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Cold, pH and salt tolerant Penicillium spp. inhabit the high altitude soils in Himalaya, India

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Abstract

Twenty five fungal cultures (Penicillium spp.), isolated from soil samples from the high altitudes in the Indian Himalayan region, have been characterized following polyphasic approach. Colony morphology performed on five different media gave varying results; potato dextrose agar being the best for the vegetative growth and sporulation as well. Microscopic observations revealed 18 isolates to be biverticillate and 7 monoverticillate. Based on the phenotypic characters (colony morphology and microscopy), all the isolates were designated to the genus Penicillium. Exposure to low temperature resulted in enhanced sporulation in 23 isolates, while it ceased in case of two. The fungal isolates produced watery exudates in varying amount that in many cases increased at low temperature. All the isolates could grow between 4 and 37 °C, (optimum 24 °C), hence considered psychrotolerant. While all the isolates could tolerate pH from 2 to 14 (optimum 5–9), 7 isolates tolerated pH 1.5 as well. While all the fungal isolates tolerated salt concentration above 10 %; 10 isolates showed tolerance above 20 %. Based on ITS region (ITS1-5.8S-ITS2) analysis the fungal isolates belonged to 25 different species of Penicillium (showing similarity between 95 and 100 %). Characters like tolerance for low temperature, wide range of pH, and high salt concentration, and enhancement in sporulation and production of secondary metabolites such as watery exudates at low temperature can be attributed to the ecological resilience possessed by these fungi for survival under low temperature environment of mountain ecosystem.

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References

  • Boysen M, Borja M, del Moral C, Salazar O, Rubio V (1996) Identification at strain level of Rhizoctonia solani AG4 isolates by direct sequence of asymmetric PCR products of the ITS regions. Curr Genet 29(2):174–181

    Article  CAS  Google Scholar 

  • Cantrell SA, Dianese JC, Fell J, Gunde-Cimerman N, Zalar P (2011) Unusual fungal niches. Mycologia 103(6):1161–1174

    Article  CAS  Google Scholar 

  • Chaurasia B, Pandey A, Palni LMS (2005) Distribution, colonization and diversity of arbuscular mycorrhizal fungi in Rhododendrons of Central Himalayan region of India. For Ecol Manag 207(3):315–324

    Article  Google Scholar 

  • Cruickshank RH, Pitt JI (1987) Identification of species in Penicillium subgenus Penicillium by enzyme electrophoresis. Mycologia 79(4):614–620

    Article  Google Scholar 

  • Davolos D, Pietrangeli B, Persiani AM, Maggi O (2012) Penicillium simile sp. nov. revealed by morphological and phylogenetic analysis. Int J Syst Evol Microbiol 62:451–458

    Article  Google Scholar 

  • Dhakar K, Pandey A (2013) Laccase production from a temperature and pH tolerant fungal strain of Trametes hirsuta (MTCC 11397). Enzym Res. doi:10.1155/2013/869062

  • El Abed S, Ibnsouda SK, Latrache H, Meftah H, Tahri NJ, Hamadi F (2012) Environmental scanning electron microscopy characterization of the adhesion of conidia from Penicillium expansum to cedar wood substrata at different pH values. World J Microbiol Biotechnol 28(4):1707–1713

    Article  Google Scholar 

  • Frisvad JC, Samson RA (2004) Polyphasic taxonomy of Penicillium subgenus Penicillium: a guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol 49:1–174

    Google Scholar 

  • Frisvad JC, Larsen TO, Dalsgaard PW, Seifert KA, Louis-Seize G, Lyhne EK, Jarvis BB, Fettinger JC, Overy DP (2006) Four psychrotolerant species with high chemical diversity consistently producing cycloaspeptide A, Penicillium jamesonlandense sp. nov., Penicillium ribium sp. nov., Penicillium soppii and Penicillium lanosum. Int J Syst Evol Microbiol 56:1427–1437

    Article  CAS  Google Scholar 

  • Gawas-Sakhalkar P, Singh SM, Simantini N, Ravindra R (2012) High-temperature optima phosphatases from the cold-tolerant Arctic fungus Penicillium citrinum. Polar Res 31. doi:10.3402/polar.v31i0.11105

  • Ghildiyal A, Pandey A (2008) Isolation of cold tolerant antifungal strains of Trichoderma sp. from glacial sites of Himalayan region. Res J Microbiol 3:559–564

    Google Scholar 

  • Gunde-Cimerman N, Sonjak S, Zalar P, Frisvad JC, Diderichsen B, Plemenitas A (2003) Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity. Phys Chem Earth 28:1273–1278

    Article  Google Scholar 

  • Houbraken J, Samson RA (2011) Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Stud Mycol 70:1–51

    Article  CAS  Google Scholar 

  • Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi—current perspective. Arch Agron Soil Sci 56(1):73–98

    Article  CAS  Google Scholar 

  • Kim WK, Sang HK, Woo SK, Park MS, Paul NC, Yu SH (2007) Six species of Penicillium associate with blue mold of grape. Mycobiology 35(4):180–185

    Article  CAS  Google Scholar 

  • Kostadinova N, Krumova E, Tosi S, Pashova, Angelova M (2009) Isolation and identification of filamentous fungi from island Livingston, Antarctica. Biotechnol Biotechnol Equip 23/2009/se special edition/on-line

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9(4):299–306

    Article  CAS  Google Scholar 

  • Leitao AL (2009) Potential of Penicillium species in the bioremediation field. Int J Environ Res Public Health 6:1393–1417

    Article  CAS  Google Scholar 

  • Malviya MK, Pandey A, Trivedi P, Gupta G, Kumar B (2009) Chitinolytic activity of cold tolerant antagonistic species of Streptomyces isolated from glacial sites of Indian Himalaya. Curr Microbiol 59:502–508

    Article  CAS  Google Scholar 

  • Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361

    Article  Google Scholar 

  • Oh JY, Kim EN, Ryoo M II, Kim KD (2008) Morphological and molecular identification of Penicillium islandicum Isolate KU101 from stored rice. Plant Pathol J 24(4):469–473

    Article  CAS  Google Scholar 

  • Panda T (2011) Penicillium abundance and diversity patterns associated with cashew plantations in coastal sand dunes, Odisha, India. J Ecol Nat Environ 3(6):221–227

    Google Scholar 

  • Pandey A, Palni LMS (2007) The rhizosphere effect in the trees of the Indian Central Himalaya with special reference to altitude. Appl Ecol Environ Res 5:93–102

    Google Scholar 

  • Pandey A, Palni LMS, Bisht D (2001) Dominant fungi in the rhizosphere of established tea bushes and their interactions with the dominant bacteria under in situ conditions. Microbiol Res 156:377–382

    Article  CAS  Google Scholar 

  • Pandey A, Das N, Kumar B, Rinu K, Trivedi P (2008) Phosphate solubilization by Penicillium spp. isolated from soil samples of Indian Himalayan region. World J Microbiol Biotechnol 24:97–102

    Article  CAS  Google Scholar 

  • Pitt JI (1973) An appraisal of identification methods for Penicillium species: novel taxonomic criteria based on temperature and water relations. Mycologia 65:1135–1157

    Article  CAS  Google Scholar 

  • Ramirez C (1982) Manual and atlas of the Penicillia. Elsevier Biomedical Press, Amsterdam

    Google Scholar 

  • Raper KB, Thom C (1949) A manual of the Penicillia. The Williams and Wilkins Company, Baltimore

    Google Scholar 

  • Rinu K, Pandey A (2010) Temperature dependent phosphate solubilization by cold and pH tolerant species of Aspergillus isolated from Himalayan soil. Mycoscience 51:263–271

    Article  CAS  Google Scholar 

  • Rinu K, Pandey A (2011) Slow and steady phosphate solubilization by a psychrotolerant strain of Paecilomyces hepiali (MTCC 9621). World J Microbiol Biotechnol 27(5):1055–1062

    Article  Google Scholar 

  • Rinu K, Pandey A, Palni LMS (2012) Utilization of psychrotolerant phosphate solubilizing fungi under low temperature conditions of the mountain ecosystem. In: Satyanarayana T, Johri BN, Prakash A (eds) Microorganisms in sustainable agriculture and biotechnology. Springer Science+Business Media, Dordrecht, pp 77–90

    Chapter  Google Scholar 

  • Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Skouboe P, Frisvad JC, Taylor JW, Lauritsen D, Boysen M, Rossen L (1999) Phylogenetic analysis of nucleotide sequences from the ITS region of terverticillate Penicillium species. Mycol Res 103(7):873–881

    Article  CAS  Google Scholar 

  • Sonjak S, Frisvad JC, Gunde-Cimerman N (2006) Penicillium mycobiota in Arctic subglacial ice. Microb Ecol 52:207–216

    Article  Google Scholar 

  • Thompson JD et al (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Visagie CM, Roets F, Jacob K (2009) A new species of Penicillium, P. ramulosum sp. nov., from the natural environment. Mycologia 101(6):888–895

    Article  Google Scholar 

  • Visagie CM, Houbraken J, Rodriques C, Silva Pereira C, Dijksterhuis J, Seifert KA, Jacobs K, Samson RA (2013) Five new Penicillium species in section Sclerotiora: a tribute to the Dutch Royal family. Persoonia 31:42–62

    Article  Google Scholar 

  • Voigt K, Cigelnik E, O’Donnell K (1999) Phylogeny and PCR identification of clinically important Zygomycetes based on nuclear ribosomal-DNA sequence data. J Clin Microbiol 37:3957–3964

    CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JS, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

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Acknowledgments

Director, G. B. Pant Institute of Himalayan Environment and Development, Almora, is gratefully acknowledged for extending the facilities. Dr. Rohit Sharma (NCCS, Pune) is thanked for validating and accessioning the fungal cultures. Ministry of Environment and Forests, Govt. of India is thanked for financial support. Senior author is thankful to Indian Council of Medical Research (ICMR), Govt. of India, New Delhi, for awarding the research fellowship.

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Correspondence to Anita Pandey.

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Dhakar, K., Sharma, A. & Pandey, A. Cold, pH and salt tolerant Penicillium spp. inhabit the high altitude soils in Himalaya, India. World J Microbiol Biotechnol 30, 1315–1324 (2014). https://doi.org/10.1007/s11274-013-1545-4

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