An eight-gene molecular phylogeny of the Kickxellomycotina, including the first phylogenetic placement of Asellariales

Mycologia

Volumn 106, Issue 5, 2014, Pages 912-935

  Tretter, Eric D ^a   Johnson, Eric M ^a   Benny, Gerald L ^b   Lichtwardt, Robert W ^c   Wang, Yan ^a   Kandel, Prasanna ^a   Novak, Stephen J ^a   Smith, James F ^a   White, Merlin M ^a  

^a BOISE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF KANSAS   (United States)

Author keywords

Arthropod symbiosis; Clades; Molecular phylogenies; Mycophyletic; Zoopagomycotina

Indexed keywords

ARTHROPOD; CLADISTICS; DIVERGENCE; FUNGUS; GENE EXPRESSION; LIFE HISTORY; MOLECULAR ANALYSIS; MORPHOLOGY; PHYLOGENY; SYMBIOSIS; TAXONOMY;

ARTHROPODA; ASELLARIALES;

FUNGAL DNA; FUNGAL PROTEIN; RIBOSOME DNA;

ANIMAL; ARTHROPOD; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; FUNGUS; FUNGUS SPORE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIOSIS;

ANIMALS; ARTHROPODS; BASE SEQUENCE; DNA, FUNGAL; DNA, RIBOSOMAL; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; FUNGI; MOLECULAR SEQUENCE DATA; MYCOLOGICAL TYPING TECHNIQUES; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SPORES, FUNGAL; SYMBIOSIS;

EID: 84907576453     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/13-253     Document Type: Article

References (78)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105, doi:10.1093/bioinformatics/bti263
2. Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F. 2004. Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20: 407-415, doi:10.1093/bioinformatics/btg427
3. Baker RH, DeSalle R. 1997. Multiple sources of character information and the phylogeny of Hawaiian Drosophilids. Syst Biol 46:654-673, doi:10.1093/sysbio/46.4.654
4. Benjamin RK. 1959. The merosporangiferous Mucorales. Aliso 4:321-433.
5. Benjamin RK. 1961. Addenda to ''The merosporangiferous Mucorales''. Aliso 5:11-19.
6. Benjamin RK. 1979. Zygomycetes and their spores. The whole fungus 2:573-622.
7. Benny GL. 2005. Zygomycetes. Published on the Internet at http://www.zygomycetes.org
8. Bollback JP. 2006. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7:88, doi:10.1186/1471-2105-7-88
9. Brain APR, Jeffries P, Young TWK. 1982. Ultrastructure of septa in Tieghemiomyces californicus. Mycologia 74:173- 181, doi:10.2307/3792883
10. Cafaro MJ. 1999. Baltomyces, a new genus of gut-inhabiting fungus in an isopod. Mycologia 91:517-519, doi:10.2307/3761352
11. Chuang S-C, Ho H-M, Benny G, Lee C-F. 2013. Two new Ramicandelaber species from Taiwan. Mycologia 105: 320-334, doi:10.3852/11-219
12. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772-772, doi:10.1038/ nmeth.2109
13. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797, doi:10.1093/nar/gkh340
14. Farr DF, Lichtwardt Robert W. 1967. Some cultural and ultrastructural aspects of Smittium culisetae (Trichomycetes) from mosquito larvae. Mycologia 59:172-182, doi:10.2307/3756952
15. Felsenstein J. 1974. The evolutionary advantage of recombination. Genetics 78:737-756.
16. Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for Basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118, doi:10.1111/j.1365-294X.1993.tb00005.x
17. Goloboff PA, Farris JS, Källersjö M, Oxelman B, Ramírez MJ, Szumik CA. 2003. Improvements to resampling measures of group support. Cladistics 19:324-332, doi:10.1111/j.1096-0031.2003.tb00376.x
18. Goloboff PA, Farris JS, Nixon KC. 2008. TNT, a free program for phylogenetic analysis. Cladistics 24: 774- 786, doi:10.1111/j.1096-0031.2008.00217.x
19. Gottlieb AM, Lichtwardt RW. 2001. Molecular variation within and among species of Harpellales. Mycologia 93: 66-81, doi:10.2307/3761606
20. Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL. 2008. The Vienna RNA Websuite. Nucleic Acids Res 36:W70-W74, doi:10.1093/nar/gkn188
21. Guindon S, Gascuel O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704, doi:10.1080/ 10635150390235520
22. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüssler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N. 2007. A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509-547, doi:10.1016/j.mycres.2007.03.004
23. Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755, doi:10.1093/bioinformatics/17.8.754
24. Humber RA. 2012. Entomophthoromycota: a new phylum and reclassification for entomophthoroid fungi. Mycotaxon 120:477-492, doi:10.5248/120.477
25. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüssler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818-822, doi:10.1038/ nature05110
26. Jeffries P, Young TWK. 1979. Ultrastructure of septa in Dimargaris cristalligena R.K. Benjamin. J Gen Microbiol 111:303-311, doi:10.1099/00221287-111-2-303
27. Keeling PJ. 2003. Congruent evidence from a-tubulin and btubulin gene phylogenies for a zygomycete origin of Microsporidia. Fungal Genet Biol 38:298-309, doi:10.1016/S1087-1845(02)00537-6
28. Keeling PJ, Luker MA, Palmer JD. 2000. Evidence from betatubulin phylogeny that microsporidia evolved from within the Fungi. Mol Biol Evol 17:23-31, doi:10.1093/ oxfordjournals.molbev.a026235
29. Kurihara Y, Degawa Y, Tokumasu S. 2004. Two novel kickxellalean fungi, Mycoëmilia scoparia gen. sp. nov. and Ramicandelaber brevisporus sp. nov. Mycol Res 108: 1143-1152, doi:10.1017/S0953756204000930
30. Le SQ, Gascuel O. 2008. An improved general amino acid replacement matrix. Mol Biol Evol 25:1307-1320, doi:10.1093/molbev/msn067
31. Lichtwardt RW, Cafaro MJ, White MM. 2001. The Trichomycetes, fungal associates of arthropods. Revised edition. Published on the Internet: http://www.nhm. ku.edu/,fungi
32. Liu YL, Hodson M, Hall B. 2006. Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of kingdom Fungi inferred from RNA polymerase II subunit genes. BMC Evol Biol 6:74, doi:10.1186/1471-2148-6-74
33. Liu YL, Whelen S, Hall BD. 1999. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799-1808, doi:10.1093/oxfordjournals.molbev.a026092
34. Maddison W, Maddison D. 2011. Mesquite 2.75: a modular systemfor evolutionary analysis. (http://mesquiteproject. org)
35. Mattern D, Schlegel M. 2001. Molecular evolution of the small subunit ribosomal DNA in woodlice (Crustacea, Isopoda, Oniscidea) and implications for Oniscidean phylogeny. Mol Phylogenet Evol 18:54-65, doi:10.1006/ mpev.2000.0861
36. Moss ST. 1975. Septal structure in the trichomycetes with special reference to Astreptonema gammari (Eccrinales). Trans Br Mycol Soc 65:115-127, doi:10.1016/ S0007-1536(75)80187-2
37. Moss ST, Lichtwardt RW. 1977. Zygospores of the Harpellales: an ultrastructural study. Can J Bot 55:3099-3110, doi:10.1139/b77-351
38. Moss ST, Young TWK. 1978. Phyletic considerations of the Harpellales and Asellariales (Trichomycetes, Zygomycotina) and the Kickxellales (Zygomycetes, Zygomycotina). Mycologia 70:944-963, doi:10.2307/3759130
39. Muller HJ. 1964. The relation of recombination to mutational advance. Mutat Res-Fund Mol M 1:2-9, doi:10.1016/0027-5107(64)90047-8
40. O'Donnell K. 1993. Fusarium and its near relatives. In: Reynolds R, Taylor JW, eds. The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. Wallingford, United Kingdom: CAB International. p 225-233.
41. O'Donnell K, Cigelnik E, Benny GL. 1998. Phylogenetic relationships among the Harpellales and Kickxellales. Mycologia 90:624-639, doi:10.2307/3761222
42. Ogawa Y, Hayashi S, Degawa Y, Yaguchi Y. 2001. Ramicandelaber, a new genus of the Kickxellales, Zygomycetes. Mycoscience 42:193-199, doi:10.1007/BF02464137
43. Ogawa Y, Kurihara Y, Suda A, Kusama Eguchi K, Watanabe K, Tokumasu S. 2005. Taxonomic position of the genus Ramicandelaber, Kickxellales, inferred from 18SrDNA. Nippon Kingakukai Kaiho 46.
44. Oman SJ, White MM. 2012. Extended studies of Baltomyces styrax in Idaho and expanded distribution of this isopod gut fungus in USA. Mycologia 104:313-320, doi:10.3852/11-204
45. Ott M, Zola J, Stamatakis A, Aluru S. 2007. Large-scale maximum likelihood-based phylogenetic analysis on the IBM BlueGene/L. In: Proceedings of the 2007 ACM/IEEE conference on Supercomputing. ACM. 4 p. Penã C, Wahlberg N, Weingartner E, Kodandaramaiah U, Nylin S, Freitas AVL, Brower AVZ. 2006. Higher level phylogeny of Satyrinae butterflies (Lepidoptera: Nymphalidae) based on DNA sequence data. Mol Phylogenet Evol 40:29-49, doi:10.1016/j.ympev.2006.02.007
46. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574, doi:10.1093/bioinformatics/ btg180
47. Saikawa M. 1989. Ultrastructure of the septum in Ballocephala verrucospora (Entomophthorales, Zygomycetes). Can J Bot 67:2484-2488, doi:10.1139/b89-318
48. Saikawa M, Oguchi M, Ruiz RFC. 1997a. Electron microscopy of two nematode-destroying fungi, Meristacrum asterospermum and Zygnemomyces echinulatus (Meristacraceae, Entomophthorales). Can J Bot 75:762-768, doi:10.1139/ b97-086
49. Saikawa M, Sugiura K, Sato H. 1997b. Electron microscopy of two trichomycetous fungi attached to the hindgut lining of pill bugs. Can J Bot 75:1479-1484, doi:10.1139/b97-862
50. Schmitt I, Crespo A, Divakar PK, Fankhauser JD, Herman-Sackett E, Kalb K, Nelsen MP, Nelson NA, Rivas-Plata E, Shimp AD, Widhelm T, Lumbsch HT. 2009. New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia 23:35-40, doi:10.3767/003158509X470602
51. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW, Miller AN, Wingfield MJ, Aime MC, An KD, Bai FY, Barreto RW, Begerow D, Bergeron MJ, Blackwell M, Boekhout T, Bogale M, Boonyuen N, Burgaz AR, Buyck B, Cai L, Cai Q, Cardinali G, Chaverri P, Coppins BJ, Crespo A, Cubas P, Cummings C, Damm U, de Beer ZW, de Hoog GS, Del-Prado R, Dentinger B, Diéguez- Uribeondo J, Divakar PK, Douglas B, Duenãs M, Duong TA, Eberhardt U, Edwards JE, Elshahed MS, Fliegerova K, Furtado M, García MA, Ge ZW, Griffith GW, Griffiths K, Groenewald JZ, Groenewald M, Grube M, Gryzenhout M, Guo LD, Hagen F, Hambleton S, Hamelin RC, Hansen K, Harrold P, Heller G, Herrera C, Hirayama K, Hirooka Y, Ho HM, Hoffmann K, Hofstetter V, Högnabba F, Hollingsworth PM, Hong SB, Hosaka K, Houbraken J, Hughes K, Huhtinen S, Hyde KD, James T, Johnson EM, Johnson JE, Johnston PR, Jones EB, Kelly LJ, Kirk PM, Knapp DG, Kõljalg U, Kovaćs GM, Kurtzman CP, Landvik S, Leavitt SD, Liggenstoffer AS, Liimatainen K, Lombard L, Luangsa-Ard JJ, Lumbsch HT, Maganti H, Maharachchikumbura SS, Martin MP, May TW, McTaggart AR, Methven AS, Meyer W, Moncalvo JM, Mongkolsamrit S, Nagy LG, Nilsson RH, Niskanen T, Nyilasi I, Okada G, Okane I, Olariaga I, Otte J, Papp T, Park D, Petkovits T, Pino-Bodas R, Quaedvlieg W, Raja HA, Redecker D, Rintoul TL, Ruibal C, Sarmiento-Ramírez JM, Schmitt I, Schüßler A, Shearer C, Sotome K, Stefani FO, Stenroos S, Stielow B, Stockinger H, Suetrong S, Suh SO, Sung GH, Suzuki M, Tanaka K, Tedersoo L, Telleria MT, Tretter E, Untereiner WA, Urbina H, Vágvölgyi C, Vialle A, Vu TD, Walther G, Wang QM, Wang Y, Weir BS, Weiß M, White MM, Xu J, Yahr R, Yang ZL, Yurkov A, Zamora JC, Zhang N, Zhuang WY, Schindel D. 2012. Nuclearribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109:6241-6246, doi:10.1073/pnas.1117018109
52. Shimodaira H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492-508, doi:10.1080/10635150290069913
53. Shimodaira H, Hasegawa M. 1999. Multiple comparisons of loglikelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114-1116, doi:10.1093/oxfordjournals. molbev.a026201
54. Shimodaira H, Hasegawa M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246- 1247, doi:10.1093/bioinformatics/17.12.1246
55. Sorenson MD, Franzosa EA. 2007. TreeRot 3. Boston University.
56. Stamatakis A. 2006a. Phylogenetic models of rate heterogeneity: a high performance computing perspective. In: Parallel and distributed processing symposium 2006. IPDPS 2006. 20th International. IEEE. 8 p.
57. Stamatakis A. 2006b. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688- 2690, doi:10.1093/bioinformatics/btl446
58. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57: 758-771, doi:10.1080/10635150802429642
59. Stöver BC, Müller KF. 2010. TreeGraph 2: Combining and visualizing evidence fromdifferent phylogenetic analyses. BMC Bioinformatics 11:7, doi:10.1186/1471-2105-11-7
60. Swofford DL. 2003. PAUP* 4: phylogenetic analysis using parsimony (*and other methods). Sunderland, Massachusetts: Sinauer Associates.
61. Tanabe Y, O'Donnell K, Saikawa M, Sugiyama J. 2000. Molecular phylogeny of parasitic Zygomycota (Dimargaritales, Zoopagales) based on nuclear small subunit ribosomal DNA sequences. Mol Phylogenet Evol 16: 253-262, doi:10.1006/mpev.2000.0775
62. Tanabe Y, Saikawa M, Watanabe MM, Sugiyama J. 2004. Molecular phylogeny of Zygomycota based on EF-1a and RPB1 sequences: limitations and utility of alternative markers to rDNA. Mol Phylogenet Evol 30:438-449, doi:10.1016/S1055-7903(03)00185-4
63. Tretter ED, Johnson EM, Wang Y, Kandel P, White MM. 2013. Examining new phylogenetic markers to uncover the evolutionary history of early-diverging fungi: comparing MCM7, TSR1 and rRNA genes for single- and multigene analyses of the Kickxellomycotina. Persoonia 30:106- 125, doi:10.3767/003158513X666394
64. Valle LG, Cafaro MJ. 2008. First report of zygospores in Asellariales and new species from the Caribbean. Mycologia 100:122-131, doi:10.3852/mycologia.100. 1.122
65. Valle LG, Santamaria S. 2005. Zygospores as evidence of sexual reproduction in the genus Orphella. Mycologia 97:1335-1347, doi:10.3852/mycologia.97.6.1335
66. Vilgalys R, Hester M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238-4246.
67. Walker WF. 1984. 5S ribosomal RNA sequences from Zygomycotina and evolutionary implications. Syst Appl Microbiol 5:448-456, doi:10.1016/S0723-2020(84)800 02-8
68. Wang Y, Tretter E, Lichtwardt RW, White MM. 2013. Overview of 75 y of Smittium research, establishing a new genus for Smittium culisetae and prospects for future revisions of the ''Smittium'' clade. Mycologia 105:90-111, doi:10.3852/11-311
69. Whisler HC. 1963. Observations on some new and unusual enterophilous Phycomycetes. Can J Bot 41:887-900, doi:10.1139/b63-074
70. White MM. 1999. Legerioides, a new genus of Harpellales in isopods and other Trichomycetes from New England, USA. Mycologia 91:1021-1030, doi:10.2307/3761634
71. White MM. 2002. Taxonomic and molecular systematic studies of the Harpellales (Trichomycetes) toward understanding the diversity, evolution and dispersal of gut fungi [doctoral dissertation]. Lawrence: Univ. Kansas. 177 p.
72. White MM. 2006. Evolutionary implications of a rRNA-based phylogeny of Harpellales. Mycol Res 110:1011-1024, doi:10.1016/j.mycres.2006.06.006
73. White MM, Siri A, Lichtwardt RW. 2006a. Trichomycete insect symbionts in Great Smoky Mountains National Park and vicinity. Mycologia 98:333-352, doi:10.3852/mycologia. 98.2.333
74. White MM, James TY, O'Donnell K, Cafaro Matías J, Tanabe Y, Sugiyama J. 2006b. Phylogeny of the Zygomycota based on nuclear ribosomal sequence data. Mycologia 98: 872-884, doi:10.3852/mycologia.98.6.872
75. 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. New York: Academic Press. p 315- 322.
76. Wilgenbusch JC, Warren DL, Swofford DL. 2004. AWTY: A system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference.
77. William RT, Strongman DB. 2012. Two new genera of fungal trichomycetes, Bactromyces and Laculus (Harpellales), from Nova Scotia, Canada. Botany 90:101- 111, doi:10.1139/b11-086
78. Young TWK. 1969. Ultrastructure of aerial hyphae in Linderina pennispora. Ann Bot 33:211-216.