Skip to main content
Log in

Effect of mycelial morphology on ergothioneine production during liquid fermentation of Lentinula edodes

  • Full Paper
  • Published:
Mycoscience

Abstract

The morphological type of a microorganism generally influences its metabolite production. In the present study, we investigated the effects of the mycelial morphology of shiitake (Lentinula edodes) on the production of 2-mercaptohistidine trimethylbetaine (ergothioneine, ESH) during liquid fermentation. Analyses of the distribution of ESH in mycelial cells of different morphological types revealed that the ESH content of pellets obtained from the liquid fermentation media was much greater than the content in the free mycelia and clumps. The concentration of ESH in pellets on day 15 of liquid fermentation reached 0.79 mg/g dry weight (DW), which is approximately three times the concentration found in mycelia clumps (0.28 mg/g DW) and free mycelia (0.31 mg/g DW). Macroscopic image analysis of the development and morphological changes of the pellets during a liquid fermentation period of up to 25 days indicated that pellet growth showed a highly positive correlation with the increase in ESH concentration (r 2 = 0.9851). A reduced agitation rate of 50 rpm for the culture medium was suitable for pellet formation and size enlargement. The results obtained in this work would be helpful in guiding the intentional manipulation of the distribution and enrichment of ESH in L. edodes through changes in liquid fermentation conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alvim FC, Mattos EM, Pirovani CP, Gramacho K, Pungartnik C, Brendel M, Cascardo JCM, Vincentz M (2009) Carbon source-induced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins. Genet Mol Res 8:1035–1050

    Article  PubMed  CAS  Google Scholar 

  • Baets SD, Laing SD, Francois C, Vandamme E (2002) Optimization of exopolysaccharide production by Tremella mesenterica NRRL Y-6158 through implementation of fed-batch fermentation. J Ind Microbiol Biotechnol 29:181–184

    Article  PubMed  Google Scholar 

  • Berovic M, Cimerman A (1982) Redox potential in submerged citric acid fermentation. Appl Microbiol Biotechnol 16:185–188

    Article  CAS  Google Scholar 

  • Berovic M, Cimerman A, Steiner W, Koloni T (1991) Submerged citric acid fermentation: rheological properties of Aspersillus niger broth in a stirred tank reactor. Appl Microbiol Biotechnol 34:579–581

    Article  CAS  Google Scholar 

  • Braun S, Vecht-Lifshitz SE (1991) Mycelial morphology and metabolite production. Trends Biotechnol 9:63–68

    Google Scholar 

  • Casas López JL, Pérez Sánchez JA, Sevilla Fernández JM, Rodríguez Porcel EM, Chisti YJ (2005) Pellet morphology, culture rheology and lovastatin production in cultures of Aspergillus terreus. J Biotechnol 116:61–77

    Google Scholar 

  • Cui YQ, Okkerse WJ, van der Lans RGJM, Luyben KChAM (1998) Modeling and measurements of fungal growth and morphology in submerged fermentations. Biotechnol Bioeng 60:216–229

    Google Scholar 

  • Dubost NJ, Beelman R, Royse D (2007) Influence of selected cultural factors and postharvest storage on ergothioneine content of common button mushroom Agaricus bisporus (J. Lge) Imbach (Agaricomycetideae). Int J Medicinal Mushrooms 9:163–176

    Article  CAS  Google Scholar 

  • Estrada A, Lee HJ, Beelman R, Jimenez-Gasco M, Royse D (2009) Enhancement of the antioxidants ergothioneine and selenium in Pleurotus eryngii var. eryngii basidiomata through cultural practices. World J Microbiol Biotechnol 25:1597–1607

    Article  Google Scholar 

  • Fazenda ML, Harvey LM, McNeil B (2010) Effects of dissolved oxygen on fungal morphology and process rheology during fed-batch processing of Ganoderma lucidum. J Microbiol Biotechnol 20:844–851

    Article  PubMed  CAS  Google Scholar 

  • Gehrig I, Bart HJ, Anke T, Germerdonk R (1998) Influence of morphology and rheology on the production characteristics of the basidiomycete Cyathus striatus. Biotechnol Bioeng 59:525–533

    Article  PubMed  CAS  Google Scholar 

  • Gibbs PA, Seviour RJ (1996) Does the agitation rate and/or oxygen saturation influence exopolysaccharide production by Aureobasidium pullulans in batch culture? Appl Microbiol Biotechnol 46:503–510

    Article  CAS  Google Scholar 

  • Gibbs PA, Seviour RJ, Schmid F (2000) Growth of filamentous fungi in submerged culture: problems and possible solutions. Crit Rev Biotechnol 20:17–48

    Article  PubMed  CAS  Google Scholar 

  • Hartman PE (1990) Ergothioneine as antioxidant. Methods Enzymol 186:310–318

    Article  PubMed  CAS  Google Scholar 

  • Hsieh C, Liu CJ, Tseng MH, Lo CT, Yang YC (2006) Effect of olive oil on the production of mycelial biomass and polysaccharides of Grifola frondosa under high oxygen concentration aeration. Enzyme Microb Technol 39:434–439

    Article  CAS  Google Scholar 

  • Hwang HJ, Kim SW, Xu CP, Choi JW, Yun JW (2004) Morphological and rheological properties of the three different species of basidiomycetes Phellinus in submerged cultures. J Appl Microbiol 96:1296–1305

    Article  PubMed  CAS  Google Scholar 

  • Lee WY, Park EJ, Ahn JK (2009) Supplementation of methionine enhanced the ergothioneine accumulation in the Ganoderma neo-japonicum mycelia. Appl Biochem Biotechnol 158:213–221

    Article  PubMed  CAS  Google Scholar 

  • Mattila P, Suonpää K, Piironen V (2002) Functional properties of edible mushrooms. Nutrition 16:694–696

    Article  Google Scholar 

  • Melville DB, Horner WH, Otken CC, Ludwig ML (1955) Studies on the origin of ergothioneine in animals. J Biol Chem 213:61–68

    PubMed  CAS  Google Scholar 

  • Metz B, Kossen NWF (1977) Biotechnology review: the growth of molds in the form of pellets. A literature review. Biotechnol Bioeng 19:781–799

    Article  CAS  Google Scholar 

  • Moore D, Robson GD, Trinci APJ (2011) Whole organism biotechnology. In: Moore D, Robson GD, Trinci APJ (eds) 21st century guidebook to fungi. Cambridge University Press, London, pp 451–510

    Google Scholar 

  • Nielsen J, Johansen CL, Jacobsen M, Krabben P, Villadsen J (1995) Pellet formation and fragmentation in submerged cultures of Penicillium chrysogenum and its relation to penicillin production. Biotechnol Prog 11:93–98

    Article  PubMed  CAS  Google Scholar 

  • Packer HL, Thomas CR (1990) Morphological measurements on filamentous microorganisms by fully automatic image analysis. Biotechnol Bioeng 35:870–881

    Article  PubMed  CAS  Google Scholar 

  • Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259

    Article  PubMed  CAS  Google Scholar 

  • Park YS, Ohta N, Okabe M (1993) Effect of dissolved oxygen concentration and impeller tip speed on itaconic acid production by Aspersillus terreus. Biotechnol Lett 15:583–586

    Article  CAS  Google Scholar 

  • Paul BD, Snyder SH (2010) The unusual amino acid l-ergothioneine is a physiologic cytoprotectant. Cell Death Differ 17:1134–1140

    Article  PubMed  CAS  Google Scholar 

  • Prosser JI, Tough AJ (1991) Growth mechanisms and growth kinetics of filamentous microorganisms. Crit Rev Biotechnol 10:253–274

    Article  PubMed  CAS  Google Scholar 

  • Rahman I, Gilmour PS, Jimenez LA, Biswas SK, Antonicelli F, Aruoma OI (2003) Ergothioneine inhibits oxidative stress- and TNF-α-induced NF-κB activation and interleukin-8 release in alveolar epithelial cells. Biochem Biophys Res Commun 302:860–864

    Article  PubMed  CAS  Google Scholar 

  • Reichl U, King R, Gilles ED (1992) Characterization of pellet morphology during submerged growth of Streptomyces tendae by image analysis. Biotechnol Bioeng 39:164–170

    Article  PubMed  CAS  Google Scholar 

  • Riley GL, Tucker KG, Paul GC, Thomas CR (2000) Effect of biomass concentration and mycelial morphology on fermentation broth rheology. Biotechnol Bioeng 68:160–172

    Article  PubMed  CAS  Google Scholar 

  • Riscaldati E, Moresi M, Federici F, Petruccioli M (2000) Effect of pH and stirring rate on itaconate production by Aspergillus terreus. J Biotechnol 83:219–230

    Article  PubMed  CAS  Google Scholar 

  • Rühl M (2009) Laccases and other ligninolytic enzymes of the basidiomycetes Coprinopsis cinerea and Pleurotus ostreatus—submerged and solid state fermentation, morphological studies of liquid cultures and characterisation of new laccases. Ph.D dissertation. Georg-August-University Göttingen, Göttingen

  • Schügerl K, Wittler R, Lorenz T (1983) The use of molds in pellet form. Trends Biotechnol 1:120–123

    Article  Google Scholar 

  • Sinha J, Bae JT, Park JP, Kim KH, Song CH, Yun JW (2001) Changes in morphology of Paecilomyces japonica and their effect on broth rheology during production of exo-biopolymers. Appl Microbiol Biotechnol 56:88–92

    Article  PubMed  CAS  Google Scholar 

  • Sobczuk TM, Camacho FG, Grima EM, Chirti Y (2005) Effects of agitation on the microalgae Phaeodactylum tricornutum and Porphyridium cruentum. Bioprocess Biosyst Eng 28:243–250

    Article  PubMed  Google Scholar 

  • Tang YJ, Zhong JJ (2003) Role of oxygen supply in submerged fermentation of Ganoderma lucidum for production of Ganoderma polysaccharide and ganoderic acid. Enzyme Microb Technol 32:478–484

    Article  CAS  Google Scholar 

  • Turło J, Gutkowskaa B, Herold F, Krzyczkowski W, Błazewicz A, Kocjan R (2008) Optimizing vitamin B12 biosynthesis by mycelial cultures of Lentinula edodes (Berk.) Pegl. Enzyme Microb Technol 43:369–374

    Article  Google Scholar 

  • Wagner R, Mitchell DA, Sassaki GL, Amazonas MALA (2004) Links between morphology and physiology of Ganoderma lucidum in submerged culture for the production of exopolysaccharide. J Biotechnol 114:153–164

    Article  PubMed  CAS  Google Scholar 

  • Yang FC, Liau CB (1998) The influence of environmental conditions on polysaccharide formation by Ganoderma lucidum in submerged cultures. Process Biochem 33:547–553

    Article  CAS  Google Scholar 

  • Yang YK, Sbimizu H, Shioya S, Suga K, Nihira T, Yamada Y (1995) Optimum autoregulator addition strategy for maximum virginiamycin production in batch culture of Streptomyces virginiae. Biotechnol Bioeng 46:437–442

    Article  PubMed  CAS  Google Scholar 

  • Zhong JJ, Yue CJ (2005) Plant cells: secondary metabolite heterogeneity and its manipulation. Biotechnology for the future. Adv Biochem Eng Biotechnol 100:53–88

    PubMed  CAS  Google Scholar 

  • Zorn H, Bouws H, Takenberg M, Nimtz M, Getzlaff R, Breithaupt DE, Berger RG (2005) An extracellular carboxylesterase from the basidiomycete Pleurotus sapidus hydrolyses xanthophyll esters. Biol Chem 386:435–440

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Toshiaki Ohshima.

About this article

Cite this article

Tepwong, P., Giri, A. & Ohshima, T. Effect of mycelial morphology on ergothioneine production during liquid fermentation of Lentinula edodes . Mycoscience 53, 102–112 (2012). https://doi.org/10.1007/s10267-011-0145-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10267-011-0145-0

Keywords

Navigation