The influence of microgravity on invasive growth in saccharomyces cerevisiae

Astrobiology

Volumn 11, Issue 1, 2011, Pages 45-55

  Van Mulders, Sebastiaan E ^a   Stassen, Catherine ^b   Daenen, Luk ^a   Devreese, Bart ^b   Siewers, Verena ^c   Van Eijsden, Rudy G E ^d   Nielsen, Jens ^c   Delvaux, Freddy R ^a   Willaert, Ronnie ^e  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Adhesion; Budding; Invasive growth; Microgravity; Proteomics; Saccharomyces cerevisiae

Indexed keywords

SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BACTERIAL COUNT; CLASSIFICATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SPACE FLIGHT; TEMPERATURE; TIME; TWO DIMENSIONAL GEL ELECTROPHORESIS; WEIGHTLESSNESS;

COLONY COUNT, MICROBIAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPACE FLIGHT; TEMPERATURE; TIME FACTORS; WEIGHTLESSNESS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 79952023959     PISSN: 15311074     EISSN: None     Source Type: Journal    
DOI: 10.1089/ast.2010.0518     Document Type: Article

References (72)

1. Abramoff, M.D., Magelhaes, P.J., and Ram, S.J. (2004) Image processing with Image J. Biophotonics International 11:36-42.
2. Altenburg, S.D., Nielsen-Preiss, S.M., and Hyman, L.E. (2008) Increased filamentous growth of Candida albicans in simulated microgravity. Genomics Proteomics Bioinformatics 6:42-50. (Pubitemid 351847760)
3. Bayly, J.C., Douglas, L.M., Pretorius, I.S., Bauer, F.F., and Dranginis, A.M. (2005) Characteristics of Flo11-dependent flocculation in Saccharomyces cerevisiae. FEMS YeastRes 5:1151-1156. (Pubitemid 41607735)
4. Benoit, M.R. and Klaus, D.M. (2005) Can genetically modified Escherichia coli with neutral buoyancy induced by gas vesicles be used as an alternative method to clinorotation for micro-gravity studies? Microbiology 151:69-74.
5. Benoit, M.R. and Klaus, D.M. (2007) Microgravity, bacteria, and the influence of motility. Adv Space Res 39:1225-1232. (Pubitemid 46829487)
6. Blankenship, J.R and Mitchell, A.P. (2006) How to build a bio-film: a fungal perspective. Curr Opin Microbiol 9:588-594. (Pubitemid 44791986)
7. Bony, M., Thines-Sempoux, D., Barre, P., and Blondin, B. (1997) Localization and cell surface anchoring of the Sacchar-omyces cerevisiae flocculation protein Flo1p. J Bacteriol 179: 4929-4936. (Pubitemid 27339742)
8. Borchers, A.T., Keen, C.L., and Gershwin, M.E. (2002) Micro-gravity and immune responsiveness: implications for space travel. Nutrition 18:889-898. (Pubitemid 35299419)
9. Braus, G.H., Grundmann, O., Brückner, S., and Mösch, H.-U. (2003) Amino acid starvation and Gcn4p regulate adhesive growth and FLO11 gene expression in Saccharomyces cerevisiae. Mol Biol Cell 14:4272-4284. (Pubitemid 37186327)
10. Bruckmann, A., Hensbergen, P.J., Balog, C.I.A., Deelder, A.M., Brandt, R, Snoek, I.S.I., Steensma, H.Y., and van Heusden, G.P.H. (2009) Proteome analysis of aerobically and anaerobi-cally grown Saccharomyces cerevisiae cells. J Proteomics 71:662-669.
11. Coleman, C.B., Allen, P.L., Rupert, M., Goulart, C., Hoehn, A., Stodieck, L.S., and Hammond, T.G (2008) Novel Sfp1 tran-scriptional regulation of Saccharomyces cerevisiae gene expres-sion changes during spaceflight. Astrobiology 8:1071-1078.
12. Cullen, P.J. and Sprague, GF. (2000) Glucose depletion causes haploid invasive growth in yeast. Proc Natl Acad Sci USA 97:13619-13624.
13. Douglas, L.M., Li, L., Yang, Y., and Dranginis, A.M. (2007) Ex-pression and characterization of the flocculin Flo11/Muc1, a Saccharomyces cerevisiae mannoprotein with homotypic prop-erties of adhesion. Eukaryot Cell 6:2214-2221.
14. Dranginis, A.M., Rauceo, J.M., Coronado, J.E., and Lipke, P.N. (2007) A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev 71:282-294. (Pubitemid 46954307)
15. Evans, S.E. (2010) Coping with Candida infections. Proc Am Thorac Soc 7:197-203.
16. Fichtner, L., Schulze, F., and Braus, GH. (2007) Differential Flo8p-dependent regulation of FLO1 and FLO11 for cell-cell and cell-substrate adherence of S. cerevisiae. Mol Microbiol 66:1276-1289. (Pubitemid 350115034)
17. Galitski, T., Saldanha, A.J., Styles, C.A., Lander, E.S., and Fink, GR. (1999) Ploidy regulation of gene expression. Science 285:251-254. (Pubitemid 29329997)
18. Gao, Q., Fang, A., Pierson, D.L., Mishra, S.K., and Demain, A.L. (2001) Shear stress enhances microcin B17 production in a rotating wall bioreactor, but ethanol stress does not. Appl Microbiol Biotechnol 56:384-387 (Pubitemid 32763349)
19. Goldstein, A.L. and McCusker, J.H. (2001) 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. Genetics 159:499-513. (Pubitemid 33035095)
20. Goossens, O., Vanhavere, F., Leys, N., De Boever, P., O'Sullivan, D., Zhou, D., Spurny, F., Yukihara, E.G, Gaza, R, and McKeever, S.W.S. (2006) Radiation dosimetry for microbial experiments in the International Space Station using different etched track and luminescent detectors. Radiat Prot Dosimetry 120:433-437. (Pubitemid 44565970)
21. Graf, C and Gavazzi, G (2007) Saccharomyces cerevisiae fungemia in an immunocompromised patient not treated with Sacchar-omyces boulardii preparation. J Infect 54:310-311. (Pubitemid 46238162)
22. Granek, J.A. and Magwene, P.M. (2010) Environmental and genetic determinants of colony morphology in yeast. PLoS Genet 6:e1000823.
23. Gullo, A. (2009) Invasive fungal infections: the challenge con-tinues. Drugs 69:65-73.
24. Guo, B., Styles, C.A., Feng, Q., and Fink, G.R. (2000) A Saccharomyces cerevisiae gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci USA 97:12158-12163.
25. Horneck, G., Klaus, D.M., and Mancinelli, R.L. (2010) Space microbiology. Microbiol Mol Biol Rev 74:121-156.
26. Hube, B. (2004) From commensal to pathogen: stage-and tissuespecific gene expression of Candida albicans. Curr Opin Microbiol 7:336-341. (Pubitemid 39091116)
27. Johanson, K., Allen, P.L., Gonzalez-Villalobos, R.A., Nesbit, J., Nickerson, C.A., Höner zu Bentrup, K., Wilson, J.W., Ramamurthy, R., D'Elia, R, Muse, K.E., Hammond, J., Freeman, J., Stodieck, L.S., and Hammond, T.G. (2007) Haploid deletion strains of Saccharomyces cerevisiae that determine survival during space flight. Acta Astronaut 60:460-471. (Pubitemid 46176073)
28. Kacena, M. and Todd, P. (1997) Growth characteristics of E. coli and B. subtilis cultured on an agar substrate in microgravity. Microgravity Sci Technol 10:58-62. (Pubitemid 127661234)
29. Kacena, M.A., Manfredi, B., and Todd, P. (1999) Effects of space flight and mixing on bacterial growth in low volume cultures. Microgravity Sci Technol 12:74-77. (Pubitemid 129304180)
30. Klaus, D.M. (1998) Microgravity and its implications for fermentation biotechnology. Trends Biotechnol 16:369-373. (Pubitemid 28410424)
31. Klaus, D.M. (2002) Space microbiology: microgravity and microorganisms. In Encyclopedia of Environmental Microbiology, edited by G. Britton, John Wiley & Sons, New York, pp 22996-23004.
32. Klis, F.M., Sosinska, G.J., de Groot, P.W.J., and Brul, S. (2009) Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEMS Yeast Res 9:1013-1028.
33. Kobayashi, O., Hayashi, N., Kuroki, R, and Sone, H. (1998) Region of Flo1 proteins responsible for sugar recognition. J Bacteriol 180:6503-6510.
34. Kobi, D., Zugmeyer, S., Potier, S., and Jaquet-Gutfreund, L. (2004) Two-dimensional protein map of an "ale"-brewing yeast strain: proteome dynamics during fermentation. FEMS Yeast Res 5:210-230.
35. Kojic, E.M. and Darouiche, R.O. (2004) Candida infections of medical devices. Clin Microbiol Rev 17:255-267. (Pubitemid 38534029)
36. Kron, S.J., Styles, C.A., and Fink, G.R (1994) Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol Biol Cell 5:1003-1022. (Pubitemid 24310588)
37. Kumamoto, CA. and Vinces, M.D. (2005) Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol 7:1546-1554. (Pubitemid 41511912)
38. Lambrechts, M.G., Bauer, F.F., Marmur, J., and Pretorius, I.S. (1996) Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudophyphal differentiation in yeast. Proc Natl Acad Sci USA 93:8419-8424. (Pubitemid 26269573)
39. Leys, N., Baatout, S., Rosier, C., Dams, A., s'Heeren, C., Wattiez, R, and Mergeay, M. (2009) The response of Cupriavidus metallidurans CH34 to spaceflight in the international space station. Antonie van Leeuwenhoek 96:227-245.
40. Liu, H.-Z., Wang, Q., Liu, X.-Y., and Tan, S.-S. (2008) Effects of spaceflight on polysaccharides of Saccharomyces cerevisiae cell wall. Appl Microbiol Biotechnol 81:543-550.
41. Lo, W.-S. and Dranginis, A.M. (1996) FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. J Bacteriol 178:7144-7151. (Pubitemid 26424627)
42. Lord, M., Chen, T., Fujita, A., and Chant, J. (2002) Analysis of budding patterns. Methods Enzymol 350:131-141. (Pubitemid 34619488)
43. Lynch, S.V., Mukundakrishnan, K., Benoit, M.R, Ayyaswamy, P.S., and Matin, A. (2006) Escherichia coli biofilms formed under low-shear modeled microgravity in a ground-based system. Appl Environ Microbiol 72:7701-7710. (Pubitemid 44927675)
44. McCusker, J.H., Clemons, K.V., Stevens, D.A., and Davis, R.W. (1994a) Saccharomyces cerevisiae virulence phenotype as deter-mined with CD-1 mice is associated with the ability to grow at 42°C and for pseudohyphae. Infect Immun 62:5447-5455. (Pubitemid 24364986)
45. McCusker, J.H., Clemons, K.V., Stevens, D.A., and Davis, R.W. (1994b) Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. Genetics 136:1261-1269. (Pubitemid 24097854)
46. Nickerson, C.A., Ott, C.M., Mister, S.J., Morrow, B.J., Burns-Keliher, L., and Pierson, D.L. (2000) Microgravity as a novel environmental signal affecting Salmonella enterica serovar ty-phimurium virulence. Infect Immun 68:3147-3152. (Pubitemid 30340402)
47. Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R, and Pierson, D.L. (2004) Microbial responses to microgravity and other low-shear environments. Microbiol Mol Biol Rev 68:345-361. (Pubitemid 38756869)
48. Palková, Z. and Vachová, L. (2006) Life within a community: benefit to yeast long-term survival. FEMS Microbiol Rev 30:806-824. (Pubitemid 44199351)
49. Pirt, S.J. (1967) A kinetic study of the mode of growth of surface colonies of bacteria and fungi. J Gen Microbiol 47:181-197
50. Pringle, J.R (1991) Staining of bud scars and other cell wall chitin with calcofluor. Methods Enzymol 194:732-735.
51. Prusty, R., Grisafi, P., and Fink, GR. (2004) The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 101:4153-4157. (Pubitemid 38405898)
52. Purevdorj-Gage, B., Sheehan, K.B., and Hyman, L.E. (2006) Ef-fects of low-shear modeled microgravity on cell function, gene expression and phenotype in Saccharomyces cerevisiae. Appl Environ Microbiol 72:4569-4575. (Pubitemid 44078779)
53. Ramage, G., Martínez, J.P., and López-Ribot, J.L. (2006) Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6:979-986. (Pubitemid 44568854)
54. Reynolds, T.B. and Fink, G.R. (2001) Bakers' yeast, a model for fungal biofilm formation. Science 291:878-881. (Pubitemid 32120759)
55. Reynolds, T.B., Jansen, A., Peng, X., and Fink, G.R (2008) Mat formation in Saccharomyces cerevisiae requires nutrient and pH gradients. Eukaryot Cell 7:122-130. (Pubitemid 351959600)
56. Roberts, R.L. and Fink, G.R (1994) Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two devel-opmental programs in the same cell type: mating and invasive growth. Genes Dev 8:2974-2985.
57. Rosenzweig, J.A., Abogunde, O., Thomas, K., Lawal, A., Nguyen, Y.-U., Sodipe, A., and Jejelowo, O. (2010) Spaceflight and modeled microgravity effects on microbial growth and virulence. Appl Microbiol Biotechnol 85:885-891.
58. Sheehan, K.B., McInnerney, K., Purevdorj-Gage, B., Altenburg, S.D., and Hyman, L.E. (2007) Yeast genomic expression pat-terns in response to low-shear modeled microgravity. BMC Genomics 8:3.
59. Sliwa, P., Kluz, J., and Korona, R (2004) Mutational load and the transition between diploidy and haploidy in experimental populations of the yeast Saccharomyces cerevisiae. Genetica 121:285-293. (Pubitemid 39182764)
60. Smukalla, S., Caldara, M., Pochet, N., Beauvais, A., Guadagnini, S., Yan, C., Vinces, M.D., Jansen, A., Prevost, M.-C., Latgé, J.P., Fink, G.R., Foster, K.R., and Verstrepen, K.J. (2008) FLO1 is a hyper-variable green beard gene that drives a transition to multicellularity in budding yeast. Cell 135:726-737.
61. Sonnenfeld, G (1999) Space flight, microgravity, stress, and immune responses. Adv Space Res 23:1945-1953.
62. Sonnenfeld, G. (2002) The immune system in space and micro-gravity. Med Sci Sports Exerc 34:2021-2027
63. Stanhill, A., Schick, N., and Engelberg, D. (1999) The yeast ras/cyclic AMP pathway induces invasive growth by suppressing the cellular stress response. Mol Cell Biol 19:7529-7538. (Pubitemid 29493416)
64. Taylor, G.R., Konstantinova, I., Sonnenfeld, G., Jennings, R., and Sjoerd, L.B. (1997) Changes in the immune system during and after spaceflight. Adv Space Res 6:1-32.
65. Teunissen, A.W.RH., and Steensma, H.Y. (1995) Review: the dominant flocculation genes of Saccharomyces cerevisiae constitute a new subtelomeric gene family. Yeast 11:1001-1013.
66. Van Mulders, S.E., Christianen, E., Saerens, S.M.G, Daenen, L., Verbelen, P.J., Willaert, R, Verstrepen, K.J., and Delvaux, F.R. (2009) Phenotypic diversity of Flo protein family-mediated adhesion in Saccharomyces cerevisiae. FEMS Yeast Res 9:178-190.
67. Vanhavere, F., Genicot, J.L., O'Sullivan, D., Zhou, D., Spurný, F., Jadrnícková, I., Sawakuchi, G.O., and Yukihara, E.G (2008) DOsimetry of BIological EXperiments in SPace (DOBIES) with luminescence (OSL and TL) and track etch detectors. Radiat Meas 43:694-697.
68. Verstrepen, K.J. and Klis, F.M. (2006) Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60:5-15. (Pubitemid 43363283)
69. Walther, I., Bechler, B., Müller, O., Hunzinger, E., and Cogoli, A. (1996) Cultivation of Saccharomyces cerevisiae in a bioreactor in microgravity. J Biotechnol 47:113-127. (Pubitemid 26276429)
70. West, J.B. (2000) Physiology of a microgravity environment historical perspectives: physiology in microgravity. J Appl Physiol 89:379-384. (Pubitemid 30482603)
71. Wilson, J.W., Ott, C.M., Ramamurthy, R., Porwollik, S., McClelland, M., Pierson, D.L., and Nickerson, C.A. (2002) Low-shear modeled microgravity alters the Salmonella enterica serovar Typhimurium stress response in an RpoS-indepen-dent manner. Appl Microbiol Biotechnol 68:5408-5416. (Pubitemid 35265674)
72. Wilson, J.W., Ott, C.M., zu Bentrup, K.H.n., Ramamurthy, R., Quick, L., Porwollik, S., Cheng, P., McClelland, M., Tsaprailis, G., Radabaugh, T., Hunt, A., Fernandez, D., Richter, E., Shah, M., Kilcoyne, M., Joshi, L., Nelman-Gonzalez, M., Hing, S., Parra, M., Dumars, P., Norwood, K., Bober, R, Devich, J., Ruggles, A., Goulart, C., Rupert, M., Stodieck, L., Stafford, P., Catella, L., Schurr, M.J., Buchanan, K., Morici, L., McCracken, J., Allen, P., Baker-Coleman, C., Hammond, T., Vogel, J., Nelson, R., Pierson, D.L., Stefanyshyn-Piper, H.M., and Nickerson, C.A. (2007) Space flight alters bacterial gene ex-pression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci USA 104:16299-16304. (Pubitemid 350099400)