1887

Abstract

During a survey of yeasts associated with wood-ingesting insects, 69 strains in the clade and related taxa were isolated from passalid and tenebrionid beetles and the decayed wood inhabited by them. The majority of these yeasts was found to be capable of fermenting xylose, and was recognized as or its close relative , which are known to be associated with wood-decaying beetles and rotten wood. Yeasts in ‘’ ( = ) and ‘’ ( = ) were also frequently isolated. The remaining six strains were identified as representing four novel species in the genera and based on multilocus sequence analyses of nuclear rRNA genes and four protein-coding genes, as well as other taxonomic characteristics. Two xylose-fermenting species, f.a., sp. nov. (type strain ATCC MYA-4653 = CBS 12535 = EH045; MycoBank MB805440) and f.a., sp. nov. (type strain ATCC MYA-4859 = CBS 12540 = MY10-052; MycoBank MB805441), formed a clade with and related species. Interestingly, can survive at 40 °C, which is a rare property among xylose-fermenting yeasts. sp. nov. (type strain ATCC MYA-4650 = CBS 11838 = EH019; MycoBank MB805442) is a sister taxon of , while sp. nov. (type strain ATCC MYA-4652 = CBS 12534 = EH030; MycoBank MB805443) is closely related to in the clade. The multilocus DNA sequence comparisons in this study suggest that the genus needs to be circumscribed to the species near (type species) and that can be characterized by the ability to ferment xylose.

Funding
This study was supported by the:
  • National Science Foundation (Award DBI-0548684)
  • ATCC Internship Program
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2013-11-01
2024-11-05
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. ( 1990 ). Basic local alignment search tool. . J Mol Biol 215, 403410.[PubMed] [CrossRef]
    [Google Scholar]
  2. Barnett J. A., Payne R. W., Yarrow D. ( 2000 ). Yeasts: Characteristics and Identification, , 3rd edn.. Cambridge:: Cambridge University Press;.
    [Google Scholar]
  3. Dowd P. F. ( 1992 ). Insect fungal symbionts: a promising source of detoxifying enzymes. . J Ind Microbiol 9, 149161. [View Article]
    [Google Scholar]
  4. Felsenstein J. ( 2009 ). phylip (Phylogeny Inference Package) version 3.69. Distributed by the author. . Department of Genome Sciences, University of Washington;, Seattle, USA:.
    [Google Scholar]
  5. Gujjari P., Suh S.-O., Lee C.-F., Zhou J. J. ( 2011 ). Trichosporon xylopini sp. nov., a hemicellulose-degrading yeast isolated from the wood-inhabiting beetle Xylopinus saperdioides . . Int J Syst Evol Microbiol 61, 25382542. [View Article] [PubMed]
    [Google Scholar]
  6. 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 Microbiol 61, 17511756. [View Article] [PubMed]
    [Google Scholar]
  7. Jeffries T. W. ( 2006 ). Engineering yeasts for xylose metabolism. . Curr Opin Biotechnol 17, 320326. [View Article] [PubMed]
    [Google Scholar]
  8. Jeffries T. W., Shi N. Q. ( 1999 ). Genetic engineering for improved xylose fermentation by yeasts. . Adv Biochem Eng Biotechnol 65, 117161.[PubMed]
    [Google Scholar]
  9. Jeffries T. W., Grigoriev I. V., Grimwood J., Laplaza J. M., Aerts A., Salamov A., Schmutz J., Lindquist E., Dehal P. & other authors ( 2007 ). Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis . . Nat Biotechnol 25, 319326. [View Article] [PubMed]
    [Google Scholar]
  10. Kurtzman C. P. ( 1990 ). Candida shehatae – genetic diversity and phylogenetic relationships with other xylose-fermenting yeasts. . Antonie van Leeuwenhoek 57, 215222. [View Article] [PubMed]
    [Google Scholar]
  11. Kurtzman C. P. ( 2006 ). Yeast species recognition from gene sequence analyses and other molecular methods. . Mycoscience 47, 6571. [View Article]
    [Google Scholar]
  12. Kurtzman C. P. ( 2011 ). Scheffersomyces Kurtzman & M. Suzuki (2010). . In The Yeasts, a Taxonomic Study, , 5th edn., pp. 773777. Edited by Kurtzman C. P., Fell J. W., Boekhout T. . London:: Elsevier;. [View Article]
    [Google Scholar]
  13. 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 Leeuwenhoek 73, 331371. [View Article] [PubMed]
    [Google Scholar]
  14. Kurtzman C. P., Robnett C. J. ( 2003 ). Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. . FEMS Yeast Res 3, 417432. [View Article] [PubMed]
    [Google Scholar]
  15. Kurtzman C. P., Robnett C. J. ( 2013 ). Relationships among genera of the Saccharomycotina (Ascomycota) from multigene phylogenetic analysis of type species. . FEMS Yeast Res 13, 2333. [View Article] [PubMed]
    [Google Scholar]
  16. Kurtzman C. P., Suzuki M. ( 2010 ). Phylogenetic analysis of ascomycete yeasts that form coenzyme Q-9 and the proposal of the new genera Babjeviella, Meyerozyma, Millerozyma, Priceomyces, and Scheffersomyces . . Mycoscience 51, 214. [View Article]
    [Google Scholar]
  17. Kurtzman C. P., Fell J. W., Boekhout T., Robert V. ( 2011 ). Methods for isolation, phenotypic characterization and maintenance of yeasts. . In The Yeasts, a Taxonomic Study, , 5th edn., pp. 87110. Edited by Kurtzman C. P., Fell J. W., Boekhout T. . London:: Elsevier;. [View Article]
    [Google Scholar]
  18. Lachance M.-A., Boekhout T., Scorzetti G., Fell J. W., Kurtzman C. P. ( 2011 ). Candida Berkhout (1923). . In The Yeasts, a Taxonomic Study, , 5th edn., pp. 9871278. Edited by Kurtzman C. P., Fell J. W., Boekhout T. . London:: Elsevier;. [View Article]
    [Google Scholar]
  19. Lichtwardt R. W., White M. M., Cafaro M. J., Misra J. K. ( 1999 ). Fungi associated with passalid beetles and their mites. . Mycologia 91, 694702. [View Article]
    [Google Scholar]
  20. Matheny P. B., Liu Y. J., Ammirati J. F., Hall B. D. ( 2002 ). Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). . Am J Bot 89, 688698. [View Article] [PubMed]
    [Google Scholar]
  21. Nardi J. B., Bee C. M., Miller L. A., Nguyen N. H., Suh S.-O., Blackwell M. ( 2006 ). Communities of microbes that inhabit the changing hindgut landscape of a subsocial beetle. . Arthropod Struct Dev 35, 5768. [View Article] [PubMed]
    [Google Scholar]
  22. Nguyen N. H., Suh S.-O., Marshall C. J., Blackwell M. ( 2006 ). Morphological and ecological similarities: wood-boring beetles associated with novel xylose-fermenting yeasts, Spathaspora passalidarum gen. sp. nov. and Candida jeffriesii sp. nov.. Mycol Res 110, 12321241. [View Article] [PubMed]
    [Google Scholar]
  23. Perlack R. D., Wright L. L., Turhollow A. F., Graham R. L., Stokes B. J., Erbach D. C. ( 2005 ). Biomass as feedstock for a bioenergy and bioproducts industry: the technical feasibility of a billion-ton annual supply. DOE/GO-102995-2135. ORNL/TM-2005. Oak Ridge, TN: US Department of Energy and Oak Ridge National Laboratory. http://www1.eere.energy.gov/biomass/pdfs/final_billionton_vision_report2.pdf [CrossRef]
    [Google Scholar]
  24. Pointing S. B. ( 1999 ). Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. . Fungal Divers 2, 1733.
    [Google Scholar]
  25. Prillinger H., Messner R., König H., Bauer R., Lopandic K., Molnar O., Dangel P., Weigang F., Kirisits T. & other authors ( 1996 ). Yeasts associated with termites: a phenotypic and genotypic characterization and use of coevolution for dating evolutionary radiations in asco- and basidiomycetes. . Syst Appl Microbiol 19, 265283. [View Article]
    [Google Scholar]
  26. Rehner S. A., Buckley E. ( 2005 ). A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. . Mycologia 97, 8498. [View Article] [PubMed]
    [Google Scholar]
  27. Ronquist F., Huelsenbeck J. P. ( 2003 ). MrBayes 3: Bayesian phylogenetic inference under mixed models. . Bioinformatics 19, 15721574. [View Article] [PubMed]
    [Google Scholar]
  28. Schäfer A., Konrad R., Kuhnigk T., Kämpfer P., Hertel H., König H. ( 1996 ). Hemicellulose-degrading bacteria and yeasts from the termite gut. . J Appl Bacteriol 80, 471478. [View Article] [PubMed]
    [Google Scholar]
  29. Schoch C. L., Seifert K. A., Huhndorf S., Robert V., Spouge J. L., Levesque C. A., Chen W. Fungal Barcoding Consortium ( 2012 ). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi . . Proc Natl Acad Sci U S A 109, 62416246. [View Article] [PubMed]
    [Google Scholar]
  30. Stiller J. W., Hall B. D. ( 1997 ). The origin of red algae: implications for plastid evolution. . Proc Natl Acad Sci U S A 94, 45204525. [View Article] [PubMed]
    [Google Scholar]
  31. Suh S.-O., Zhou J. J. ( 2010 ). Methylotrophic yeasts near Ogataea (Hansenula) polymorpha: a proposal of Ogataea angusta comb. nov. and Candida parapolymorpha sp. nov.. FEMS Yeast Res 10, 631638.[PubMed]
    [Google Scholar]
  32. Suh S.-O., Zhou J. J. ( 2011 ). Kazachstania intestinalis sp. nov., an ascosporogenous yeast from the gut of passalid beetle Odontotaenius disjunctus . . Antonie van Leeuwenhoek 100, 109115. [View Article] [PubMed]
    [Google Scholar]
  33. Suh S.-O., Marshall C. J., McHugh J. V., Blackwell M. ( 2003 ). Wood ingestion by passalid beetles in the presence of xylose-fermenting gut yeasts. . Mol Ecol 12, 31373145. [View Article] [PubMed]
    [Google Scholar]
  34. Suh S.-O., White M. M., Nguyen N. H., Blackwell M. ( 2004 ). The status and characterization of Enteroramus dimorphus: a xylose-fermenting yeast attached to the gut of beetles. . Mycologia 96, 756760. [View Article] [PubMed]
    [Google Scholar]
  35. Suh S.-O., McHugh J. V., Pollock D. D., Blackwell M. ( 2005 ). The beetle gut: a hyperdiverse source of novel yeasts. . Mycol Res 109, 261265. [View Article] [PubMed]
    [Google Scholar]
  36. Swofford D. L. ( 2002 ). paup. Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. . Sunderland, MA:: Sinauer Associates;.
    [Google Scholar]
  37. Tatusova T. A., Madden T. L. ( 1999 ). blast 2 sequences, a new tool for comparing protein and nucleotide sequences. . FEMS Microbiol Lett 174, 247250. [View Article] [PubMed]
    [Google Scholar]
  38. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. ( 1997 ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. . Nucleic Acids Res 25, 48764882. [View Article] [PubMed]
    [Google Scholar]
  39. Urbina H., Blackwell M. ( 2012 ). Multilocus phylogenetic study of the Scheffersomyces yeast clade and characterization of the N-terminal region of xylose reductase gene. . PLoS ONE 7, e39128. [View Article] [PubMed]
    [Google Scholar]
  40. 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. . Mycologia 105, 650660. [View Article] [PubMed]
    [Google Scholar]
  41. Vega E. F., Dowd P. E. ( 2005 ). The role of yeast as insect endosymbionts. . In Insect-Fungal Associations: Ecology and Evolution, pp. 211243. Edited by Vega F. E., Blackwell M. . New York:: Oxford University Press;.
    [Google Scholar]
  42. Zhang N., Suh S. O., Blackwell M. ( 2003 ). Microorganisms in the gut of beetles: evidence from molecular cloning. . J Invertebr Pathol 84, 226233. [View Article] [PubMed]
    [Google Scholar]
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