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Yeast Diversity in the Extreme Acidic Environments of the Iberian Pyrite Belt

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Abstract

In the Iberian Pyrite Belt (IPB), acid rock drainage gives rise to aquatic habitats with low pH and high concentrations of heavy metals, a situation that causes important environmental problems. We investigated the occurrence and diversity of yeasts in two localities of the IPB: São Domingos (Portugal) and Rio Tinto (Spain). Yeast isolation was performed on conventional culture media (MYP), acidified (pH 3) media (MYP3), and on media prepared with water from the study sites (MYPw). The main goal of the study was to determine the structure of the yeast community; a combination of molecular methods was used for accurate species identifications. Our results showed that the largest fraction of the yeast community was recovered on MYPw rather than on MYP and MYP3. Twenty-seven yeast species were detected, 48% of which might represent undescribed taxa. Among these, an undescribed species of the genus Cryptococcus required low pH for growth, a property that has not been observed before in yeasts. The communities of S. Domingos and R. Tinto showed a considerable resemblance, and eight yeast species were simultaneously found in both localities. Taking into consideration the physicochemical parameters studied, we propose a hierarchic organization of the yeast community in terms of high-, intermediate-, or low-stress conditions of the environment. According to this ranking, the acidophile yeast Cryptococcus sp. 5 is considered the most tolerant species, followed by Cryptococcus sp. 3 and Lecytophora sp. Species occurring in situations of intermediate environmental stress were Candida fluviatilis, Rhodosporidium toruloides, Williopsis californica, and three unidentified yeasts belonging to Rhodotorula and Cryptococcus.

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References

  1. Abe, F, Miura, T, Nagahama, T, Inoue, A, Usami, R, Horikoshi, K, (2001) Isolation of a highly copper-tolerant yeast, Cryptococcus sp., from the Japan Trench and the induction of superoxide dismutase activity by Cu2+. Biotechnol Lett 23: 2027–2034

    Article  CAS  Google Scholar 

  2. Aksu, Z, Dönmez, G (2001) Comparison of copper (II) biosorptive properties of live and treated Candida sp. J Environ Sci Health 36: 367–381

    CAS  Google Scholar 

  3. Altschul, SF, Madden, TL, Schaffer, AA, Zhang, J, Zhang, Z, Miller, W, Lipman, DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402

    Article  PubMed  CAS  Google Scholar 

  4. Becker, S, Böger, P, Oehlmann, R, Ernst, A (2000) PCR bias in ecological analysis: a case study for quantitative Taq nuclease assays in analyses of microbial communities. Appl Environ Microbiol 66: 4945–4953

    Article  PubMed  CAS  Google Scholar 

  5. Brierley, CL, Brierley, JA, Davidson, MS (1989) Applied microbiology for metal recovery and removal from wastewater. In: Beveridge, TJ, Doyle, RJ (Eds.) Metal Ions and Bacteria. Wiley, New York, pp 359–381

    Google Scholar 

  6. Cánovas, D, Duran, C, Rodriguez, N, Amils, R, de Lorenzo, V (2003) Testing the limits of biological tolerance to arsenic in a fungus isolated from the River Tinto. Environ Microbiol 5: 133–138

    Article  PubMed  Google Scholar 

  7. Doemel, WN, Brock, TD (1971) The physiological ecology of Cyanidium caldarium. J Gen Microbiol 67: 17–32

    Google Scholar 

  8. Durán, C, Marín, I, Amils, R (1999) Specific metal sequestering acidophilic fungi. In: Amils, R, Ballester, A (Eds.) Biohydrometallurgy and the Environment, Towards the Mining of the 21st Century, Proceedings of the International Biohydrometallurgy Symposium, IBS '99. Elsevier, Amsterdam, pp 521–530

  9. Fournier, D, Lemieux, R, Couillard, D (1998) Essential interactions between Thiobacillus ferrooxidans and heterotrophic microorganisms during a wastewater sludge bioleaching process. Environ Pollut 101: 303–309

    Article  PubMed  CAS  Google Scholar 

  10. Gadanho, M, Sampaio, JP (2002) Polyphasic taxonomy of the basidiomycetous yeast genus Rhodotorula: Rh. glutinis sensu stricto and Rh. dairenensis comb. nov. FEMS Yeast Res 2: 47–58

    PubMed  CAS  Google Scholar 

  11. Gadanho, M, Sampaio, JP (2005) Microeukaryotic diversity in the extreme environments of the Iberian Pyrite Belt: a comparison between universal and fungi-specific primer sets, temperature gradient gel electrophoresis and cloning. FEMS Microbiol Ecol (in press)

  12. Gadanho, M, Sampaio, JP (2005) Occurrence and diversity of yeasts in the Mid-Atlantic Ridge hydrothermal fields near the Azores archipelago. Microb Ecol (in press)

  13. Gadanho, M, Almeida, JMGCF, Sampaio, JP (2003) Assessment of yeast diversity in a marine environment in the south of Portugal by microsatellite-primed PCR. Antonie van Leeuwenhoek 84: 217–227

    Article  PubMed  CAS  Google Scholar 

  14. González-Toril, E, Llobet-Brossa, E, Casamayor, EO, Amann, R, Amils, R (2003) Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69: 4853–4865

    Article  PubMed  Google Scholar 

  15. Goto, S, Sugiyama, J, Iizuka, H (1969) A taxonomic study of Antarctic yeasts. Mycologia 6: 748–774

    Google Scholar 

  16. Gupta, R, Ahuja, P, Khan, S, Saxena, RK, Mohapatra, H (2000) Microbial biosorbents: meeting challenges of heavy metal pollution in aqueous solutions. Curr Sci 78: 967–973

    CAS  Google Scholar 

  17. Hagler, AN, Ahearn, DG (1987) Ecology of aquatic yeasts. In: Rose, AN, Harrison, JS (Eds.) The Yeasts, vol. 2, Yeasts and the Environment. Academic Press, London, pp 181–205

    Google Scholar 

  18. Hedrick, LR (1976) Candida fluviatilis sp. nov. and other yeasts from aquatic environments. Antonie van Leeuwenhoek 42: 329–332

    Article  PubMed  CAS  Google Scholar 

  19. Herbert, RA (1992) A perspective on the biotechnological potential of extremophiles. Trends Biotechnol 10: 395–402

    Article  PubMed  CAS  Google Scholar 

  20. Huelsenbeck, JP, Ronquist, FR (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755

    Article  PubMed  CAS  Google Scholar 

  21. Kurtzman, CP (1994) Molecular taxonomy of the yeasts. Yeast 10: 1727–1740

    Article  PubMed  CAS  Google Scholar 

  22. Lachance, M-A, Starmer, WT (1998) Ecology and yeasts. In: Kurtzman, CP, Fell, JW (Eds.) The Yeasts, a Taxonomic Study, 4th edn., Elsevier, Amsterdam, pp 21–30

    Google Scholar 

  23. Larget, B, Simon, DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16: 750–759

    CAS  Google Scholar 

  24. Libkind, D, Brizzio, S, Ruffini, A, Gadanho, M, van Broock, M, Sampaio, JP (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Antonie van Leeuwenhoek 84: 313–322

    Article  PubMed  CAS  Google Scholar 

  25. López-Archilla, AI, Marin, I, Amils, R (2001) Microbial community composition and ecology of an acidic aquatic environment: the Tinto River, Spain. Microb Ecol 41: 20–35

    PubMed  Google Scholar 

  26. López-Archilla, AI, González, AE, Terrón, MC, Amils, R (2004) Ecological study of the fungal populations of the acidic Tinto River in southwestern Spain. Can J Microbiol 50: 923–934

    Article  PubMed  Google Scholar 

  27. Lozovaia, OG, Kasatkina, TP, Podgorskii, VS (2004) Search of heavy metals biosorbents among yeasts of different taxonomic groups. Mikrobiol Z 66: 92–101

    PubMed  CAS  Google Scholar 

  28. Moreira, D, López-Archilla, AI, Amils, R, Marín, I (1994) Characterization of two new thermoacidophilic microalgae: genome organization and comparison with Galdieria sulphuraria. FEMS Microbiol Lett 122: 109–114

    Article  CAS  Google Scholar 

  29. Nakagawa, T, Nagaoka, T, Taniguchi, S, Miyaji, T, Tomizuka, N (2004) Isolation and characterization of psychrophilic yeasts producing cold-adapted pectinolytic enzymes. Lett Appl Microbiol 38: 383–387

    Article  PubMed  CAS  Google Scholar 

  30. Nagahama, T, Hamamoto, M, Nakase, T, Takami, H, Horikoshi, K (2001) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. Antonie van Leeuwenhoek 80: 101–110

    Article  PubMed  CAS  Google Scholar 

  31. Nguyen, VAT, Senoo, K, Mishima, T, Hisamatsu, M (2001) Multiple tolerance of Rhodotorula glutinis R-1 to acid, aluminum ion and manganese ion, and its unusual ability of neutralizing acidic medium. J Biosci Bioeng 92: 366–371

    Article  PubMed  CAS  Google Scholar 

  32. Phaff, HJ, Starmer, WT (1987) Yeasts associated with plants, insects and soil. In: Rose, AH, Harrison, JS (Eds.) The Yeasts, vol. 1, Biology of Yeasts. Academic Press, London, pp 123–180

    Google Scholar 

  33. Podgorskii, VS, Kasatkina, TP, Lozovaia, OG (2004) Yeasts—biosorbents of heavy metals. Mikrobiol Z 66: 91–103

    PubMed  CAS  Google Scholar 

  34. Polz, MF, Cavanaugh, CM (1998) Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64: 3724–3730

    PubMed  CAS  Google Scholar 

  35. Rajapaksha, RMCP, Tobor-Kaplon, MA, Baath, E (2004) Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 70: 2966–2973

    Article  PubMed  CAS  Google Scholar 

  36. Rothschild, LJ, Mancinelli, RL (2001) Life in extreme environments. Nature 409: 1091–1101

    Article  Google Scholar 

  37. Salinas, E, Orellano, M, Rezza, I, Martinez, L, Marchesvky, E, Tossetti, M (2000) Removal of cadmium and lead from dilute aqueous solutions by Rhodotorula rubra. Bioresour Technol 72: 107–112

    Article  CAS  Google Scholar 

  38. Sampaio, JP (2004) Diversity, phylogeny and classification of basidiomycetous yeasts. In: Agerer, R, Blanz, P, Piepenbring, M (Eds.) Frontiers in Basidiomycote Mycology. IHW-Verlag, Eching, pp 49–80

    Google Scholar 

  39. Sampaio, JP, Gadanho, M, Santos, S, Duarte, F, Pais, C, Fonseca, A, Fell, JW (2001) Polyphasic taxonomy of the genus Rhodosporidium: R. kratochvilovae and related anamorphic species. Int J Syst Evol Microbiol 51: 687–697

    PubMed  CAS  Google Scholar 

  40. Sharp, RJ, Munster, MJ (1986) Biotechnological implications for microorganisms from extreme environments. In: Herbert, RA, Codd, GA (Eds.) Microbes in Extreme Environments. Academic Press, London, pp 215–295

    Google Scholar 

  41. Suzuki, MT, Giovannoni, SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62: 625–630

    PubMed  CAS  Google Scholar 

  42. Watanabe, K, Futamata, H, Harayama, S (2002) Understanding the diversity in catabolic potential of microorganisms for the development of bioremediation strategies. Antonie van Leeuwenhoek 81: 655–663

    Article  PubMed  CAS  Google Scholar 

  43. Zettler, LAA, Gómez, F, Zettler, E, Keenan, BG, Amils, R, Sogin, ML (2002) Eukaryotic diversity in Spain's river of fire. Nature 417: 137

    Article  PubMed  Google Scholar 

  44. Zettler, LAA, Messerli, MA, Laatsch, AD, Smith, PJS, Sogin, ML (2003) From genes to genomes: beyond biodiversity in Spain's Rio Tinto. Biol Bull 204: 205–209

    Google Scholar 

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Acknowledgments

M. Gadanho was supported by grant SFRH/BD/1170/2000. D. Libkind was supported by a CONICET Ph.D. fellowship and by the SETCIP-GRICES PO/PA02-BI/002 bilateral cooperation agreement.

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Authors and Affiliations

  1. Centro de Recursos Microbiológicos (CREM), Secção Autónoma de Biotecnologia (SABT), Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516, Caparica, Portugal

    Mário Gadanho & José Paulo Sampaio

  2. Laboratorio de Microbiología Aplicada y Biotecnología, Universidad Nacional del Comahue, Centro Regional Universitario Bariloche (CRUB)-CONICET (Consejo Nacional de Investigaciones Científicas y Tecnológicas), Bariloche, Río Negro, Argentina

    Diego Libkind

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  1. Mário Gadanho
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Correspondence to José Paulo Sampaio.

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Dedicated to our colleague and friend Dr. A. Madeira-Lopes who first called our attention to the fascinating microbiology of the IPB environments.

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Gadanho, M., Libkind, D. & Sampaio, J.P. Yeast Diversity in the Extreme Acidic Environments of the Iberian Pyrite Belt. Microb Ecol 52, 552–563 (2006). https://doi.org/10.1007/s00248-006-9027-y

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