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Pectinolytic yeasts from cold environments: novel findings of Guehomyces pullulans, Cystofilobasidium infirmominiatum and Cryptococcus adeliensis producing pectinases

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Abstract

One hundred and three yeasts isolated from soil samples from King George Island and Tierra del Fuego province were screened in relation with their capability to produce pectinolytic enzymes. Although all the yeasts showed well-developed colonies at 20 °C, only eight showed a clear halo around the colony, indicative of pectin degradation. A secondary screening demonstrated that only four yeasts were capable to produce pectinases at low temperatures (8 °C). It could be seen that the selected yeasts were able to grow and produce high levels of polygalacturonase activity when submerged fermentations were performed using pectin-containing fruit wastes as substrates. None of the strains produced neither lyase nor rhamnogalacturonan hydrolase activities. Regarding pectin esterase activity, it was only produced in lower amounts by G. pullulans 8E (0.022 U ml−1). A TLC analysis of the substrate cleavage pattern of the pectinolytic systems was consistent with an endo-type activity. The clarification of apple juice was only accomplished by G. pullulans pectinolytic system, with a clarification of 80% (%T650) using 4 U/ml of enzyme at 20 °C. As far as we concern this work describes for the first time the production of pectinases by the cold-adapted yeasts species Cystofilobasidium infirmominiatum, Cryptococcus adeliensis and G. pullulans.

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References

  • Abe F, Minegishi H, Miura T et al (2006) Characterization of cold- and high-pressure-active polygalacturonases from a deep-sea yeast, Cryptococcus liquefaciens strain N6. Biosci Biotech Bioch 70:296–299

    Article  CAS  Google Scholar 

  • Albersheim P (1966) Pectin lyase from fungi. Methods Enzymol 8:628–631

    Article  CAS  Google Scholar 

  • Alkorta I, Garbisu C, MaJ Llama, Serra JL (1998) Industrial applications of pectic enzymes: a review. Process Biochem 33:21–28

    Article  CAS  Google Scholar 

  • Barnby FM, Morpeth FF, Pyle DL (1990) Endopolygalacturonase production from Kluyveromyces marxianus. I. Resolution, purification, and partial characterisation of the enzyme. Enzyme Microb Technol 12:891–897

    Article  CAS  Google Scholar 

  • Birgisson H, Delgado O, Garcia Arroyo L et al (2003) Cold-adapted yeasts as producers of cold-active polygalacturonases. Extremophiles 7:185–193

    CAS  PubMed  Google Scholar 

  • Blanco P, Sieiro C, Villa TG (1999) Production of pectic enzymes in yeasts. FEMS Microbiol Lett 175:1–9

    Article  CAS  PubMed  Google Scholar 

  • Branda E, Turchetti B, Diolaiuti G et al (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369

    Article  CAS  PubMed  Google Scholar 

  • Brandão LR, Libkind D, Vaz ABM et al (2011) Yeasts from an oligotrophic lake in Patagonia (Argentina): diversity, distribution and synthesis of photoprotective compounds and extracellular enzymes. FEMS Microbiol Ecol 76:1–13

    Article  PubMed  Google Scholar 

  • Brizzio S, Turchetti B, de Garcia V et al (2007) Extracellular enzymatic activities of basidiomycetous yeasts isolated from glacial and subglacial waters of northwest Patagonia (Argentina). Can J Microbiol 53:519–525

    Article  CAS  PubMed  Google Scholar 

  • Buzzini P, Martini A (2002) Extracellular enzymatic activity profiles in yeast and yeast-like strains isolated from tropical environments. J Appl Microbiol 93:1020–1025

    Article  CAS  PubMed  Google Scholar 

  • Cavalitto FS, Hours AR, Mignone FC (2000) Growth and protopectinase production of Geotrichum klebahnii in batch and continuous cultures with synthetic media. J Ind Microbiol Biotech 25:260–265

    Article  CAS  Google Scholar 

  • Christensen ET, Nielsen EJ, Kreiberg DJ et al (1998) Pectin methyl esterase from orange fruit: characterization and localization by in situ hybridization and immunohistochemistry. Planta 206:493–503

    Article  CAS  PubMed  Google Scholar 

  • Connell L, Redman R, Craig S et al (2008) Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microb Ecol 56:448–459

    Article  CAS  PubMed  Google Scholar 

  • Contreras Esquivel JC, Voget CE (2004) Purification and partial characterization of an acidic polygalacturonase from Aspergillus kawachii. J Biotechnol 110:21–28

    Article  CAS  PubMed  Google Scholar 

  • de García V, Brizzio S, Libkind D et al (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol Ecol 59:331–341

    Article  PubMed  Google Scholar 

  • DePriest T, Ivanova N, Fahselt D et al (2002) Sequences of psychrophilic fungi amplified from glacier-preserved ascolichens. Can J Bot 78:1450–1459

    Google Scholar 

  • Dey TB, Banerjee R (2014) Application of decolourized and partially purified polygalacturonase and α-amylase in apple juice clarification. Braz J Microbiol 45:97–104

    Article  PubMed  PubMed Central  Google Scholar 

  • Fell JW, Hunter IL (1968) Isolation of heterothallic yeast strains of Metschnikowia kamienski and their mating reactions with Chlamydozyma wickerham spp. Antonie Van Leeuwenhoek 34:365–376

    Article  CAS  PubMed  Google Scholar 

  • García-Carreño FL, Dimes LE, Haard NF (1993) Substrate-gel electrophoresis for composition and molecular weight of proteinases or proteinaceous proteinase inhibitors. Anal Biochem 214:65–69

    Article  PubMed  Google Scholar 

  • Gunde-Cimerman N, Butinar L, Sonjak S et al. (2005) Halotolerant and halophilic fungi from coastal environments in the Arctics. In: Gunde-Cimerman N, Oren O, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya, Springer, pp 397–423

  • Hoondal G, Tiwari R, Tewari R et al (2002) Microbial alkaline pectinases and their industrial applications: a review. Appl Microbiol Biotech 59:409–418

    Article  CAS  Google Scholar 

  • Kutty SN, Philip R (2008) Marine yeasts—a review. Yeast 25:465–483

    Article  CAS  PubMed  Google Scholar 

  • Margesin R, Fauster V, Fonteyne PA (2005) Characterization of cold-active pectate lyases from psychrophilic Mrakia frigida. Lett Appl Microbiol 40:453–459

    Article  CAS  PubMed  Google Scholar 

  • Martinez A, Cavello I, Garmendia G et al (2016) Yeasts from sub-Antarctic region: biodiversity, enzymatic activities and their potential as oleaginous microorganisms. Extremophiles 20:759–769

    Article  CAS  PubMed  Google Scholar 

  • Merín MG, Morata de Ambrosini VI (2015) Highly cold-active pectinases under wine-like conditions from non-Saccharomyces yeasts for enzymatic production during winemaking. Lett Appl Microbiol 60:467–474

    Article  PubMed  Google Scholar 

  • Morgan-Kiss RM, Priscu JC, Pocock T et al (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa T, Kaichiro Y, Tatsuro M, Noboru T (2002) Cold-active pectinolytic activity of psychrophilic-basidiomycetous yeast Cystofilobasidium capitatum strain PPY-1. J Biosci Bioeng 94:175–177

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa T, Nagaoka T, Miyaji T, Tomizuka N (2005) Cold-active polygalacturonase from psychrophilic-basidiomycetous yeast Cystofilobasidium capitatum strain PPY-1. Biosci Biotech Bioch 69:419–421

    Article  CAS  Google Scholar 

  • Nakkeeran E, Umesh-Kumar S, Subramanian R (2011) Aspergillus carbonarius polygalacturonases purified by integrated membrane process and affinity precipitation for apple juice production. Biores Technol 102:3293–3297

    Article  CAS  Google Scholar 

  • Normand J, Ralet MC, Thibault JF et al (2010) Purification, characterization, and mode of action of a rhamnogalacturonan hydrolase from Irpex lacteus, tolerant to an acetylated substrate. Appl Microbiol Biotech 86:577–588

    Article  CAS  Google Scholar 

  • Pedrolli DB, Gomes E, Monti R, Carmona EC (2008) Studies on productivity and characterization of polygalacturonase from Aspergillus giganteus submerged culture using citrus pectin and orange waste. Appl Biochem Biotech 144:191–200

    Article  CAS  Google Scholar 

  • Sakai T, Sakamoto T, Hallaert J, Vandamme EJ (1993) Pectin, pectinase, and protopectinase: production, properties, and applications. Adv Appl Microbiol 39:213–294

    Article  CAS  PubMed  Google Scholar 

  • Sampaoi JP (2011) Cystofilobasidium Oberwinkler & Bandoni (1983). Fifth: 1429–1430

  • Sandri IG, Fontana RC, Barfknecht DM, da Silveira MM (2011) Clarification of fruit juices by fungal pectinases. LWT-Food Sci Technol 44:2217–2222

    Article  CAS  Google Scholar 

  • Slavikova E, Kosikova B, Mikulasova M (2002) Biotransformation of waste lignin products by the soil-inhabiting yeast Trichosporon pullulans. Can J Microbiol 48:200–203

    Article  CAS  PubMed  Google Scholar 

  • Sunnotel O, Nigam P (2002) Pectinolytic activity of bacteria isolated from soil and two fungal strains during submerged fermentation. World J Microbiol Biotechnol 18:835–839

    Article  CAS  Google Scholar 

  • Vaz ABM, Rosa LH, Vieira MLA et al (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 42:937–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vishniac HS (2005) Yeast biodiversity in the Antarctic. In: Peter G, Rosa C (eds) Biodiversity and ecophysiology of yeasts. Springer, pp 419–440

  • Whitaker JR (1984) Pectic substances, pectic enzymes and haze formation in fruit juices. Enzyme Microb Technol 6:341–349

    Article  CAS  Google Scholar 

  • Yukimura K, Nakai R, Kohshima S et al (2009) Spore-forming halophilic bacteria isolated from Arctic terrains: implications for long-range transportation of microorganisms. Polar Sci 3:163–169

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 112-201101-00662) and Agencia Nacional de Promoción Científica y Tecnológica (PICT 2014-1655).

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Correspondence to Ivana Cavello.

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Communicated by A. Driessen.

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Supplementary Fig. 1. Polygalacturonase activity against different pectic substrates (TIFF 88 kb)

792_2016_904_MOESM2_ESM.tif

Supplementary Fig. 2. Effect of carbon sources on PGase production. PGase activity (U/ml) produced in a culture medium containing 10 g l−1 citrus pectin (dark gray color box), 5 g l−1 glucose and 0.5 g l−1 citrus pectin (light gray color box) and 10 g l−1 glucose (medium gray color box) (TIFF 71 kb)

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Cavello, I., Albanesi, A., Fratebianchi, D. et al. Pectinolytic yeasts from cold environments: novel findings of Guehomyces pullulans, Cystofilobasidium infirmominiatum and Cryptococcus adeliensis producing pectinases. Extremophiles 21, 319–329 (2017). https://doi.org/10.1007/s00792-016-0904-0

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  • DOI: https://doi.org/10.1007/s00792-016-0904-0

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