1887

Abstract

Two novel yeast species were isolated from the guts of two different termite species. A new member of the genus Sugiyamaella was isolated from the hindgut and nest material of the lower Australian termite Mastotermes darwiniensis. The second novel yeast species, isolated from the higher termite Odontotermes obesus, was identified as a member of the genus Papiliotrema. Both yeast species were able to hydrolyse xylan, methylumbelliferyl β-xylobiose and methylumbelliferyl β-xylotriose. The ability to debranch different hemicellulose side chains and growth without the addition of external vitamins was observed. A symbiotic role of the novel yeast species is indicated, especially in respect to xylan degradation and the production of vitamins. Here, we describe these species as Sugiyamaella mastotermitis sp. nov., MycoBank 816574 (type strain MD39V=DSM 100793=CBS 14182), and Papiliotrema odontotermitis f.a., sp. nov., MycoBank 816575 (type strain OO5=DSM 100791=CBS 14181). Additionally, we transfer Candida qingdaonensis to the genus Sugiyamaella and propose the following combination: Sugiyamaella qingdaonensis f.a., comb. nov., MycoBank 816576.

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2016-11-01
2019-10-21
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References

  1. Akhtar M. S., Rashid M. I..( 2001;). Studies on population density and diversity of termites of district Bahawalnagar. . J Res Sci12:116–122.
    [Google Scholar]
  2. Brune A..( 2014;). Symbiotic digestion of lignocellulose in termite guts. . Nat Rev Microbiol12:168–180. [CrossRef][PubMed]
    [Google Scholar]
  3. Castresana J..( 2000;). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. . Mol Biol Evol17:540–552. [CrossRef][PubMed]
    [Google Scholar]
  4. Christ E., Kowalczyk M., Zuchowska M., Claus H., Löwenstein R., Szopinska-Morawska A., Renaut J., König H..( 2015;). An exemplary model study for overcoming stuck fermentation during spontaneous fermentation with the aid of a Saccharomyces triple hybrid. . J Agr Sci7:18–34. [CrossRef]
    [Google Scholar]
  5. Daniel H.-M., Lachance M.-A., Kurtzman C. P..( 2014;). On the reclassification of species assigned to Candida and other anamorphic ascomycetous yeast genera based on phylogenetic circumscription. . Antonie van Leeuwenhoek106:67–84. [CrossRef][PubMed]
    [Google Scholar]
  6. Deák T..( 2008;). Handbook of Food Spoilage Yeasts, , 2nd edn., Boca Raton, FL:: CRC Press;.
    [Google Scholar]
  7. Ferreira-Paim K., Ferreira T. B., Andrade-Silva L., Mora D. J., Springer D. J., Heitman J., Fonseca F. M., Matos D., Melhem M. S., Silva-Vergara M. L..( 2014;). Phylogenetic analysis of phenotypically characterized Cryptococcus laurentii isolates reveals high frequency of cryptic species. . PLoS One9:e108633. [CrossRef][PubMed]
    [Google Scholar]
  8. Fröhlich J., König H..( 2008;). Micromanipulation and identification of single microbial cells. . In Molecular Microbial Ecology Manual, pp. 1823–1837. Edited by Kowalchuk G. A., Akkermans A. D., Head I. M., de Bruijn F. J., van Elsas J. D.. Heidelberg:: Springer;.[CrossRef]
    [Google Scholar]
  9. Ganter P. F..( 2006;). Yeast and invertebrate associations. . In Biodiversity and Ecophysiology of Yeasts, pp. 303–370. Edited by Rosa C., Gábor P.. Heidelberg:: Springer;.[CrossRef]
    [Google Scholar]
  10. Hagler A. N., Ahearn D. G..( 1981;). Rapid diazonium blue B test to detect basidiomycetous yeasts. . Int J Syst Bacteriol31:204–208. [CrossRef]
    [Google Scholar]
  11. Handel S., König H..( 2016;). Wide distribution of symbiotic yeasts in the gut of lower and higher termites and in a wood-feeding cockroach. . J Appl Entomol. submitted.
    [Google Scholar]
  12. Houseknecht J. L., Hart E. L., Suh S.-O., Zhou J. J..( 2011;). Yeasts in the Sugiyamaella clade associated with wood-ingesting beetles and the proposal of Candida bullrunensis sp. nov. . Int J Syst Evol Microbiol61:1751–1756. [CrossRef][PubMed]
    [Google Scholar]
  13. Kambhampati S., Peterson A..( 2007;). Ecological niche conservation and differentiation in the wood-feeding cockroaches, Cryptocercus, in the United States. . Biol J Linn Soc90:457–466. [CrossRef]
    [Google Scholar]
  14. Katoh K., Standley D. M..( 2013;). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. . Mol Biol Evol30:772–780. [CrossRef][PubMed]
    [Google Scholar]
  15. Krishna K., Weesner F. M..( 1970;). Biology of Termites: Volume II, , 1st edn.. New York:: Academic Press;.
    [Google Scholar]
  16. Kuhnigk T., Borst E.-M., Ritter A., Kämpfer P., Graf A., Hertel H., König H..( 1994;). Degradation of lignin monomers by the hindgut flora of xylophagous termites. . System Appl Microbiol17:76–85. [CrossRef]
    [Google Scholar]
  17. Kurtzman C. P..( 2007;). Eleven new species of Sugiyamaella and Candida from forest habitats. . FEMS Yeast Res7:1046–1063. [CrossRef][PubMed]
    [Google Scholar]
  18. Kurtzman C. P., Robnett C. J..( 2003;). Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. . FEMS Yeast Res3:417–432. [CrossRef][PubMed]
    [Google Scholar]
  19. Kurtzman C. P., Robnett C. J..( 1998;). Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. . Antonie van Leeuw J Microb73:331–371.[CrossRef]
    [Google Scholar]
  20. König H., Varma A..( 2006;). Intestinal Microorganisms of Termites and Other Invertebrates, , 1st edn.. Heidelberg:: Springer;.[CrossRef]
    [Google Scholar]
  21. König H., Fröhlich J., Li L., Wenzel M., Dröge S., Breunig A., Pfeiffer P., Radek R., Brugerolle G..( 2007;). The flagellates of the Australian termite Mastotermes darwiniensis: Identification of their symbiotic bacteria and cellulases. . Symbiosis44:51–65.
    [Google Scholar]
  22. König H., Li L., Fröhlich J..( 2013;). The cellulolytic system of the termite gut. . Appl Microbiol Biotechnol97:7943–7962. [CrossRef][PubMed]
    [Google Scholar]
  23. Liu X.-Z., Wang Q.-M., Göker M., Groenewald M., Kachalkin A. V., Lumbsch H. T., Millanes A. M., Wedin M., Yurkov A. M. et al..( 2015;). Towards an integrated phylogenetic classification of the Tremellomycetes. . Stud Mycol81:85–147. [CrossRef][PubMed]
    [Google Scholar]
  24. Manzoor F., Akhtar M. S..( 2006;). Morphometric analysis of population samples of soldier caste of Odontotermes obesus (Rambur) (Isoptera, Termitidae, Macrotermtinae). . Anim Biodivers Conserv29:91–107.
    [Google Scholar]
  25. Molnar O., Schatzmayr G., Fuchs E., Prillinger H..( 2004;). Trichosporon mycotoxinivorans sp. nov., a new yeast species useful in biological detoxification of various mycotoxins. . Syst Appl Microbiol27:661–671. [CrossRef][PubMed]
    [Google Scholar]
  26. Morais C. G., Lara C. A., Marques S., Fonseca C., Lachance M.-A., Rosa C. A..( 2013;). Sugiyamaella xylanicola sp. nov., a xylan-degrading yeast species isolated from rotting wood. . Int J Syst Evol Microbiol63:2356–2360. [CrossRef][PubMed]
    [Google Scholar]
  27. Nageswara Rao A., Samatha C., Sammaiah C..( 2012;). Bio-diversity of termites in Bhadrachalam forest region, Khammam district, Andhra Pradesh. . J Biodiversity3:55–59.
    [Google Scholar]
  28. Ni J., Tokuda G..( 2013;). Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. . Biotechnol Adv31:838–850. [CrossRef][PubMed]
    [Google Scholar]
  29. O’Donnel K..( 1993;). Fusarium and its near relatives. . In The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics, pp. 223–225. Edited by Reynolds D. R., Taylor J. W.. Wallingford, UK:: CAB International;.
    [Google Scholar]
  30. Pfeiffer P., Radler F..( 1985;). High performance liquid chromatographic determination of organic acids, sugars, glycerin and alcohol in wine on a cation exchange resin. . Z Lebensm Unters Forsch181:24–27.[PubMed][CrossRef]
    [Google Scholar]
  31. Prillinger H., Messner R., König H., Bauer R., Lopandic K., Molnar O., Dangel P., Weigang F., Kirisits T. et al.( 1996;). Yeasts associated with termites: a phenotypic and genotypic characterization and use of coevolution for dating evolutionary radiations in asco- and basidiomycetes. . System Appl Microbiol19:265–283. [CrossRef]
    [Google Scholar]
  32. Raspor P., Zupan J..( 2006;). Yeasts in extreme environments. . In Biodiversity and Ecophysiology of Yeasts, pp. 371–418. Edited by Rosa C., Gábor P.. Heidelberg:: Springer;.[CrossRef]
    [Google Scholar]
  33. Roonwal M. L., Bose G..( 1978;). Vegetational distribution of termites of Rajasthan (India) and their economic importance. . Proc Indian natn Sci Acad.44: Part B, 320–329.
    [Google Scholar]
  34. Saluja P., Prasad G. S..( 2007;). Cryptococcus rajasthanensis sp. nov., an anamorphic yeast species related to Cryptococcus laurentii, isolated from Rajasthan, India. . Int J Syst Evol Microbiol57:414–418. [CrossRef][PubMed]
    [Google Scholar]
  35. Schweigkofler W., Suzuki M., Lopandic K., Prillinger H..( 2000;). Galactocandida mastotermitis and G. reticulitermitis: two new ascomycetous yeast species associated with termites. . Programs, Abstracts and Papers: 3rd Int. Congr. Symbiosis, Marburg, Germany, 186.
  36. Schäfer A., Konrad R., Kuhnigk T., Kämpfer P., Hertel H., König H..( 1996;). Hemicellulose-degrading bacteria and yeasts from the termite gut. . J Appl Bacteriol80:471–478. [CrossRef][PubMed]
    [Google Scholar]
  37. Silvestro D., Michalak I..( 2012;). raxmlGUI: a graphical front-end for RAxML. . Org Divers Evol12:335–337. [CrossRef]
    [Google Scholar]
  38. Stamatakis A., Hoover P., Rougemont J..( 2008;). A rapid bootstrap algorithm for the RAxML Web servers. . Syst Biol57:758–771. [CrossRef][PubMed]
    [Google Scholar]
  39. Urbina H., Frank R., Blackwell M..( 2013;). Scheffersomyces cryptocercus: a new xylose-fermenting yeast associated with the gut of wood roaches and new combinations in the Sugiyamaella yeast clade. . Mycologia105:650–660. [CrossRef][PubMed]
    [Google Scholar]
  40. Vega F. E., Dowd P. E..( 2005;). The role of yeast as insect endosymbionts. . In Insect-Fungal Associations: Ecology and Evolution, pp. 211–243. Edited by Vega F. E., Blackwell M.. New York:: Oxford University Press;.
    [Google Scholar]
  41. Vogel H. J..( 1956;). A convenient medium for Neurospora (medium N). . Microbial Genet Bull13:42–43.
    [Google Scholar]
  42. Wang S.-A., Li F.-L., Bai F.-Y..( 2010;). Candida laoshanensis sp. nov. and Candida qingdaonensis sp. nov., anamorphic, ascomycetous yeast species isolated from decayed wood. . Int J Syst Evol Microbiol60:1697–1701. [CrossRef][PubMed]
    [Google Scholar]
  43. White T. J., Bruns T., Lee S., Taylor J..( 1990;). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. . In PCR Protocols: A Guide to Methods and Applications, pp. 315–322. Edited by Innis M., White T., Sninsky J. J.. San Diego:: Academic Press Inc;.
    [Google Scholar]
  44. Wickerham L. J..( 1951;). Taxonomy of yeasts. . Tech Bull U. S. Dep Agric1029:1–56.
    [Google Scholar]
  45. Yurkov A., Guerreiro M. A., Sharma L., Carvalho C., Fonseca Á..( 2015;). Correction: Multigene assessment of the species boundaries and sexual status of the basidiomycetous yeasts Cryptococcus flavescens and C. terrestris (Tremellales). . PLoS One10:e0126996. [CrossRef][PubMed]
    [Google Scholar]
  46. van der Walt J. P., Nel E. E..( 1968;). Candida edax sp.n. . Antonie van Leeuwenhoek34:106–108. [CrossRef][PubMed]
    [Google Scholar]
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