , 2004, Genetica.

[51]  D. Pierson,et al.  Low-Shear Modeled Microgravity Alters the Salmonella enterica Serovar Typhimurium Stress Response in an RpoS-Independent Manner , 2002, Applied and Environmental Microbiology.

[52]  Gordon Ramage,et al.  Candida biofilms on implanted biomaterials: a clinically significant problem. , 2006, FEMS yeast research.

[53]  John B. West,et al.  Historical Perspectives: Physiology in microgravity , 2000 .

[54]  Sara D. Altenburg,et al.  Increased Filamentous Growth of Candida albicans in Simulated Microgravity , 2008, Genom. Proteom. Bioinform..

[55]  Joshua A. Granek,et al.  Environmental and Genetic Determinants of Colony Morphology in Yeast , 2010, PLoS genetics.

[56]  D. Klaus,et al.  Can genetically modified Escherichia coli with neutral buoyancy induced by gas vesicles be used as an alternative method to clinorotation for microgravity studies? , 2005, Microbiology.

[57]  L. Hyman,et al.  Effects of Low-Shear Modeled Microgravity on Cell Function, Gene Expression, and Phenotype in Saccharomyces cerevisiae , 2006, Applied and Environmental Microbiology.

[58]  Filip Vanhavere,et al.  DOsimetry of BIological EXperiments in SPace (DOBIES) with luminescence (OSL and TL) and track etch detectors , 2008 .

[59]  S. Pirt,et al.  A kinetic study of the mode of growth of surface colonies of bacteria and fungi. , 1967, Journal of general microbiology.

[60]  D. Klaus,et al.  Space Microbiology , 2010, Microbiology and Molecular Biology Reviews.

[61]  A. Demain,et al.  Shear stress enhances microcin B17 production in a rotating wall bioreactor, but ethanol stress does not , 2001, Applied Microbiology and Biotechnology.

[62]  Bernhard Hube,et al.  From commensal to pathogen: stage- and tissue-specific gene expression of Candida albicans. , 2004, Current opinion in microbiology.

[63]  R. W. Davis,et al.  Saccharomyces cerevisiae virulence phenotype as determined with CD-1 mice is associated with the ability to grow at 42 degrees C and form pseudohyphae , 1994, Infection and immunity.

[64]  P. Todd,et al.  Growth characteristics of E. coli and B. subtilis cultured on an agar substrate in microgravity , 1997 .

[65]  Carla Goulart,et al.  Novel Sfp1 transcriptional regulation of Saccharomyces cerevisiae gene expression changes during spaceflight. , 2008, Astrobiology.

[66]  R. Darouiche,et al.  Candida Infections of Medical Devices , 2004, Clinical Microbiology Reviews.

[67]  D. Klaus Space Microbiology: Microgravity and Microorganisms , 2003 .

[68]  K. Foster,et al.  FLO1 Is a Variable Green Beard Gene that Drives Biofilm-like Cooperation in Budding Yeast , 2008, Cell.

[69]  A. Deelder,et al.  Proteome analysis of aerobically and anaerobically grown Saccharomyces cerevisiae cells. , 2009, Journal of proteomics.

[70]  P. Ayyaswamy,et al.  Escherichia coli Biofilms Formed under Low-Shear Modeled Microgravity in a Ground-Based System , 2006, Applied and Environmental Microbiology.

[71]  G. Braus,et al.  Differential Flo8p-dependent regulation of FLO1 and FLO11 for cell–cell and cell–substrate adherence of S. cerevisiae S288c , 2007, Molecular microbiology.

[72]  P. Barré,et al.  Localization and cell surface anchoring of the Saccharomyces cerevisiae flocculation protein Flo1p , 1997, Journal of bacteriology.