Abstract
The present study was performed to screen for psychrophilic yeasts that are able to secrete cold active enzymes. Yeast isolates were obtained from environmental samples from northern Turkey and examined for enzyme production at low temperatures. The isolates which were capable of cold active enzyme production on plates were identified by molecular identification techniques. It has been found that the isolates belonged to three genera of yeasts, i.e., Rhodosporidiobolus, Cystofilobasidium and Yamadazyma. The isolates were then fermented in different media at 15 °C and the pectinase, amylase and protease activities were determined in the range of 0.76–1.73, 0.5–1.57 and 2.11–10.53 U/mL, respectively. Maximum enzyme activities were found in Yamadazyma isolates for all three enzymes. To the best of our knowledge, cold active pectinase, amylase and protease production by Yamadazyma spp. were investigated for the first time in the present study. Besides, this is the first report which indicates cold active amylase production by Cystofilobasidium capitatum and pectinase production by Rhodosporidiobolus colostri. Yeast isolates obtained in this study may have potential for industrial cold active enzyme production.
Similar content being viewed by others
References
Abrashev R, Feller G, Kostadinova N, Krumova E, Alexieva Z, Gerginova M, Spasova B, Miteva-Staleva J, Vassilev S, Angelova M (2016) Production, purification, and characterization of a novel cold-active superoxide dismutase from the Antarctic strain Aspergillus glaucus 363. Fungal Biol 120:679–689. https://doi.org/10.1016/j.funbio.2016.03.002
Alcaino J, Cifuentes V, Baeza M (2015) Physiological adaptations of yeasts living in cold environments and their potential applications. World J Microbiol Biotechnol 31:1467–1473. https://doi.org/10.1007/s11274-015-1900-8
Alias N, Ahmad Mazian M, Salleh AB, Basri M, Rahman RNZRA (2014) Molecular cloning and optimization for high level expression of cold-adapted serine protease from antarctic yeast Glaciozyma antarctica PI12. Enzyme Res. https://doi.org/10.1155/2014/197938
Anuradha K, Padma PN, Venkateshwar S, Reddy G (2010) Fungal isolates from natural pectic substrates for polygalacturonase and multienzyme production. Indian J Microbiol 50:339–344. https://doi.org/10.1007/s12088-010-0054-5
Birgisson H, Osvaldo D, Arroyo LG, Hatti-Kaul R, Mattiasson B (2003) Cold-adapted yeasts as producers of cold-active polygalacturonases. Extremophiles 7:185–193. https://doi.org/10.1007/s00792-002-0310-7
Carrasco M, Rozas JM, Barahona S, Alcaíno J, Cifuentes V, Baeza M (2012) Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiol 12:251. https://doi.org/10.1186/1471-2180-12-251
Carrasco M, Villarreal P, Barahona S, Alcaíno J, Cifuentes V, Baeza M (2016) Screening and characterization of amylase and cellulase activities in psychrotolerant yeasts. BMC Microbiol 16:21. https://doi.org/10.1186/s12866-016-0640-8
Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR (2002) Low-temperature extremophiles and their applications. Curr Opin Biotechnol 13:253–261. https://doi.org/10.1016/S0958-1669(02)00317-8
Chi Z, Ma C, Wang P, Li HF (2007) Optimization of medium and cultivation conditions for alkaline protease production by the marine yeast Aureobasidium pullulans. Bioresour Technol 98:534–538. https://doi.org/10.1016/j.biortech.2006.02.006
Ciafardini G, Zullo BA, Antonielli L, Corte L, Roscini L, Cardinali G, Williopsis B (2013) Yamadazyma terventina sp. nov., a yeast species of the Yamadazyma clade from Italian olive oils. Int J Syst Evol Microbiol 63:372–376. https://doi.org/10.1099/ijs.0.045898-0
De Gobba C, Tompa G, Otte J (2014) Bioactive peptides from caseins released by cold active proteolytic enzymes from Arsukibacterium ikkense. Food Chem 165:205–215. https://doi.org/10.1016/j.foodchem.2014.05.082
De Santi C, Leiros HKS, Di Scala A, de Pascale D, Altermark B, Willassen NP (2016) Biochemical characterization and structural analysis of a new cold-active and salt-tolerant esterase from the marine bacterium Thalassospira sp. Extremophiles 20:323–336. https://doi.org/10.1007/s00792-016-0824-z
Divya K, Padma PN (2016) Screening of diverse organic and inorganic nitrogen sources for cold-active polygalacturonase and amylase production by Geotrichum sp. using Plackett–Burman design. Int J Technol Res Eng 3:875–878
Dursun D, Dalgıç AC (2016) Optimization of astaxanthin pigment bioprocessing by four different yeast species using wheat wastes. Biocatal Agric Biotechnol 7:1–6. https://doi.org/10.1016/j.bcab.2016.04.006
França L, Sannino C, Turchetti B, Buzzini P, Margesin R (2016) Seasonal and altitudinal changes of culturable bacterial and yeast diversity in Alpine forest soils. Extremophiles 20:855–873. https://doi.org/10.1007/s00792-016-0874-2
Groenewald M, Robert V, Smith MT (2011) The value of the D1/D2 and internal transcribed spacers (ITS) domains for the identification of yeast species belonging to the genus Yamadazyma. Persoonia 26:40–46. https://doi.org/10.3767/003158511X559610
Joshi S, Satyanarayana T (2013) Biotechnology of cold-active proteases. Biology (Basel) 2:755–783. https://doi.org/10.3390/biology2020755
Kasana RC (2010) Proteases from psychrotrophs: an overview. Crit Rev Microbiol 36:134–145. https://doi.org/10.3109/10408410903485525
Khatri BP, Bhattarai T, Shrestha S, Maharjan J (2015) Alkaline thermostable pectinase enzyme from Aspergillus niger strain MCAS2 isolated from Manaslu Conservation Area, Gorkha, Nepal. Springerplus 4:488. https://doi.org/10.1186/s40064-015-1286-y
Kim EH, Cho KH, Lee YM, Yim JH, Lee HK, Cho JC, Hong SG (2010) Diversity of cold-active protease-producing bacteria from arctic terrestrial and marine environments revealed by enrichment culture. J Microbiol 48:426–432. https://doi.org/10.1007/s12275-010-0015-z
Kuddus M, Ramteke PW (2012) Recent developments in production and biotechnological applications of cold active microbial proteases. Crit Rev Microbiol 38:330–338. https://doi.org/10.1155/2013/742859
Mari E, Guerrini S, Granchi L (2016) Enumeration and rapid identification of yeasts during extraction processes of extra virgin olive oil in Tuscany. World J Microbiol Biotechnol 32:1–10. https://doi.org/10.1007/s11274-016-2049-9
Martín MC, Morata de Ambrosini VI (2013) Cold active acid pectinolytic system from psychrotolerant Bacillus: color extraction from red grape skin. J Enol Vitic 64:495–504. https://doi.org/10.5344/ajev.2013.13002
Martín MC, Morata de Ambrosini VI (2014) Effect of a cold-active pectinolytic system on colour development of Malbec red wines elaborated at low temperature. Int J Food Sci Technol 49:1893–1901. https://doi.org/10.1111/ijfs.12498
Melikoglu M, Lin CSK, Webb C (2013) Kinetic studies on the multi-enzyme solution produced via solid state fermentation of waste bread by Aspergillus awamori. Biochem Eng J 80:76–82. https://doi.org/10.1016/j.bej.2013.09.016
Merín MG, Mendoza LM, Farías ME, Morata de Ambrosini VI (2011) Isolation and selection of yeasts from wine grape ecosystem secreting cold-active pectinolytic activity. Int J Food Microbiol 147:144–148. https://doi.org/10.1016/j.ijfoodmicro.2011.04.004
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428
Mojallali L, Shahbani Zahiri H, Rajaei S, Akbari Noghabi K, Haghbeen K (2014) A novel ∼ 34-kDa α-amylase from psychrotroph Exiguobacterium sp. SH3: production, purification, and characterization. Biotechnol Appl Biochem 61:118–125. https://doi.org/10.1002/bab.1140
Naga Padma P, Anuradha K, Reddy G (2011) Pectinolytic yeast isolates for cold-active polygalacturonase production. Innov Food Sci Emerg Technol 12:178–181. https://doi.org/10.1016/j.ifset.2011.02.001
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. https://doi.org/10.1111/j.1472-765X.2004.01503.x
Nakagawa T, Nagaoka T, Miyaji T, Tomizuka N (2005) A cold-active pectin lyase from the psychrophilic and basidiomycetous yeast Cystofilobasidium capitatum strain PPY-1. Biotechnol Appl Biochem 196:193–196. https://doi.org/10.1042/ba20040190
Prasad S, Manasa P, Buddhi S, Tirunagari P, Begum Z, Rajan S, Shivaji S (2014) Diversity and bioprospective potential (cold-active enzymes) of cultivable marine bacteria from the subarctic glacial fjord, Kongsfjorden. Curr Microbiol 68:233–238. https://doi.org/10.1007/s00284-013-0467-6
Ranjan K, Lone MA, Sahay S (2016) Detergent compatible cold-active alkaline amylases from Clavispora lusitaniae CB13. J Microbiol Biotechnol Food Sci 5:306–310. https://doi.org/10.15414/jmbfs.2016.5.4.306-310
Rattanachomsri U, Tanapongpipat S, Eurwilaichitr L, Champreda V (2009) Simultaneous non-thermal saccharification of cassava pulp by multi-enzyme activity and ethanol fermentation by Candida tropicalis. J Biosci Bioeng 107:488–493. https://doi.org/10.1016/j.jbiosc.2008.12.024
Santiago M, Ramírez-Sarmiento CA, Zamora RA, Parra LP (2016) Discovery, molecular mechanisms, and industrial applications of cold-active enzymes. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01408
Schmidt M, Prieme A, Stougaard P (2007) Arsukibacterium ikkense gen. nov., sp. nov, a novel alkaliphilic, enzyme-producing gamma-proteobacterium isolated from a cold and alkaline environment in Greenland. Syst Appl Microbiol 30:197–201. https://doi.org/10.1016/j.syapm.2006.05.003
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci 109:6241–6246. https://doi.org/10.1073/pnas.1117018109
Siddiqui KS (2015) Some like it hot, some like it cold: temperature dependent biotechnological applications and improvements in extremophilic enzymes. Biotechnol Adv 33:1912–1922. https://doi.org/10.1016/j.biotechadv.2015.11.001
Singh P, Singh SM, Dhakephalkar P (2014) Diversity, cold active enzymes and adaptation strategies of bacteria inhabiting glacier cryoconite holes of High Arctic. Extremophiles 18:229–242. https://doi.org/10.1007/s00792-013-0609-6
Song Q, Wang Y, Yin C, Zhang XH (2016) LaaA, a novel high-active alkalophilic alpha-amylase from deep-sea bacterium Luteimonas abyssi XH031T. Enzyme Microb Technol 90:83–92. https://doi.org/10.1016/j.enzmictec.2016.05.003
Tsuji M, Yokota Y, Shimohara K, Kudoh S, Hoshino T (2013) An application of wastewater treatment in a cold environment and stable lipase production of antarctic basidiomycetous yeast Mrakia blollopis. PLoS ONE 8:1–7. https://doi.org/10.1371/journal.pone.0059376
Uçkun Kiran E, Trzcinski AP, Liu Y (2015) Enhancing the hydrolysis and methane production potential of mixed food waste by an effective enzymatic pretreatment. Bioresour Technol 183:47–52. https://doi.org/10.1016/j.biortech.2015.02.033
Unver Y, Yildiz M, Taskin M, Arslan NP, Ortucu S (2015) Protease production by free and immobilized cells of the cold-adapted yeast Cryptococcus victoriae CA-8. Biocatal Biotransform 33:105–110. https://doi.org/10.3109/10242422.2015.1060229
Waghmare SR, Gurav AA, Mali SA, Nadaf NH, Jadhav DB, Sonawane KD (2015) Purification and characterization of novel organic solvent tolerant 98 kDa alkaline protease from isolated Stenotrophomonas maltophilia strain SK. Protein Expr Purif 107:1–6. https://doi.org/10.1016/j.pep.2014.11.002
Yadav AN, Sachan SG, Verma P, Kaushik R, Saxena AK (2016) Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. J Basic Microbiol 56:294–307. https://doi.org/10.1002/jobm.201500230
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. da Costa.
Rights and permissions
About this article
Cite this article
Daskaya-Dikmen, C., Karbancioglu-Guler, F. & Ozcelik, B. Cold active pectinase, amylase and protease production by yeast isolates obtained from environmental samples. Extremophiles 22, 599–606 (2018). https://doi.org/10.1007/s00792-018-1020-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-018-1020-0