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Applying dimorphic yeasts as model organisms to study mycelial growth: Part 1. Experimental investigation of the spatio-temporal development of filamentous yeast colonies

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Abstract

Colony development of the dimorphic yeasts Yarrowia lipolytica and Candida boidinii on solid agar substrates under glucose limitation served as a model system for mycelial development of higher filamentous fungi. Strong differences were observed in the behaviour of both yeasts: C. boidinii colonies reached a final colony extension which was small compared to the size of the growth field. They formed cell-density profiles which steeply declined along the colony radius and no biomass decay processes could be detected. The stop of colony extension coincided with the depletion of glucose from the growth substrate. These findings supported the hypothesis that glucose-limited C. boidinii colonies can be regarded as populations of single cells which grow according to a diffusion-limited growth mechanism. Y. lipolytica colonies continued to extend after the depletion of the primary nutrient resource, glucose, until the populations covered the entire growth field which was accomplished by utilization of mycelial biomass.

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References

  1. Gow NAR, Robson GD, Gadd GM (1999) The fungal colony. University Press, Cambridge

    Book  Google Scholar 

  2. Punt PJ, van Biezen N, Conesa A, Albers A, Mangnus J, van den Hondel C (2002) Filamentous fungi as cell factories for heterologous protein production. Trends Biotechnol 20:200–206

    Article  CAS  Google Scholar 

  3. Nielsen J (1993) A simple morphologically structured model describing the growth of filamentous microorganisms. Biotechnol Bioeng 41:715–727

    Article  CAS  Google Scholar 

  4. Boddy L (1999) Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91:13–32

    Article  Google Scholar 

  5. Ritz K (1995) Growth response of some soil fungi to spatially heterogeneous nutrients. FEMS Microbiol Ecol 16:269–280

    Article  CAS  Google Scholar 

  6. Ritz K, Millar SM, Crawford JW (1996) Detailed visualisation of hyphal distribution in fungal mycelia growing in heterogeneous nutritional environments. J Microbiol Methods 25:23–28

    Article  Google Scholar 

  7. Jacobs H, Boswell GP, Scrimgeour CM, Davidson FA, Gadd GM, Ritz K (2004) Translocation of carbon by Rhizoctonia solani in nutritionally-heterogeneous microcosms. Mycol Res 108:453–462

    Article  Google Scholar 

  8. Olsson S, Gray SN (1998) Patterns and dynamics of 32P-phosphate and labelled 2-aminobutyric acid (14C-AIB) translocation in intact basidiomycete mycelia. FEMS Microbiol Ecol 26:109–120

    Article  CAS  Google Scholar 

  9. Walther T, Reinsch H, Grosse A, Ostermann K, Deutsch A, Bley T (2004) Mathematical modeling of regulatory mechanisms in yeast colony development. J Theor Biol 229:327–338

    Article  CAS  Google Scholar 

  10. Davidson FA, Sleeman BD, Rayner ADM, Crawford JW, Ritz K (1997) Travelling waves and pattern formation in a model for fungal development. J Math Biol 35:589–608

    Article  Google Scholar 

  11. Boswell GP, Jacobs H, Ritz K, Gadd GM, Davidson FA (2007) The development of fungal networks in complex environments. Bull Math Biol 69:605–634

    Article  Google Scholar 

  12. Boswell GP, Jacobs H, Davidson FA, Gadd GM, Ritz K (2003) Growth and function of fungal mycelia in heterogeneous environments. Bull Math Biol 65:447–477

    Article  Google Scholar 

  13. Falconer RE, Brown JL, White NA, Crawford JW (2005) Biomass recycling and the origin of phenotype in fungal mycelia. Proc R Soc B 272:1727–1734

    Article  Google Scholar 

  14. Davidson FA (1998) Modelling the qualitative response of fungal mycelia to heterogeneous environments. J Theor Biol 195:281–292

    Article  Google Scholar 

  15. Davidson FA, Park AW (1998) A mathematical model for fungal development in heterogeneous environments. Appl Math Lett 11:51–56

    Article  Google Scholar 

  16. Davidson FA, Sleeman BD, Rayner ADM, Crawford JW, Ritz K (1996) Context-dependent macroscopic patterns in growing and interacting mycelial networks. Proc R Soc Lond B 263:873–880

    Article  Google Scholar 

  17. Walther T, Reinsch H, Ostermann K, Deutsch A, Bley T (2005) Coordinated development of yeast colonies: Quantitative modeling of diffusion-limited growth - Part 2. Eng Life Sci 5:125–133

    Article  CAS  Google Scholar 

  18. Walther T, Reinsch H, Ostermann K, Deutsch A, Bley T (2010) Applying dimorphic yeasts as model organisms to study mycelial growth: Part 2. Application of mathematical models to identify different construction principles in yeast colonies (submitted)

  19. Walther T, Reinsch H, Ostermann K, Deutsch A, Bley T (2005) Coordinated development of yeast colonies: experimental analysis of the adaptation to different nutrient concentrations—Part 1. Eng Life Sci 5:115–124

    Article  CAS  Google Scholar 

  20. Varon M, Choder M (2000) Organization and cell–cell interaction in starved Saccharomyces cerevisiae colonies. J Bacteriol 182:3877–3880

    Article  CAS  Google Scholar 

  21. Palkova Z, Devaux F, Icicova M, Minarikova L, Le Crom S, Jacq C (2002) Ammonia pulses and metabolic oscillations guide yeast colony development. Mol Biol Cell 13:3901–3914

    Article  CAS  Google Scholar 

  22. Palkova Z, Forstova J (2000) Yeast colonies synchronise their growth and development. J Cell Sci 113:1923–1928

    CAS  Google Scholar 

  23. Palkova Z, Janderova B, Gabriel J, Zikanova B, Pospisek M, Forstova J (1997) Ammonia mediates communication between yeast colonies. Nature 390:532–536

    Article  CAS  Google Scholar 

  24. Boschke E, Bley T (1998) Growth patterns of yeast colonies depending on nutrient supply. Acta Biotechnol 18:17–27

    Article  Google Scholar 

  25. Dominguez A, Ferminan E, Gaillardin C (2000) Yarrowia lipolytica: an organism amenable to genetic manipulation as a model for analyzing dimorphism in fungi. In: Ernst H, Schmidt A (eds) Dimorphism in human pathogenic and apathogenic yeasts, vol 5, 1st edn. Karger, Basel, pp 151–172

    Chapter  Google Scholar 

  26. Perez-Campo FM, Dominguez A (2001) Factors affecting the morphogenetic switch in Yarrowia lipolytica. Curr Microbiol 43:429–433

    Article  CAS  Google Scholar 

  27. Atlas RM (1996) Handbook of microbiological media, 2nd edn. CRC Press, Bocaraton

    Google Scholar 

  28. Gow NAR, Gooday GW (1982) Growth kinetics and morphology of colonies of the filamentous form of Candida albicans. J Gen Microbiol 128:2187–2194

    CAS  Google Scholar 

  29. Olsson L (1999) Nutrient translocation and electrical signalling in mycelia. In: Gow NAR, Robson GD, Gadd GM (eds) The fungal colony, 1st edn. University Press, Cambridge

    Google Scholar 

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Acknowledgments

This work was supported by DFG grant 218147.

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Author notes

  1. Thomas Walther

    Present address: Laboratoire d’Ingénierie des Systèmes Biologiques et des Procédés, UMR INSA/CNRS 5504, UMR INSA/INRA 792, Institut National des Sciences Appliquées (INSA), 135 Avenue de Rangueil, 31077, Toulouse Cedex 04, France

Authors and Affiliations

  1. Institute of Food Technology and Bioprocess Engineering, Technical University Dresden, 01062, Dresden, Germany

    Thomas Walther, Holger Reinsch, Philipp Weber & Thomas Bley

  2. Institute of Genetics, Technical University Dresden, 01062, Dresden, Germany

    Kai Ostermann

  3. Center for Information Services and High Performance Computing, Technical University Dresden, 01062, Dresden, Germany

    Andreas Deutsch

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  1. Thomas Walther
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  4. Kai Ostermann
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  6. Thomas Bley
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Correspondence to Thomas Walther.

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449_2010_442_MOESM1_ESM.tif

Schematic illustration of the experimental setup for the comparison of the growth of “cut-out” and undisturbed yeast colonies. One batch of colonies was precultured (A) until the colony interior in one half of the batch was removed after 13 days (B). Then, “cut-out” and undisturbed colonies were further cultivated up to a maximum cultivation time of 56 days (C). The asterisk represents the centre of the petri dish. The dimensions of the growth fields are the same as in Fig. 1. (TIFF 2812 kb)

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Walther, T., Reinsch, H., Weber, P. et al. Applying dimorphic yeasts as model organisms to study mycelial growth: Part 1. Experimental investigation of the spatio-temporal development of filamentous yeast colonies. Bioprocess Biosyst Eng 34, 13–20 (2011). https://doi.org/10.1007/s00449-010-0442-6

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  • DOI: https://doi.org/10.1007/s00449-010-0442-6

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