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Unraveling the decolourizing ability of yeast isolates from dye-polluted and virgin environments: an ecological and taxonomical overview

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Abstract

Microcosm assays with dye-amended culture media under a shot-feeding strategy allowed us to obtain 100 yeast isolates from the wastewater outfall channel of a dyeing textile factory in Tucumán (Argentina). Meanwhile, 63 yeast isolates were obtained from Phoebe porphyria (Laurel del monte) samples collected from Las Yungas rainforest (Tucumán), via a classical isolation scheme. Isolated yeasts, both from dye-polluted and virgin environments, were compared for their textile dye decolourization ability when cultured on solid and liquid media. Nine isolates from wastewater and 17 from Las Yungas showed the highest decolourization potential on agar plates containing six different reactive dyes, either alone or as a mixture. Five yeasts from each environment were further selected on the basis of their high dye removal rate in Vilmafix® Red 7B-HE- or Vilmafix® Blue RR-BB-amended liquid cultures. Yeasts from wastewater showed slightly higher decolourization percentages after 36 h of culture than yeasts from Las Yungas (98–100% vs. 91–95%, respectively). However, isolates from Las Yungas exhibited higher specific decolourization rates than isolates from effluents (1.8–3.0 vs. 0.9–1.3 mg g−1h−1, respectively). All selected isolates were first grouped according to microsatellite-PCR analysis and representative isolates from each group were subsequently identified based on the 26S rRNA gene sequence analysis. Yeasts from wastewater were identified as the ascomycetous Pichia kudriavzevii (100%) and closely related to Candida sorbophila (99.8%), whilst yeasts from Las Yungas were identified as the basidiomycetous Trichosporon akiyoshidainum and Trichosporon multisporum. It is suggested that findings concerning yeast selection during screening programs for dye-decolourizing yeasts may be explained in the light of the copiotroph-oligotroph microorganisms rationale.

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Abbreviations

WRF:

White rot fungi

NDM:

Normal decolourization medium

HAU:

Halo arbitrary units

CDAU:

Colony dying arbitrary units

LiP:

Lignin peroxidase

Lacc:

Laccase

MnP:

Manganese dependent peroxidase

ABTS:

2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid)

TMPD:

N,N,N′,N′-tetramethyl-p-phenylenediamine

YCB:

Yeast carbon base

YNB:

Yeast nitrogen base

References

  • Aksu Z (2003) Reactive dye bioaccumulation by Saccharomyces cerevisiae. Process Biochem 38:1437–1444

    Article  CAS  Google Scholar 

  • Aksu Z (2005) Application of biosorption for the removal of organic pollutants: a review. Process Biochem 40:997–1026

    Article  CAS  Google Scholar 

  • Aksu Z, Dönmez G (2003) A comparative study on the biosorption characteristics of some yeasts for Remazol Blue reactive dye. Chemosphere 50:1075–1083

    Article  CAS  PubMed  Google Scholar 

  • Assas N, Marouani L, Hamdi M (2000) Scale down and optimization of olive mill wastewaters decolourization by Geotrichum candidum. Bioprocess Biosyst Eng 22:503–507

    CAS  Google Scholar 

  • Barrasa J, Martínez A, Martínez M (2009) Isolation and selection of novel basidiomycetes for decolourization of recalcitrant dyes. Folia Microbiol 54:59–66

    Article  CAS  Google Scholar 

  • Chamarro E, Marco A, Esplugas S (2001) Use of fenton reagent to improve organic chemical biodegradability. Water Res 35:1047–1051

    Article  CAS  PubMed  Google Scholar 

  • Chander M, Arora DS (2007) Evaluation of some white-rot fungi for their potential to decolourise industrial dyes. Dyes Pigm 72:192–198

    Article  CAS  Google Scholar 

  • de Figueroa LIC, Martínez MA, Spencer JFT (2004) Yeasts: ecology in Northwest Argentina

  • de Vrind-de Jong EW, Corstjens PLAM, Kempers ES, Westbroek P, de Vrind JPM (1990) Oxidation of manganese and iron by Leptothrix discophora: use of N,N,N′,N′-tetramethyl-p-phenylenediamine as an indicator of metal oxidation. Appl Environ Microbiol 56:3458–3462

    PubMed  Google Scholar 

  • Dönmez G (2002) Bioaccumulation of the reactive textile dyes by Candida tropicalis growing in molasses medium. Enzyme Microb Technol 30:363–366

    Article  Google Scholar 

  • Ertugrul S, San NO, Dönmez G (2009) Treatment of dye (Remazol Blue) and heavy metals using yeast cells with the purpose of managing polluted textile wastewaters. Ecol Eng 35:128–134

    Article  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • Jadhav JP, Parshetti GK, Kalme SD, Govindwar SP (2007) Decolourization of azo dye methyl red by Saccharomyces cerevisiae MTCC 463. Chemosphere 68:394–400

    Article  CAS  PubMed  Google Scholar 

  • Jarosz-Wilkołazka A, Kochmanska-Rdest J, Malarczyk E, Wardas W, Leonowicz A (2002) Fungi and their ability to decolourize azo and anthraquinonic dyes. Enzyme Microb Technol 30:566–572

    Article  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Kaushik P, Malik A (2009) Fungal dye decolourization: recent advances and future potential. Environ Int 35:127–141

    Article  CAS  PubMed  Google Scholar 

  • Kurtzman CP, Robnett CJ (1997) Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5′ end of the large-subunit (26S) ribosomal DNA gene. J Clin Microbiol 35:1216–1223

    CAS  PubMed  Google Scholar 

  • Kurtzman CP, Robnett CJ, Basehoar-Powers E (2008) Phylogenetic relationships among species of Pichia, Issatchenkia and Williopsis determined from multigene sequence analysis, and the proposal of Barnettozyma gen. nov., Lindnera gen. nov. and Wickerhamomyces gen. nov. FEMS Yeast Res 8:939–954

    Article  CAS  PubMed  Google Scholar 

  • Lucas MS, Amaral C, Sampaio A, Peres JA, Dias AA (2006) Biodegradation of the diazo dye Reactive Black 5 by a wild isolate of Candida oleophila. Enzyme Microb Technol 39:51–55

    Article  CAS  Google Scholar 

  • MacGillivray AR, Shiaris MP (1993) Biotransformation of polycyclic aromatic hydrocarbons by yeasts isolated from coastal sediments. Appl Environ Microbiol 59:1613–1618

    CAS  PubMed  Google Scholar 

  • Martins MAM, Cardoso MH, Queiroz MJ, Ramalho MT, Campus AMO (1999) Biodegradation of azo dyes by the yeast Candida zeylanoides in batch aerated cultures. Chemosphere 38:2455–2460

    Article  CAS  PubMed  Google Scholar 

  • Máximo C, Pessoa Amorim MT, Costa-Ferreira M (2003) Biotransformation of industrial reactive azo dyes by Geotrichum sp. CCMI 1019. Enzyme Microb Technol 32:145–151

    Article  Google Scholar 

  • Meehan C, Banat IM, McMullan G, Nigam P, Smyth F, Marchant R (2000) Decolourization of Remazol Black-B using a thermotolerant yeast, Kluyveromyces marxianus IMB3. Environ Int 26:75–79

    Article  CAS  PubMed  Google Scholar 

  • Middelhoven WJ (1997) Assimilation of organic acids: the pH as determining factor. Yeast 46:18–19

    Google Scholar 

  • O’Neill C, Hawkes FR, Hawkes DL, Lourenço ND, Pinheiro HM, Deleé W (1999) Colour in textile effluents—sources, measurement, discharge consents and simulation: a review. J Chem Technol Biotechnol 74:1009–1018

    Article  Google Scholar 

  • Oren A, Guverich P, Henys Y (1991) Reduction of nitrosubstituted aromatic compounds by the halophilic anaerobic eubacteria Haloanaerobium praevalens and Sporohalobacter marismortui. Appl Environ Microbiol 57:3367–3370

    CAS  PubMed  Google Scholar 

  • Pajot HF, Figueroa LIC, Fariña JI (2007) Dye-decolourizing activity in isolated yeasts from the ecoregion of Las Yungas (Tucumán, Argentina). Enzyme Microb Technol 40:1503–1511

    Article  CAS  Google Scholar 

  • Pajot HF, Figueroa LIC, Spencer JF, Fariña JI (2008) Phenotypical and genetic characterization of Trichosporon sp. HP-2023. A yeast isolate from Las Yungas rainforest (Tucumán, Argentina) with dye-decolourizing ability. Antonie van Leeuwenhoek 94:233–244

    Article  PubMed  Google Scholar 

  • Pearce CI, Lloyd JR, Guthrie JT (2003) The removal of colour from textile wastewater using whole bacterial cells: a review. Dyes Pigm 58:179–196

    Article  CAS  Google Scholar 

  • Ramalho PA, Scholze H, Cardoso MH, Ramalho MT, Oliveira-Campos AM (2002) Improved conditions for the aerobic reductive decolourisation of azo dyes by Candida zeylanoides. Enzyme Microb Technol 31:848–854

    Article  CAS  Google Scholar 

  • Ramalho PA, Cardoso MH, Cavaco-Paulo A, Ramalho MT (2004) Characterization of azo reduction activity in a novel ascomycete yeast strain. Appl Environ Microbiol 70:2279–2288

    Article  CAS  PubMed  Google Scholar 

  • Ramalho PA, Paiva S, Cavaco-Paulo A, Casal M, Cardoso MH, Ramalho MT (2005) Azo reductase activity of intact Saccharomyces cerevisiae cells is dependent on the Fre1p component of plasma membrane ferric reductase. Appl Environ Microbiol 71:3882–3888

    Article  CAS  PubMed  Google Scholar 

  • Raspor P, Zupan J (2006) Yeasts in extreme environments. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 371–417

    Chapter  Google Scholar 

  • Reznick D, Bryant MJ, Bashey F (2002) r-and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83:1509–1520

    Google Scholar 

  • Rodrigues MG, Fonseca A (2003) Molecular systematics of the dimorphic ascomycete genus Taphrina. Int J Syst Evol Microbiol 53:607–616

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Saratale RG, Saratale GD, Chang JS, Govindwar SP (2009) Decolorization and biodegradation of textile dye Navy blue HER by Trichosporon beigelii NCIM-3326. J Hazard Mater 166:1421–1428

    Article  CAS  PubMed  Google Scholar 

  • Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tate R (2000) Soil microbiology, 2nd edn. John Wiley, New York

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Tien M, Kirk TK (1984) Lignin-degrading enzyme from Phanerochaete chrysosporium: purification, characterization and catalytic properties of a unique H2O2-requiring oxygenase. Proc Natl Acad Sci USA 81:2280–2284

    Article  CAS  PubMed  Google Scholar 

  • Villas-Bôas SG, Esposito E, Mendonça MM (2002) Novel lignocellulolytic ability of Candida utilis during solid-substrate cultivation on apple pomace. World J Microbiol Biotechnol 18:541–545

    Article  Google Scholar 

  • Wesenberg D, Kyriakides I, Agathos SN (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Yang M, Pritsch K, Yediler A, Hagn A, Schloter M, Kettrup A (2003) Decolourization of synthetic dyes and production of manganese-dependent peroxidase by new fungal isolates. Biotechnol Lett 25:709–713

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Yediler A, Yang M, Kettrup A (2005) Decolourization of an azo dye, Reactive Black 5 and MnP production by yeast isolate: Debaryomyces polymorphus. Biochem Eng J 24:249–253

    Article  CAS  Google Scholar 

  • Yang Q, Tao L, Yang M, Zhang H (2008) Effects of glucose on the decolourization of Reactive Black 5 by yeast isolates. J Environ Sci 20:105–108

    Article  Google Scholar 

  • Yarrow D (1998) Methods for the isolation, maintenance and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts. Elsevier Science B.V., Amsterdam, pp 77–100

    Chapter  Google Scholar 

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Acknowledgments

Thanks are due to Dr. W. J. Middelhoven for advice concerning Trichosporon identification. This work was supported by Agencia Nacional de Promoción Científica y Tecnológica-FONCYT (PICT2003-14496), Consejo Nacional de Investigaciones Científicas y Técnicas, CONICET (PIP 6202), and Consejo de Investigaciones de la Universidad Nacional de Tucumán, CIUNT (D-311).

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Authors and Affiliations

  1. PROIMI – CONICET (Planta Piloto de Procesos Industriales Microbiológicos), Av. Belgrano y Caseros, T4001MVB, Tucumán, Argentina

    Hipólito F. Pajot, Osvaldo D. Delgado, Lucía I. C. de Figueroa & Julia I. Fariña

  2. Cátedra de Microbiología Superior, Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán, Tucumán, Argentina

    Lucía I. C. de Figueroa

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  1. Hipólito F. Pajot
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  2. Osvaldo D. Delgado
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  3. Lucía I. C. de Figueroa
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  4. Julia I. Fariña
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Correspondence to Hipólito F. Pajot.

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Pajot, H.F., Delgado, O.D., de Figueroa, L.I.C. et al. Unraveling the decolourizing ability of yeast isolates from dye-polluted and virgin environments: an ecological and taxonomical overview. Antonie van Leeuwenhoek 99, 443–456 (2011). https://doi.org/10.1007/s10482-010-9495-4

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