Advertisement

Talaromyces australis and Penicillium murcianum pigment production in optimized liquid cultures and evaluation of their cytotoxicity in textile applications

  • Vicente A. HernándezEmail author
  • Ángela MachucaEmail author
  • Isaac Saavedra
  • Daniel Chavez
  • Allisson Astuya
  • Carolina Barriga
Original Paper
  • 40 Downloads

Abstract

In this work Talaromyces australis and Penicillium murcianum pigment production in liquid cultures and the cytotoxic effect of such pigments on skin model cells were studied. Response surface methodology (RSM) was used to optimize culture conditions aiming to increase pigment production in malt extract and peptone-glucose-yeast extract medium. Cytotoxicity of fungal pigments and also from lixiviates of wool fabrics dyed with T. australis and P. murcianum pigment was evaluated on mammalian cell lines HEK293 and NIH/3T3. Results showed that variations on initial pH, NaCl and peptone, resulted in increments up to 188.2% for red pigment of T. australis and 107.4% for yellow pigment of P. murcianum, regarding non-optimized conditions. Tested fungi also showed great differences in culture conditions for the maximum pigment production, with P. murcianum requiring an alkaline medium (initial pH 9) supplemented with NaCl and T. australis an acidic medium (initial pH 5) without addition of salt. The cytotoxicity assays provided evidences on the safe nature of these natural pigments when used for textile applications. The cytotoxicity assay showed that the threshold of toxicity, given by the lowest IC50 value (0.21 g L−1) was more than double of the concentration of pigment required to dye the wool samples. In addition, cytotoxicity of lixiviates depicted no toxic effect over tested cells.

Keywords

Fungal pigments IC50 Mammalian cell lines Natural pigments Response surface methodology Wool fabrics 

Notes

Acknowledgements

This work was financially supported by CONICYT IDeA FONDEF ID15I-10105. VAH acknowledge the support from CONICYT PIA/APOYO CCTE AFB170007, and PAI Convocatoria Nacional Subvención a Instalación en la Academia 2018, 77180054.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicting interests.

References

  1. Akilandeswari P, Pradeep BV (2016) Exploration of industrially important pigments from soil fungi. Appl Microbiol Biotechnol 100:1631–1643CrossRefGoogle Scholar
  2. Babitha S, Soccol C, Pandey A (2007) Effect of stress on growth, pigment production and morphology of Monascus sp. in solid cultures. J Basic Microbiol 47:118–126CrossRefGoogle Scholar
  3. Bhosale P (2004) Environmental and cultural stimulants in the production of carotenoids from microorganisms. Appl Microbiol Biotechnol 63:351–361CrossRefGoogle Scholar
  4. Chadni Z, Rahaman M, Jerin I, Hoque K, Reza M (2017) Extraction and optimisation of red pigment production as secondary metabolites from Talaromyces verruculosus and its potential use in textile industries. Mycology 8:48–57CrossRefGoogle Scholar
  5. Chintapenta LK, Rath CC, Maringinti B, Ozbay G (2014) Pigment production from a mangrove Penicillium. Afr J Biotechnol 13:2668–2674CrossRefGoogle Scholar
  6. Dufossé L, Galaup P, Yaron A, Arad S, Blanc P, Chidambara M, Ravishankar G (2005) Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality? Trends Food Sci Technol 16:389–406CrossRefGoogle Scholar
  7. Dufossé L, Fouillaud M, Caro Y, Mapari S, Sutthiwong N (2014) Filamentous fungi are large-scale producers of pigments and colorants for the food industry. Curr Opin Biotechnol 26:56–61CrossRefGoogle Scholar
  8. Escobar L, Rivera A, Aristizábal F (2010) Estudio comparativo de los métodos de resazurina y MTT en estudios de citotoxicidad en líneas celulares tumorales humanas. Vitae 17:67–74Google Scholar
  9. Feng Y, Shao Y, Chen F (2012) Monascus pigments. Appl Microbiol Biotechnol 96:1421–1440CrossRefGoogle Scholar
  10. Gmoser R, Ferreira J, Lennartsson P, Taherzadeh M (2017) Filamentous ascomycetes fungi as a source of natural pigments. Fungal Biol Biotechnol 4:4CrossRefGoogle Scholar
  11. Gunasekaran S, Poorniammal R (2008) Optimization of fermentation conditions for red pigment production from Penicillium sp. under submerged cultivation. Afr J Biotechnol 7:1894–1898CrossRefGoogle Scholar
  12. Halle W (2003) The Registry of Cytotoxicity: toxicity testing in cell cultures to predict acute toxicity (LD50) and to reduce testing in animals. Altern Lab Anim 31:89–198CrossRefGoogle Scholar
  13. Hamdi M, Blanc PJ, Loret MO, Goma G (1997) A new process for red pigment production by submerged culture of Monascus purpureus. Bioprocess Eng 17:75–79Google Scholar
  14. Hernández V, Galleguillos F, Sagredo N, Machuca A (2018) A Note on the dyeing of wool fabrics using natural dyes extracted from rotten wood-inhabiting fungi. Coatings 8:77CrossRefGoogle Scholar
  15. Hernández V, Galleguillos F, Thibaut R, Müller A (2019) Fungal dyes for textile applications: testing of industrial conditions for wool fabrics dyeing. J Tex I 110:61–66Google Scholar
  16. Hill D (1997) Is there a future for natural dyes? Rev Prog Color Relat Top 27:18–25CrossRefGoogle Scholar
  17. Kalinec G, Thein P, Park C, Kalinec F (2016) HEI-OC1 cells as a model for investigating drug cytotoxicity. Hear Res 335:105–117CrossRefGoogle Scholar
  18. Lee J, Kim D, Kim J, Kim P (2000) In vitro cytotoxicity tests on cultured human skin fibroblasts to predict skin irritation potential of surfactants. Toxicol In Vitro 14:345–349CrossRefGoogle Scholar
  19. Morales-Oyervides L, Oliveira J, Sousa-Gallagher M, Méndez-Zavala A, Montañez J (2017) Assessment of the dyeing properties of the pigments produced by Talaromyces spp. J Fungi 3:38CrossRefGoogle Scholar
  20. Myers R, Montgomery D, Anderson-Cook C (2009) Response surface methodology: process and product optimization using designed experiments, 3rd edn. Wiley, New JerseyGoogle Scholar
  21. Ogbonna C (2016) Production of food colourants by filamentous fungi. Afr J Microbiol Res 10:960–971CrossRefGoogle Scholar
  22. Orozco S, Kilikian B (2008) Effect of pH on citrinin and red pigments production by Monascus purpureus CCT3802. World J Microbiol Biotechnol 24:263–268CrossRefGoogle Scholar
  23. Pagano MC, Dhar P (2015) Fungal pigments: an overview. In: Gupta VK, Mach RL, Sreenivasaprad S (eds) Fungal Biomolecules. Wiley, London, pp 173–181Google Scholar
  24. Pandey N, Jain R, Pandey A, Tamta S (2018) Optimisation and characterisation of the orange pigment produced by a cold adapted strain of Penicillium sp. (GBPI_P155) isolated from mountain ecosystem. Mycology 9:81–92CrossRefGoogle Scholar
  25. Patakova P, Branska B, Patrovsky M (2017) Monascus secondary metabolites. In: Mérillon J, Ramawat K (eds) Fungal Metabolites. Springer, Switzerland, pp 821–851CrossRefGoogle Scholar
  26. Rajeswari K, Subashkumar R, Vijayaraman K (2014) Degradation of textile dyes by isolated Lysinibacillus sphaericus strain RSV-1 and Stenotrophomonas maltophilia strain RSV-2 and toxicity assessment of degraded product. J Environ Anal Toxicol 4:222Google Scholar
  27. Shah S, Shier W, Tahir N, Hameed A, Ahmad A (2014) Penicillium verruculosum SG: a source of polyketide and bioactive compounds with varying cytotoxic activities against normal and cancer lines. Arch Microbiol 196:267–278CrossRefGoogle Scholar
  28. Shukla S, Jadaun A, Arora V, Sinha R, Biyani N, Jain V (2015) In vitro toxicity assessment of chitosan oligosaccharide coated iron oxide nanoparticles. Toxicol Rep 2:27–39CrossRefGoogle Scholar
  29. Soto-Cruz O, Angel P, Rodriguez R (2008) Advance in food science and food biotechnology in developing countries. Mexican Association of Food Science, SaltilloGoogle Scholar
  30. Stanly P, Pradeep B (2013) Optimization of pigment and biomass production from Fusarium moniliforme under submerged fermentation conditions. Int J Pharm Pharm Sci 5:526–535Google Scholar
  31. Tudor D, Robinson S, Cooper P (2013) The influence of pH on pigment formation by lignicolous fungi. Int Biodeter Biodegr 80:22–28CrossRefGoogle Scholar
  32. Van der Molen K, Raja H, El-Elimat T, Oberlies N (2013) Evaluation of culture media for the production of secondary metabolites in a natural products screening program. AMB Express 3:71CrossRefGoogle Scholar
  33. Wiegand C, Hansen T, Köhnlein J, Exner I, Damisch-Pohl M, Schott P, Krühner-Wiesenberger U, Hipler U, Pohlen E (2018) Optimized protocol for the biocompatibility testing of compression stockings and similar products with close skin contact in vitro. J Tex I 109:891–902Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Vicente A. Hernández
    • 1
    • 2
    Email author
  • Ángela Machuca
    • 3
    Email author
  • Isaac Saavedra
    • 2
  • Daniel Chavez
    • 3
  • Allisson Astuya
    • 4
  • Carolina Barriga
    • 4
  1. 1.Facultad de Ciencias ForestalesUniversidad de ConcepciónConcepciónChile
  2. 2.Centro de BiotecnologíaUniversidad de ConcepciónConcepciónChile
  3. 3.Escuela de Ciencias y TecnologíaUniversidad de ConcepciónLos ÁngelesChile
  4. 4.Departamento de Oceanografía y Centro de Investigación Oceanográfica COPAS Sur-Austral, Facultad Ciencias Naturales y OceanográficasUniversidad de ConcepciónConcepciónChile

Personalised recommendations