Advertisement

Mrakia fibulata sp. nov., a psychrotolerant yeast from temperate and cold habitats

  • A. M. YurkovEmail author
  • C. Sannino
  • B. Turchetti
Original Paper

Abstract

Tree fluxes are sugar-rich, sometimes ephemeral, substrates occurring on sites where tree sap (xylem or phloem) is leaking through damages of tree bark. Tree sap infested with microorganisms has been the source of isolation of many species, including the biotechnologically relevant carotenoid yeast Phaffia rhodozyma. Tree fluxes recently sampled in Germany yielded 19 species, including several psychrophilic yeasts of the genus Mrakia. Four strains from tree fluxes represented a potential novel Mrakia species previously known from two isolates from superficial glacial melting water of Calderone Glacier (Italy). The Italian isolates, originally identified as Mrakia aquatica, and two strains from Germany did not show any sexual structures. But another culture collected in Germany produced clamped hyphae with teliospores. A detailed examination of the five isolates (three from Germany and two from Italy) proved them to be a novel yeast species, which is described in this manuscript as Mrakia fibulata sp. nov. (MB 830398), holotype DSM 103931 and isotype DBVPG 8059. In contrast to other sexually reproducing Mrakia species, M. fibulata produces true hyphae with clamp connections. Also, this is the first psychrotolerant Mrakia species which grows above 20 °C. Spring tree fluxes are widespread and can be recognized and sampled by amateurs in a Citizen Science project. This substrate is a prominent source of yeasts, and may harbor unknown species, as demonstrated in the present work. The description of Mrakia fibulata is dedicated to our volunteer helpers and amateurs, like Anna Yurkova (9-years-old daughter of Andrey Yurkov), who collected the sample which yielded the type strain of this species.

Keywords

1 new species Basidiomycete Mrakia Psychrophilic Tree fluxes 

Notes

Acknowledgements

Natalia Yurkova and Anna Yurkova are much acknowledged for assistance in sampling. Evelyne Brambilla, Gabrielle Gresenz, Carolla Plagge and Susanne Schneider (DSMZ) are acknowledged for assistance in the lab.

Author contributions

AY: Sampled, isolated and identified yeasts from spring fluxes in Germany; performed physiological tests for strains isolated in Germany; performed phylogenetic analyses; observed teleomorph and made microphotographs; wrote the manuscript. CS: Performed physiological tests for strains isolated in Italy. BT: Sampled, isolated and identified yeasts from glaciers in Italy; improved the dataset for phylogenetic analyses; wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10482_2019_1359_MOESM1_ESM.pdf (900 kb)
Supplementary material 1 (PDF 900 kb)
10482_2019_1359_MOESM2_ESM.pdf (84 kb)
Supplementary material 2 (PDF 85 kb)

References

  1. Babjeva I, Reshetova I (1998) Yeast resources in natural habitats at polar circle latitude. Food Technol Biotechnol 36:1–5Google Scholar
  2. Birgisson H, Delgado O, Arroyo LG, Hatti-Kaul R, Mattiasson B (2003) Cold-adapted yeasts as producers of cold-active polygalacturonases. Extremophiles 7:185–193PubMedCrossRefGoogle Scholar
  3. Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369PubMedCrossRefGoogle Scholar
  4. Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241PubMedCrossRefGoogle Scholar
  5. Buzzini P, Turk M, Perini L, Turchetti B, Gunde-Cimerman N (2017) Yeasts in polar and subpolar habitats. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: diversity. Springer, Berlin, pp 330–365Google Scholar
  6. Buzzini P, Turchetti B, Yurkov A (2018) Extremophilic yeasts: the toughest yeasts around? Yeast 35:487–497PubMedCrossRefGoogle Scholar
  7. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  8. De Francesco G, Sannino C, Sileoni V, Marconi O, Filippucci S, Tasselli G, Turchetti B (2018) Mrakia gelida in brewing process: an innovative production of low alcohol beer using a psychrophilic yeast strain. Food Microbiol 76:354–362PubMedCrossRefGoogle Scholar
  9. De García V, Brizzio S, Libkind D, Buzzini P, Van Broock M (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol Ecol 59:331–341PubMedCrossRefGoogle Scholar
  10. Duo Saito RD, Connell L, Rodriguez R, Redman R, Libkind D, de Garcia V (2018) Metabarcoding analysis of the fungal biodiversity associated with Castaño Overa Glacier–Mount Tronador, Patagonia, Argentina. Fungal Ecol 36:8–16CrossRefGoogle Scholar
  11. Essiamah SK (1980) Spring sap of trees. Ber Dtsch Bot Ges 93:257–267Google Scholar
  12. Fell JW (2011) Mrakia Y. Yamada & Komagata (1987). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 1503–1510CrossRefGoogle Scholar
  13. Ferreira EMS, de Sousa FMP, Rosa LH, Pimenta RS (2019) Taxonomy and richness of yeasts associated with angiosperms, bryophytes, and meltwater biofilms collected in the Antarctic Peninsula. Extremophiles 23:151–159PubMedCrossRefPubMedCentralGoogle Scholar
  14. Gardner AS, Moholdt G, Cogley JG, Wouters B, Arendt AA, Wahr J, Berthier E, Hock R, Pfeffer WT, Kaser G, Ligtenberg SR (2013) A reconciled estimate of glacier contributions to sea level rise: 2003 to 2009. Science 340:852–857PubMedCrossRefPubMedCentralGoogle Scholar
  15. Glushakova AM, Chernov IY (2004) Seasonal dynamics in a yeast population on leaves of the common wood sorrel Oxalis acetosella L. Microbiology 73:184–188CrossRefGoogle Scholar
  16. Glushakova AM, Chernov IY (2010) Seasonal dynamics of the structure of epiphytic yeast communities. Microbiology 79:830–839CrossRefGoogle Scholar
  17. Groenewald M, Lombard L, de Vries M, Lopez AG, Smith M, Crous PW (2018) Diversity of yeast species from Dutch garden soil and the description of six novel Ascomycetes. FEMS Yeast Res 18:foy076Google Scholar
  18. Grunewald K, Scheithauer J (2010) Europe’s southernmost glaciers: response and adaptation to climate change. J Glaciol 56:129–142CrossRefGoogle Scholar
  19. Hotaling S, Hood E, Hamilton TL (2017) Microbial ecology of mountain glacier ecosystems: biodiversity, ecological connections and implications of a warming climate. Environ Microbiol 19:2935–2948PubMedCrossRefPubMedCentralGoogle Scholar
  20. Kabisch J, Erl-Hoening C, Wenning M, Boehnlein C, Gareis M, Pichner R (2016) Spoilage of vacuum-packed beef by the yeast Kazachstania psychrophila. Food Microbiol 53:15–23PubMedCrossRefGoogle Scholar
  21. Kachalkin AV, Glushakova AM, Yurkov AM, Chernov IY (2008) Characterization of yeast groupings in the phyllosphere of Sphagnum mosses. Microbiology 77:474–481CrossRefGoogle Scholar
  22. Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166PubMedCrossRefGoogle Scholar
  23. Kurtzman CP, Fell JW, Boekhout T, Robert V (2011) Methods for isolation, phenotypic characterization and maintenance of yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 87–110CrossRefGoogle Scholar
  24. Lachance MA, Dobson J, Wijayanayaka DN, Smith AM (2010) The use of parsimony network analysis for the formal delineation of phylogenetic species of yeasts: Candida apicola, Candida azyma, and Candida parazyma sp. nov., cosmopolitan yeasts associated with floricolous insects. Antonie van Leeuwenhoek 97:155PubMedCrossRefGoogle Scholar
  25. Lachance MA, Wijayanayaka TM, Bundus JD, Wijayanayaka DN (2011) Ribosomal DNA sequence polymorphism and the delineation of two ascosporic yeast species: Metschnikowia agaves and Starmerella bombicola. FEMS Yeast Res 11:324–333PubMedCrossRefGoogle Scholar
  26. Maksimova IA, Chernov IY (2004) Community structure of yeast fungi in forest biogeocenoses. Microbiology 73:474–481CrossRefGoogle Scholar
  27. 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 38:383–387PubMedCrossRefGoogle Scholar
  28. NASA Global Climate Change: Arctic Sea Ice Minimum. https://climate.nasa.gov/vital-signs/arctic-sea-ice/. Accessed 25 Mar 2019
  29. Overland JE, Hanna E, Hanssen-Bauer I, Kim SJ, Walsh JE, Wang M, Bhatt US, Thoman RL (2018) Surface air temperature. In: Osborne E, Richter-Menge J, Jeffries M (eds) Arctic report card 2018, National Oceanic and Atmospheric Administration. pp 5–11Google Scholar
  30. Parkes D, Marzeion B (2018) Twentieth-century contribution to sea-level rise from uncharted glaciers. Nature 563:551–554PubMedCrossRefGoogle Scholar
  31. Péter G, Takashima M, Čadež N (2017) Yeast habitats: different but global. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: ecology. Springer, Berlin, pp 38–71Google Scholar
  32. Rämä T, Davey ML, Nordén J, Halvorsen R, Blaalid R, Mathiassen GH, Alsos IG, Kauserud H (2016) Fungi sailing the Arctic ocean: speciose communities in North Atlantic driftwood as revealed by high-throughput amplicon sequencing. Microb Ecol 72:295–304PubMedCrossRefGoogle Scholar
  33. Rime T, Hartmann M, Brunner I, Widmer F, Zeyer J, Frey B (2015) Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol Ecol 24:1091–1108PubMedCrossRefGoogle Scholar
  34. Roe GH, Baker MB, Herla F (2017) Centennial glacier retreat as categorical evidence of regional climate change. Nat Geosci 10:95–99CrossRefGoogle Scholar
  35. Sahade R, Lagger C, Torre L, Momo F, Monien P, Schloss I, Barnes DK, Servetto N, Tarantelli S, Tatián M, Zamboni N (2015) Climate change and glacier retreat drive shifts in an Antarctic benthic ecosystem. Sci Adv 1:e1500050PubMedPubMedCentralCrossRefGoogle Scholar
  36. Sannino C, Tasselli G, Filippucci S, Turchetti B, Buzzini P (2017) Yeasts in nonpolar cold habitats. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: diversity. Springer, Berlin, pp 366–396Google Scholar
  37. Santiago IF, Soares MA, Rosa CA, Rosa LH (2015) Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19:1087–1097PubMedCrossRefPubMedCentralGoogle Scholar
  38. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337CrossRefGoogle Scholar
  39. Singh SM, Tsuji M, Gawas-Sakhalker P, Loonen MJ, Hoshino T (2016) Bird feather fungi from Svalbard Arctic. Polar Biol 39:523–532CrossRefGoogle Scholar
  40. Spirin V, Malysheva V, Yurkov A, Miettinen O, Larsson KH (2018) Studies in the Phaeotremella foliacea group (Tremellomycetes, Basidiomycota). Mycol Prog 17:451–466CrossRefGoogle Scholar
  41. Sylvester K, Wang QM, James B, Mendez R, Hulfachor AB, Hittinger CT (2015) Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: a survey and the discovery of eight new yeast species. FEMS Yeast Res 15:fov002PubMedCrossRefGoogle Scholar
  42. Tasselli G, Filippucci S, Sannino C, Turchetti B, Buzzini P (2017) Cold-adapted basidiomycetous yeasts as a source of biochemicals. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, Berlin-Heidelberg, pp 555–584CrossRefGoogle Scholar
  43. Tepeeva AN, Glushakova AM, Kachalkin AV (2018a) Yeast communities of the Moscow city soils. Microbiology 87:407–415CrossRefGoogle Scholar
  44. Tepeeva AN, Glushakova AM, Kachalkin AV (2018b) The influence of heating mains on yeast communities in urban soils. Eurasian Soil Sci 51:460–466CrossRefGoogle Scholar
  45. Tsuji M, Goshima T, Matsushika A, Kudoh S, Hoshino T (2013a) Direct ethanol fermentation from lignocellulosic biomass by Antarctic basidiomycetous yeast Mrakia blollopis under a low temperature condition. Cryobiology 67:241–243PubMedCrossRefGoogle Scholar
  46. Tsuji M, Yokota Y, Shimohara K, Kudoh S, Hoshino T (2013b) An application of wastewater treatment in a cold environment and stable lipase production of antarctic basidiomycetous yeast Mrakia blollopis. PLoS ONE 8:e59376PubMedPubMedCentralCrossRefGoogle Scholar
  47. Tsuji M, Tanabe Y, Vincent WF, Uchida M (2019) Mrakia hoshinonis sp. nov., a novel psychrophilic yeast isolated from a retreating glacier on Ellesmere Island in the Canadian High Arctic. Int J Syst Evol Microbiol 69:944–948PubMedCrossRefGoogle Scholar
  48. Yurkov AM, Golubev WI (2012) Phylogenetic study of Cryptococcus laurentii mycocinogenic strains. Mycol Prog 12:777–782CrossRefGoogle Scholar
  49. Yurkov AM, Wehde T, Federici J, Schäfer AM, Ebinghaus M, Lotze-Engelhard S, Mittelbach M, Prior R, Richter C, Röhl O, Begerow D (2016) Yeast diversity and species recovery rates from beech forest soils. Mycol Prog 15:845–859CrossRefGoogle Scholar
  50. Zekollari H, Huss M, Farinotti D (2019) Modelling the future evolution of glaciers in the European Alps under the EURO-CORDEX RCM ensemble. Cryosphere 13:1125–1146CrossRefGoogle Scholar
  51. Zhang T, Wei XL, Zhang YQ, Liu HY, Yu LY (2015) Diversity and distribution of lichen-associated fungi in the Ny-Ålesund Region (Svalbard, High Arctic) as revealed by 454 pyrosequencing. Sci Rep 5:14850PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Leibniz Institute DSMZ - German Collection of Microorganisms and Cell CulturesBrunswickGermany
  2. 2.Department of Agricultural, Food and Environmental Sciences & Industrial Yeasts Collection DBVPGUniversity of PerugiaPerugiaItaly

Personalised recommendations