Effect of Growth Media, pH and Temperature on Yeast to Hyphal Transition in Candida albicans

Abstract

The transition of C. albicans from unicellular yeast form to filamentous form i.e., pseudohyphae and hyphae is referred to as morphogenesis. C. albicans has the ability to respond to environmental conditions and accordingly changing its cell morphology. Three main morphological forms of C. albicans are unicellular yeast, pseudohyphae and hyphae. The effect of different growth media (Horse serum medium, RPMI-1640, MSGB), incubation temperatures (34°C, 37°C, 40°C) and pH values (5.4, 6.4, 7.4) on germ tube production by C. albicans was evaluated. Horse serum medium noticeably promotes filamentation while RPMI-1640 medium shows moderate filamentation and MSGB media shows moderately low filamentation. The germ tube of C. albicans developed early in 1.5 hr at high temperature i.e., 40°C. Incubation temperature of 37°C was associated with highest germ tube formation while 34°C shows low filamentation. A pH of 5.4 also induces low filamentation, pH 6.4 gives moderately lower than pH 7.4. A pH of 7.4 was best suited for germ tube induction. The peak of mycelium production appears between 1.5 and 6 hr after inoculation of C. albicans culture. These results suggested that environmental factors are important in selectively favoring yeast or hyphal form, most important being the growth medium, incubation temperature and external pH value.

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S. Nadeem, A. Shafiq, S. Hakim, Y. Anjum and S. U. Kazm, "Effect of Growth Media, pH and Temperature on Yeast to Hyphal Transition in Candida albicans," Open Journal of Medical Microbiology, Vol. 3 No. 3, 2013, pp. 185-192. doi: 10.4236/ojmm.2013.33028.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] J. Schulze and U. Sonnenborn, “Yeast in the Gut: From Commensals to Infectious Agents,” Deutsches Arzteblatt, Vol. 106, No. 51-52, 2009, pp. 837-842.
[2] F. C. Odds, “Candida and Candidosis,” 5th Edition, Baillière Tindall, London, 1988.
[3] D. R. Soll, M. Staebell, C. Langtimm, M. Pfaller, J. Hicks and T. V. G Rao, “Multiple Candida Strains in the Course of a Single Systemic Infection,” Journal of Clinical Microbiology, Vol. 26, No. 8, 1988, pp. 1448-1459.
[4] J. D. Sobel, “Vaginitis,” New England Journal of Medicine, Vol. 337, No. 26, 1997, pp. 1896-1903. doi:10.1056/NEJM199712253372607
[5] R. A. Calderone, “Candida and Candidiasis,” ASM Press, Washington DC, 2002.
[6] J. A. Sexton, V. Brown, and M. Johnston, “Regulation of Sugar Transport Andmetabolism by the Candida albicans Rgt1 Transcriptional Repressor,” Yeast, Vol. 24, No. 10, 2007, pp. 847-860. doi:10.1002/yea.1514
[7] H. J. Lo, J. R. Kohler, B. Di Domenico, D. Loebenberg, A. Cacciapuoti and G. R. Fink, “Nonfilamentous C. albicans Mutants Are a Virulent,” Cell, Vol. 90, No. 5, 1997, pp. 939-949. doi:10.1016/S0092-8674(00)80358-X
[8] B. R. Braun, W. S. Head, M. X. Wang and A. D. Johnson, “Identification and Characterization of TUP1-Regulated Genes in C. albicans,” Genetics, Vol. 156, No. 1, 2000, pp. 31-44.
[9] B. R. Braun, D. Kadosh and A. D. Johnson, “NRG1, a Repressor of Filamentous Growth in C. albicans, Is Down-Regulated during Filament Induction,” EMBO Journal, Vol. 20, No. 17, 2001, pp. 4753-4761. doi:10.1093/emboj/20.17.4753
[10] A. M. Murad, P. Leng, M. Straffon, J. Wishart, S. Macaskill, D. MacCallum, et al., “NRG1 Represses Yeast-Hypha Morphogenesis and Hypha-Specific Gene Expression in C. albicans,” EMBO Journal, Vol. 20, No. 17, 2001, pp. 4742-4752. doi:10.1093/emboj/20.17.4742
[11] S. P. Saville, A. L. Lazzell, C. Monteagudo and J. L. Lopez-Ribot, “Engineered Control of Cell Morphology in Vivo Reveals Distinct Roles for Yeast and Filamentous Forms of C. albicans during Infection,” Eukaryotic Cell, Vol. 2, No. 5, 2003, pp. 1053-1060. doi:10.1128/EC.2.5.1053-1060.2003
[12] M. S. A Khan, I. Ahmad, F. Aqil, M. Owais, M. Shahid and J. Musarrat, “Virulence and Pathogenicity of Fungal Pathogens with Special Reference to C. albicans,” In: I. Ahmad, M. Owais, M. Shahid and F. Aqil, Eds., Combating Fungal Infections: Problems and Remedy, Springer- Verlag, Berlin, 2010, pp. 21-45. doi:10.1007/978-3-642-12173-9_2
[13] P. Sudbery, N. Gow and J. Berman, “The Distinct Morphogenic States of Candida albicans,” Trends in Microbiology, Vol. 12, No. 7, 2004, pp. 317-324. doi:10.1016/j.tim.2004.05.008
[14] L. A. Merson-Davies and F. C. Odds, “A Morphology Index for Characterization of Cell Shape in C. albicans,” Journal of General Microbiology, Vol. 135, No. 11, 1989, pp. 3143-3152.
[15] M. Montazeri and H. G. Hedrick, “Factors Affecting Spore Formation in a Candida albicans Strain,” Applied and Environmental Microbiology, Vol. 47, No. 6, 1984, pp. 1341-1342.
[16] Y. L. Yang, “Virulence Factors of Candida Species,” Journal of Microbiology Immunology and Infection, Vol. 36, No. 4, 2003, pp. 223-228.
[17] H. Court and P. Sudbery, “Regulation of Cdc42 GTPase Activity in the Formation of Hyphae in C. albicans,” Molecular Biology of the Cell, Vol. 18, No. 1, 2007, pp. 265-281. doi:10.1091/mbc.E06-05-0411
[18] J. Berman, “Morphogenesis and Cell Cycle Progression in C. albicans,” Current Opinion in Microbiology, Vol. 9, No. 6, 2006, pp. 595-601.
[19] L. H. Kimura and N. N. Pearsall, “Adherence of C. albicans to Human Vaginal and Buccal Epithelial Cells,” Journal of Infectious Diseases, Vol. 21, No. 1, 1978, pp. 64-68. doi:10.1016/j.mib.2006.10.007
[20] J. C. Lee and R. D. King, “Characterization of C. albicans Adherence to Human Vaginal Epithelial Cells in Vitro,” Infection and Immunology, Vol. 41, No. 3, 1983, pp. 1024-1030.
[21] J. D. Sobel, G. Muller and H. R. Buckley, “Critical Role of Germ Tube Formation in the Pathogenesis of Candidal Vaginitis,” Infection and Immunology, Vol. 44, No. 3, 1984, pp. 576-580.
[22] J. Berman and P. E. Sudbery, “C. albicans: A Molecular Revolution Built on Lessons from Budding Yeast,” Nature Reviews Genetics, Vol. 3, No. 12, 2002, pp. 918-930. doi:10.1038/nrg948
[23] N. A. R. Gow, “Cell Biology and Cell Cycle of Candida albicans,” In: R. A. Calderone, Ed., Candida and Candidiasis, American Society for Microbiology, Washington, DC, 2002, pp. 145-158.
[24] P. Sundstrom, “Candida albicans Hypha Formation and Virulence,” In: J. Heitman, Ed., Molecular Principles of Fungal Pathogenesis, American Society for Microbiology, Washington DC, 2006, pp. 45-47.
[25] D. W. Hill and L. P. Gerbhardt, “Morphological Transformation of Candida albicans in Tissues of Mice,” Proceedings of the Society for Experimental Biology and Medicine, Vol. 92, No. 2, 1988, pp. 640-644.
[26] P. J. Kozinn, C. L. Taschdjian and J. J. Burchall., “Transmission of P-32 Labeled Candida albicans to Newborn Mice at Birth,” American Journal of Diseases of Children, Vol. 99, No. 1, 1960, pp. 31-34.
[27] G. Young, “The Process of Invasion and the Persistence of Candida albicans Injected Intraperitoneally into Mice,” Journal of Infectious Diseases, Vol. 102, No. 2, 1964, pp. 114-120. doi:10.1093/infdis/102.2.114
[28] N. A. Gow, A. J. Brown and F. C. Odds, “Fungal Morphogenesis and Host Invasion,” Current Opinion in Microbiology, Vol. 5, No. 4, 2002, pp. 366-371.
[29] G. D. Brown, “Innate Antifungal Immunity: The Key Role of Phagocytes,” Annual Review of Immunology, Vol. 29, No. 1, 2001, pp. 1-21. doi:10.1146/annurev-immunol-030409-101229
[30] R. Kaposzta, L. Marodi, M. Hollinshead, S. Gordon and R. P. da Silva, “Rapid Recruitment of Late Endosomes and Lysosomes in Mouse Macrophages Ingesting Candida albicans,” Journal of Cell Science, Vol. 112, No. 19, 1999, pp. 3237-3248.
[31] L. E. Lewis, J. M. Bain, C. Lowes, C. Gillespie, F. M. Rudkin, et al., “Stage Specific Assessment of Candida albicans Phagocytosis by Macrophages Identifies Cell Wall Composition and Morphogenesis as Key Determinants,” PLOS Pathogens, Vol. 8, No. 3, 2012, Article ID: e1002578.
[32] A. J. P. Brown, “Expression of Growth Form-Specific Factors during Morphogenesis in C. albicans,” In: R. Calderone, Ed., Candida and Candidiasis, ASM Press, Washington DC, 2002, pp. 87-93.
[33] A. R. Holmes and M. G. Shepherd, “Proline Induced Germ-Tube Formation in C. albicans: Role of Proline Uptake and Nitrogen Metabolism,” Journal of General Microbiology, Vol. 133, No. 11, 1987, pp. 3219-3228.
[34] E. G. Mattia, G. Corruba, L. Angiolella and A. Casone, “Induction of Germ Tube Formation by N-acetyl-D Glucosamine in Candida albicans: Uptake of Inducer and Germinative Response,” Journal of Bacteriology, Vol. 152, No. 2, 1982, pp. 555-562.
[35] G. Tripathi, C. Wiltshire, S. Macaskill, H. Tournu, S. Budge and A. J. Brown, “Gcn4 Coordinates Morphogenetic and Metabolic Responses to Amino Acid Starvation in Candida albicans,” EMBO Journal, Vol. 21, No. 20, 2002, pp. 5448-5456. doi:10.1093/emboj/cdf507
[36] J. F. Ernst, “Transcription Factors in Candida albicans—Environmental Control of Morphogenesis,” Microbiology, Vol. 146, No. 8, 2000, pp. 1763-1774.
[37] J. Buffo, M. A. Herman and D. R. Soll, “A Characterization of pH-Regulated Dimorphism in Candida albicans,” Mycopathologia, Vol. 85, No. 1-2, 1984, pp. 21-30. doi:10.1007/BF00436698
[38] D. O. McClary, “Factors Affecting the Morphology of Candida albicans,” Annals of the Missouri Botanical Gardens, Vol. 39, No. 2, 1952, pp. 137-164. doi:10.2307/2394509
[39] S. Kabli, “Morphogenesis of Two Candida albicans Strains as Influenced by Growth Media, pH Value and Incubation Temperature,” American-Eurasian Journal of Agriculture and Environmental Science, Vol. 1, No. 2, 2006, pp. 127-132.
[40] White Labs, “Cell Counting/Viability Testing,” 2013. http://www.whitelabs.com/content/cell-countingviability-testing-0
[41] E. G. Evans, F. C. Odds and K. T. Holland, “Optimum Conditions for Initiation of Filamentation in Candida albicans,” Canadian Journal of Microbiology, Vol. 21, No. 3, 1975, pp. 338-342. doi:10.1139/m75-048
[42] K. L. Lee, H. R. Buckley and H. R. Campbell, “An Amino Acid Liquid Synthetic Medium for Development of Mycellal and Yeast Forms of Candida albicans,” Medical Mycology, Vol. 13, No. 2, 1975, pp. 148-153. doi:10.1080/00362177585190271
[43] P. Auger and J. Joly, “Factors Influencing Germ Tube Production in Candida albicans,” Mycopathologia, Vol. 61, No. 3, 1977, pp. 183-186. doi:10.1007/BF00468014
[44] V. Paranjape and A. Datta, “Role of Nutritional Status & the Cell in pH Regulated Dimorphism of Candida albicans,” FEMS Microbiology Letters, Vol. 80, No. 2-3, 1991, pp. 333-336. doi:10.1111/j.1574-6968.1991.tb04685.x
[45] M. Casanova, A. M. Cervera, D. Gozalbo and J. P. Martinez, “Hemin Induces Germ Tube Formation in Candida albicans,” Infection and Immunology, Vol. 65, No. 10, 1997, pp. 4360-4364.
[46] C. Westwater, E. Balish and D. A. Schofield, “Candida albicans-Conditioned Medium Protects Yeast Cells from Oxidative Stress: A Possible Link between Quorum Sensing and Oxidative Stress Resistance,” Eukaryotic Cell, Vol. 4, No. 10, 2005, pp. 1654-1666. doi:10.1128/EC.4.10.1654-1661.2005
[47] E. Mattia and A. Cassone, “Inducibility of Germ-Tube Formation in Candida albicans at Different Phases of Yeast Growth,” Microbiology, Vol. 113, No. 2, 1979, pp. 439-442. doi:10.1099/00221287-113-2-439
[48] K. V. Clemons, J. L. Spearow, R. Parmar, M. Espiritu and D. A. Stevens, “Genetic Susceptibility of Mice to Candida albicans Vaginitis Correlates with Host Estrogen Sensitivity,” Infection and Immunology, Vol. 72, No. 8, 2004, pp. 4878-4880. doi:10.1128/IAI.72.8.4878-4880.2004
[49] F. Sabie and G. M. Gadd, “Induction of Germ-Tube Formation by Candida albicans in Amino Acid Liquid Synthetic Medium at 25 Degrees C,” Mycopathologia, Vol. 101, No. 2, 1988, pp. 77-83. doi:10.1007/BF00452890
[50] H. Tournu, G. Tripathi, G. Bertram, S. Macaskill, A. Mavor, L. Walker, F. C. Odds, N. A. Gow and A. J. Brown, “Global Role of the Protein Kinase Gcn2 in the Human Pathogen Candida albicans,” Eukaryotic Cell, Vol. 4, No. 10, 2005, pp. 1687-1696. doi:10.1128/EC.4.10.1687-1696.2005
[51] D. C. Johnson, K. E. Cano, E. C. Kroger and D. S. McNabb, “Novel Regulatory Function for the CCAAT- Binding Factor in Candida albicans,” Eukaryotic Cell, Vol. 4, No. 10, 2005, pp. 1662-1676. doi:10.1128/EC.4.10.1662-1676.2005
[52] M. Bruatto, M. Gremmi, A. Nardacchione and M. Amerio, “Effect of Glucose Starvation on Germ-Tube Production by Candida albicans,” Mycopathologia, Vol. 123, No. 2, 1993, pp. 105-110. doi:10.1007/BF01365088
[53] H. Lotz, K. Sohn, H. Brunner, F. A. Muhlschlegel and S. Rupp, “RBR1, a Novel pH-Regulated Cell Wall Gene of Candida albicans, Is Repressed by RIM101 and Activated by NRG1,” Eukaryotic Cell, Vol. 3, No. 3, 2004, pp. 776-784. doi:10.1128/EC.3.3.776-784.2004
[54] B. Enjalbert and M. Whiteway, “Release from Quorum-Sensing Molecules Triggers Hyphal Formation during Candida albicans Resumption of Growth,” Eukaryotic Cell, Vol. 4, No. 7, 2005, pp. 1203-1210. doi:10.1128/EC.4.7.1203-1210.2005
[55] M. Cornet, F. Bidard, P. Schwarz, G. Da Costa, S. Blanchin-Roland, F. Dromer and C. Gaillardin, “Deletions of Endocytic Components VPS28 and VPS32 Affect Growth at Alkaline pH and Virulence through both RIM101-Dependent and RIM101-Independent Pathways in Candida albican,” Infection and Immunology, Vol. 73, No. 12, 2005, pp. 7977-7987. doi:10.1128/IAI.73.12.7977-7987.2005

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