Scheffersomyces cryptocercus: A new xylose-fermenting yeast associated with the gut of wood roaches and new combinations in the Sugiyamaella yeast clade

Mycologia

Volumn 105, Issue 3, 2013, Pages 650-660

  Blackwell, Meredith ^a   Urbina, Hector ^a   Frank, Robert ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

RPB1; Saccharomycotina; XYL1; Xylose reductase

Indexed keywords

ASEXUAL REPRODUCTION; CARBOHYDRATE; COCKROACH; FERMENTATION; MICROBIAL COMMUNITY; MICROHABITAT; NEW SPECIES; STOMACH CONTENT; YEAST;

XYLOSE; XYLOSE REDUCTASE;

ANIMAL; ARTICLE; CLASSIFICATION; FERMENTATION; GASTROINTESTINAL TRACT; GENETICS; INSECT; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; RPB1; SACCHAROMYCETALES; SACCHAROMYCOTINA; UNITED STATES; WOOD; XYL1;

RPB1; SACCHAROMYCOTINA; XYL1; XYLOSE REDUCTASE;

ANIMALS; FERMENTATION; GASTROINTESTINAL TRACT; INSECTS; NORTH CAROLINA; SACCHAROMYCETALES; TENNESSEE; WOOD; XYLOSE;

MLCS; MLOWN;

EID: 84880837044     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/12-094     Document Type: Article

References (56)

1. Agbogbo FK. 2007. Production of ethanol from corn stover hemicellulose hydrolyzate using Pichia stipitis. J Ind Microbiol Biotechnol 34:723-727, doi:10.1007/s10295-007-0247-z
2. Agbogbo FK,Coward-Kelly G. 2008. Cellulosic ethanol production using the naturally occurring xylose-fermenting yeast, Pichia stipitis. Biotechnol Lett 30:1515-1524, doi:10.1007/s10529-008-9728-z
3. Agbogbo FK,Wenger KS. 2006. Effect of pretreatment chemicals on xylose fermentation by Pichia stipitis. Biotechnol Lett 28:2065-2069, doi:10.1007/s10529-006-9192-6
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403- 410, doi:10.1016/S0022-2836(05)80360-2
5. Barnett JA, Payne RW, Yarrow D. 2000. Yeasts: characteristics and identification. Cambridge, UK: Cambridge Univ. Press. 1139 p
6. Berkov A, Feinstein J, Small J, Nkamany M. 2007. Yeasts isolated from Neotropical wood-boring beetles in SE Peru. Biotropica 39:530-538, doi:10.1111/j.1744-7429.2007.00280.x
7. Berlanga M, Paster BJ, Guerrero R. 2009. The taxophysiological paradox: changes in the intestinal microbiota of the xylophagous cockroach Cryptocercus punctulatus depending on the physiological state of the host. Int Microbiol 12:227-236, doi:10.2436/20.1501.01.102
8. Boundy-Mills K. 2006. Methods for investigating yeast biodiversity. In: Peter G, Rosa CA, eds. Biodiversity and ecophysiology of yeast. Berlin: Springer-Verlag. p 67-100
9. Calderon O, Berkov A. 2012. Midgut and fat body bacteriocytes in Neotropical cerambycid beetles (Coleoptera: Cerambycidae). Environ Entomol 41:108-117, doi:10.1603/EN11258
10. Carpenter KJ, Chow L, Keeling PJ. 2009. Morphology, phylogeny and diversity of Trichonympha (Parabasalia: Hypermastigida) of the wood-feeding cockroach Cryptocercus punctulatus. J Eukaryot Microbiol 56:305-313, doi:10.1111/j.1550-7408.2009.00406.x
11. Carpenter KJ,Horak A, Chow L, Keeling PJ. 2011. Symbiosis, morphology and phylogeny of Hoplonymphidae (Parabasalia) of the wood-feeding roach Cryptocercus punctulatus. J Eukaryot Microbiol 58:426-436, doi:10.1111/j.1550-7408.2011.00564.x
12. Carpenter KJ,Horak A,Keeling PJ. 2010. Phylogenetic position and morphology of Spirotrichosomidae (Parabasalia): new evidence from Leptospironympha of Cryptocercus punctulatus. Protist 161:122-132, doi:10.1016/j.protis.2009.06.003
13. Clark JW, Kambhampati S. 2003. Phylogenetic analysis of Blattabacterium, endosymbiotic bacteria from the wood roach, Cryptocercus (Blattodea: Cryptocercidae), including a description of three new species. Mol Phylogenet Evol 26:82-88, doi:10.1016/S1055-7903(02)00330-5
14. Engel MS, Grimaldi DA, Krishna AK. 2009. Termites (Isoptera): their phylogeny, classification and rise to ecological dominance. Am Mus Novit 3650:1-27, http://hdl.handle.net/2246/5969, doi:10.1206/651.1
15. Fadda ME, Mossa V, Pisano MB, Deplano M, Cosentino S. 2004. Occurrence and characterization of yeasts isolated from artisanal Fiore Sardo cheese. Int J Food Microbiol 95:51-59, doi:10.1016/j.ijfoodmicro.2004.02.001
16. Fadda ME, Viale S, Deplano M, Pisano MB, Cosentino S. 2010. Characterization of yeast population and molecular fingerprinting of Candida zeylanoides isolated from goat's milk collected in Sardinia. Int J Food Microbiol 136:376-380, doi:10.1016/j.ijfoodmicro.2009.10.007
17. Golubev WI, Blagodatskaya M, Suetin SO, Trotsenko R. 1981. Pichia inositovora and Candida paludigena, two new species of yeasts isolated from peat. Int J Syst Bacteriol 31:91-96, doi:0020-77 13/8 1/01009 1-06$02.00/0
18. Grünwald S, Pilhofer M, Holl W. 2010. Microbial associations in gut systems of wood-and bark-inhabiting longhorned beetles [Coleoptera: Cerambycidae]. Syst Appl Microbiol 33:25-34, doi:10.1016/j.syapm.2009.10.002
19. Henninger W, Windisch S. 1976. Kluyveromyces blattae sp. n., a new multispored yeast for Blatta orientalis (author's transl). Arch Microbiol 109:153-156, doi:10.1007/BF00425128
20. Hibbett DS. 1996. Phylogenetic evidence for horizontal transmission of group I introns in the nuclear ribosomal DNA of mushroom-forming fungi. Mol Biol Evol 13:903-917, doi:10.1093/oxfordjournals.molbev.a025658
21. Houseknecht JL, Hart EL, Suh SO, Zhou JJ. 2011. Yeasts in the Sugiyamaella clade associated with wood-ingesting beetles and the proposal of Candida bullrunensis sp. nov. Int J Syst Evol Microbiol 61:1751-1756, doi:10.1099/ijs.0.026427-0
22. Hughes GL, Allsopp PG, Webb RI, Yamada R, Iturbe- Ormaetxe I, Brumbley SM, O'Neill SL. 2011. Identification of yeast associated with the planthopper, Perkinsiella saccharicida: potential applications for Fiji leaf gall control. Curr Microbiol 63:392-401, doi:10.1007/s00284-011-9990-5
23. Kitade O. 2004. Comparison of symbiotic flagellate faunae between termites and wood-feeding cockroach of the genus Cryptocercus. Microbes Environ, 19:215-220
24. Klass KD, Nalepa C, Lo N. 2008. Wood-feeding cockroaches as models for termite evolution (Insecta: Dictyoptera): Cryptocercus vs. Parasphaeria boleiriana. Mol Phylogenet Evol 46:809-817, doi:10.1016/J.Ympev.2007.11.028
25. Knapp S, McNeill J, Turland NJ. 2011. Changes to publication requirements made at the XVIII International Botanical Congress in Melbourne: What does e-publication mean for you Taxon 60:1498-1501
26. Kurtzman CP. 2007. Eleven new species of Sugiyamaella and Candida from forest habitats. FEMS Yeast Res 7:1046- 1063, doi:10.1111/j.1567-1364.2007.00224.x
27. Kurtzman CP, Fell JW, Boekhout T. 2011. The yeasts, a taxonomic study. 5th ed. Amsterdam: Elsevier. p xxii + 1-289, xv + 290-1335, xvi + 1336-2080
28. Kurtzman CP, Robnett CJ. 1998. Three new insect-associated species of the yeast genus Candida. Can J Microbiol 44:965-973.
29. Lamarche J, Stefani FO, Seguin A, Hamelin RC. 2011. Impact of endochitinase-transformed white spruce on soil fungal communities under greenhouse conditions. FEMS Microbiol Ecol 76:199-208, doi:10.1111/j.1574-6941. 2011.01041.x
30. Legendre F, Whiting MF, Bordereau C, Cancello EM, Evans TA, Grandcolas P. 2008. The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: implications for the evolution of the worker and pseudergate castes, and foraging behaviors. Mol Phylogenet Evol 48:615-627, doi:10.1016/j.ympev.2008.04.017
31. Liu K, Warnow TJ, Holder MT, Nelesen SM, Yu J, Stamatakis AP, Linder CR. 2012. SATe-II: very fast and accurate simultaneous estimation of multiple sequence alignments and phylogenetic trees. Syst Biol 61:90-106, doi:10.1093/sysbio/syr095
32. Maddison W, Maddison D. 2005. Mesquite: a modular system for evolutionary analysis. Evolution 62:1103-1118.
33. Maekawa K, Park YC, Lo N. 2005. Phylogeny of endosymbiont bacteria harbored by the woodroach Cryptocercus spp. (Cryptocercidae: Blattaria): molecular clock evidence for a late Cretaceous-early Tertiary split of Asian and American lineages. Mol Phylogenet Evol 36:728-733, doi:10.1016/J.Ympev.2005.03.033
34. Nardi JB, Bee CM, Miller LA, Nguyen NH, Suh SO, Blackwell M. 2006. Communities of microbes that inhabit the changing hindgut landscape of a subsocial URBINA ET AL.: YEASTS FROM A WOOD ROACH 659 beetle. Arthropod Struct Dev 35:57-68, doi:10.1016/ j.asd.2005.06.003
35. Nguyen NH, Suh SO, Blackwell M. 2007. Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia 99:842-58, doi:10.3852/mycologia.99.6.842
36. Nguyen NH, Suh SO, Marshall CJ, 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 110:1232-1241, doi:10.1016/j.mycres. 2006.07.002
37. Noda S, Inoue T, Hongoh Y, Vongkaluang C, Kudo T, Ohkuma M. 2006. Identification and characterization of ectosymbionts of distinct lineages in Bacteroidales attached to flagellated protists in the gut of termites and a wood-feeding cockroach. Environ Microbiol 8: 11-20, doi:10.1111/j.1462-2920.2005.00860.x
38. Ohama T, Suzuki T, Mori M, Osawa S, Ueda T, Watanabe K, Nakase T. 1993. Non-universal decoding of the leucine codon CUG in several Candida species. Nucleic Acids Res 21:4039-4045, doi:10.1093/nar/21.17.4039
39. Ohkuma M, Noda S, Hongoh Y, Nalepa CA, Inoue T. 2009. Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc Biol Sci 276:239- 245, doi:10.1098/rspb.2008.1094
40. Prillinger P, Künig H. 2006. The intestinal yeasts. In: Künig H, Varma A, eds. Soil biology. Vol. 6. Intestinal microorganisms of soil invertebrates. Berlin, Heidelberg: Springer-Verlag. p 319-334.
41. Prillinger P, Messner R, König H, Bauer R, Lopandic K, Molnar O, Danget P, Weigang F, Kirisits T, Nakase T, Sigler L. 1996. Yeasts associated with termites: a phenotypic and genotypic characterization and use of coevolution for dating evolutionary radiations in asco- and basidiomycetes. System Appl Microbiol 19:265-283, doi:10.1016/j.bbr.2011.03.031
42. Sacchi L, Nalepa CA, Bigliardi E, Corona S, Grigolo A, Laudani U, Bandi C. 1998. Ultrastructural studies of the fat body and bacterial endosymbionts of Cryptocercus punctulatus Scudder (Blattaria: Cryptocercidae).Symbiosis 25:251-269.
43. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, the Barcoding Consortium. 2012. Nuclear ribosomal internal spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci USA 109: 6241- 6246, doi:10.1073/ pnas.1117018109
44. Schoch CL, Sung GH, Lopez-Giraldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Matheny PB, Kauff F, Wang Z, Gueidan C, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Groenewald JZ, Arzanlou M, de Hoog GS, Crous PW, Hewitt D, Pfister DH, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh SO, Blackwell M, Hillis DM, Griffith GW, Castlebury LA, Rossman AY, Lumbsch HT, Lücking R, Budel B, Rauhut A, Diederich P, Ertz D, Geiser DM, Hosaka K, Inderbitzin P, Kohlmeyer J, Volkmann-Kohlmeyer B, Mostert L, O'Donnell K, Sipman H, Rogers JD, Shoemaker RA, Sugiyama J, Summerbell RC, Untereiner W, Johnston PR, Stenroos S, Zuccaro A, Dyer PS, Crittenden PD, Cole MS, Hansen K, Trappe JM, Yahr R, Lutzoni F, Spatafora JW. 2009. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224-239, doi:10.1093/sysbio/syp020
45. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690, doi:10.1093/bioinformatics/btl446
46. Suh SO, Blackwell M. 2004. Three new beetle-associated yeast species in the Pichia guilliermondii clade. FEMS Yeast Res 5:87-95, doi:10.1016/j.femsyr.2004.06.001
47. Suh SO, Blackwell M., Kurtzman CP, Lachance MA. 2006. Phylogenetics of Saccharomycetales, the ascomycete yeasts. Mycologia 98:1006-1017, doi:10.3852/mycologia.98.6.1006
48. Suh SO, Marshall CJ, McHugh JV, Blackwell M. 2003. Wood ingestion by passalid beetles in the presence of xylosefermenting gut yeasts. Mol Ecol 12:3137-3145, doi:10.1046/j.1365-294X.2003.01973.x
49. Suh SO, McHugh JV, Pollock DD, Blackwell M. 2005. The beetle gut: a hyperdiverse source of novel yeasts. Mycol Res 109:261-265, doi:10.1017/S0953756205002388
50. Suh SO, White MM, Nguyen NH, Blackwell M. 2004. The status and characterization of Enteroramus dimorphus: a xylose-fermenting yeast attached to the gut of beetles. Mycologia 96:756-760, doi:10.2307/3762109
51. Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC. 1995. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology 141:1507-1521, doi:10.1099/13500872-141-7-1507
52. Urbina H, Blackwell M. 2012. Multilocus phylogenetic study of the Scheffersomyces yeast clade and molecular characterization of the N-terminal region of xylose reductase gene. PLoS ONE 7(6):e39128, doi:10.1371/journal.pone.0039128
53. White TJ, Bruns TD, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. San Diego: Academic Press. p 315-322.
54. Wohlbach DJ, Kuo A, Sato TK, Potts KM, Salamov AA, Labutti KM, Sun H, Clum A, Pangilinan JL, Lindquist EA, Lucas S, Lapidus A, Jin M, Gunawan C, Balan V, Dale BE, Jeffries TW, Zinkel R, Barry KW, Grigoriev IV, Gasch AP. 2011. Comparative genomics of xylose-fermenting fungi for enhanced biofuel production. Proc Natl Acad SciU S A 108:13212-13217, doi:10.1073/pnas.1103039108
55. Yarrow D. 1998. Methods for the isolation, maintenance and identification of yeasts. In: Kurtzman CP, Fell JW, eds. The yeasts, a taxonomic study. Amsterdam: Elsevier. p 77-100.
56. Zhang N, Suh SO, Blackwell M. 2003. Microorganisms in the gut of beetles: evidence from molecular cloning. J Invertebr Pathol 84:226-33, doi:10.1016/j.jip.2003.10.002