New species and emendations of Orphella: taxonomic and phylogenetic reassessment of the genus to establish the Orphellales, for stonefly gut fungi with a twist

LITERATURE CITED

• Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F. 2004. Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20:407–415.
   PubMed Web of Science ®Google Scholar
• Ayres DL, Darling A, Zwickl DJ, Beerli P, Holder MT, Lewis PO, Huelsenbeck JP, Ronquist F, Swofford DL, Cummings MP. 2012. BEAGLE: an application programming interface and high-performance computing library for statistical phylogenetics. Systematic Biology 61:170–173.
   PubMed Web of Science ®Google Scholar
• Benjamin RK 1963 Addenda to “The merosporangiferous Mucorales” II. Aliso 5:273–288.
   Google Scholar
• Bench ME, White MM. 2012. New species and first records of trichomycetes from immature aquatic insects in Idaho. Mycologia 104:295–312.
   Web of Science ®Google Scholar
• Benny GL, Smith ME, Kirk PM, Tretter ED, White MM. 2016. Challenges and future perspectives in the systematics of Kickxellomycotina, Mortierellomycotina, Mucoromycotina, and Zoopagomycotina. In: D-W Li, ed. Biology of microfungi. Switzerland: Springer International Publishing. p. 65–126.
   Google Scholar
• Benny GL, White MM. 2001. The classification and phylogeny of Trichomycetes and Zygomycetes. In: Misra JK, BW Horn BW, eds. Trichomycetes and other fungal groups. Enfield, New Hampshire: Science Publishers. p. 39–53.
   Google Scholar
• Cafaro MJ. 2005. Eccrinales (Trichomycetes) are not fungi, but a clade of protists at the early divergence of animals and fungi. Molecular Phylogenetics and Evolution 35:21–34.
   PubMed Web of Science ®Google Scholar
• Doweld AB. 2014. Orphellaceae Doweld fam. nov. IF550368. Index Fungorum 65: 1.
   Google Scholar
• Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792–1797.
   PubMed Web of Science ®Google Scholar
• Ferrington LC Jr, White MM, Lichtwardt RW. 2003. A new genus of Trichomycetes from Dixa fluvica Peters (Diptera: Dixidae). Aquatic Insects 25:85–94.
   Web of Science ®Google Scholar
• Frison TH. 1935. The stoneflies, or Plecoptera, of Illinois. Illinois Natural History Survey Bulletin 20:280–471.
   Google Scholar
• Frison TH. 1942. Studies of North American Plecoptera. Illinois Natural History Survey Bulletin 22:235–355.
   Google Scholar
• Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch HT, 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 Y-C, 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 K-H, Lichtwardt RW, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, 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. Mycological Research 111:509–547.
   PubMed Web of Science ®Google Scholar
• Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755.
   PubMed Web of Science ®Google Scholar
• Ingold CT. 1971. Fungal spores. Their liberation and dispersal. Oxford: Claredon Press. 302 p.
   Google Scholar
• 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 EA, Amtoft A, Stajich JE, Hosaka K, Sung G-H, 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 D, Spatafora JW, Vilgalys R. 2006. Reconstructing the early evolution of the fungi using a six gene phylogeny. Nature 443:818–822.
   PubMed Web of Science ®Google Scholar
• Jones EBG. 2006. Form and function of fungal spore appendages. Mycoscience 47:167–183.
   Google Scholar
• Kandel P, White MM. 2012. A new species of Ephemerellomyces from North America highlights its morphological plasticity and possible intergeneric similarities with other Harpellales. Fungal Biology 116:171–184.
   Google Scholar
• Kim S-K, Adler PH. 2007. Size variation of trichospores of Harpella melusinae in larval black flies. Mycologia 99:351–355.
   Google Scholar
• Kohno M. 1941. New species of stoneflies from Japan. Kontyû 15: 132–138.Japanese.
   Google Scholar
• Kurihara Y, Degawa Y, Tokumasu S. 2004. Two novel kickxellalean fungi, Mycoëmilia scoparia gen. sp. nov. and Ramicandelaber brevisporus sp. nov. Mycological Research 108:1143–1152.
   Google Scholar
• Léger L, Gauthier M. 1931. Orphella coronata n. g., n. sp. Entophyte parasite des larves de Némurides. Travaux du Laboratoire d’Hydrobiologie et de Pisciculture de l’Université de Grenoble 23:67–72.
   Google Scholar
• Léger L, Gauthier M. 1932. Endomycètes nouveaux des larves aquatiques d’Insectes. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences Paris 194:2262–2265.
   Google Scholar
• Lichtwardt RW. 1986. The Trichomycetes: fungal associates of arthropods. New York: Springer. 343 p.
   Google Scholar
• Lichtwardt RW.1995. Biogeography and fungal systematics. Canadian Journal of Botany 73(Supplement 1):S731–S737.
   Google Scholar
• Lichtwardt RW. 2004. Keys to the Trichomycetes. [ cited 2018 Feb 18]. Available from: http://keys.lucidcentral.org/key-server/data/0b08020c-0f0c-4908-8807-030c020a0002/media/Html/index.html. These online keys have been revised frequently from 2004–2017.
   Google Scholar
• Lichtwardt RW, Cafaro MJ, White MM. 2001a. The Trichomycetes, fungal associates of arthropods. Revised edition. [updated 2018 Jan; cited 2018 Feb 18]. Available from: https://keyserver.lucidcentral.org/key-server/data/0b08020c-0f0c-4908-8807-030c020a0002/media/Html/monograph/text/mono.htm
   Google Scholar
• Lichtwardt RW, Peterson SW, Huss MJ. 1991. Orphella hiemalis: a new and rare trichomycete occurring in winter-emerging stoneflies (Plecoptera, Capniidae). Mycologia 83:214–219.
   Web of Science ®Google Scholar
• Lichtwardt RW, White MM, Colbo MH. 2001b. Harpellales in Newfoundland aquatic insect larvae. Mycologia 93:764–773.
   Web of Science ®Google Scholar
• Lichtwardt RW, Williams MC. 1988. Distribution and species diversity of trichomycete gut fungi in aquatic insect larvae in two Rocky Mountain streams. Canadian Journal of Botany 66:1259–1264.
   Google Scholar
• Lichtwardt RW, Williams MC, Ferrington LC Jr, Hayford BL. 1997. Harpellales: generic confusion due to precocious development. Mycologia 89:109–113.
   Web of Science ®Google Scholar
• Maddison W, Maddison D. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. [cited 2013 Mar 11]. Available from: http://mesquiteproject.org
   Google Scholar
• McCreadie JW, Beard CE, Adler PH. 2005. Context-dependent symbiosis between black flies (Diptera: Simuliidae) and trichomycete fungi (Harpellales: Legeriomycetaceae). Oikos 108:362–370.
   Google Scholar
• Moss ST, Lichtwardt RW, Manier, J-F. 1975. Zygopolaris, a new genus of Trichomycetes producing zygospores with polar attachment. Mycologia 67:120–127.
   Web of Science ®Google Scholar
• 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; 2007 Nov 10–16; Reno, NV. New York, NY: ACM. p. 4.
   Google Scholar
• O’Donnell K, Cigelnick E, Benny, GL. 1998. Phylogenetic relationships among the Harpellales and Kickxellales. Mycologia 90:624–639.
   Web of Science ®Google Scholar
• Reynolds NK, Smith ME, Tretter ED, Gause J, Heeney D, Cafaro MJ, Smith JF, Novak SJ, Bourland WA, White MM. 2017. Resolving relationships at the animal-fungal divergence: a molecular phylogenetic study of the protist trichomycetes (Ichthyosporea, Eccrinida). Molecular Phylogenetics and Evolution 109:447–464.
   Google Scholar
• Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574.
   PubMed Web of Science ®Google Scholar
• Santamaria S, Girbal J. 1998. Two new species of Orphella from Spain. Mycological Research 102:174–178.
   Google Scholar
• Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W and the Fungal Barcoding Consortium. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America 109:6241–6246.
   Google Scholar
• Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O`Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE. 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046, doi:10.3852/16-042
   PubMed Web of Science ®Google Scholar
• Stamatakis A. 2006a. Phylogenetic models of rate heterogeneity: a high performance computing perspective. In: Proceedings 20th IEEE International Parallel and Distributed Processing Symposium; 2006 Apr 25–29; Rhodes Island, Greece. IEEE. p. 8.
   Google Scholar
• Stamatakis A.2006b. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690.
   PubMed Web of Science ®Google Scholar
• Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology 57:758–771.
   PubMed Web of Science ®Google Scholar
• Stöver BC, Müller KF. 2010. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11:7.
   PubMed Web of Science ®Google Scholar
• Strongman DB. 2007. Trichomycetes in aquatic insects from Prince Edward Island, Canada. Canadian Journal of Botany 85:949–963.
   Google Scholar
• Strongman DB, Wang J. 2015. New trichomycete species from China and additional information on Gauthieromyces. Mycologia 107:874–888.
   Web of Science ®Google Scholar
• Strongman DB, White MM. 2006. New species of Lancisporomyces, Orphella, and Paramoebidium, endosymbionts of stonefly nymphs from stream in Nova Scotia, Canada. Canadian Journal of Botany 84:1478–1495.
   Google Scholar
• Strongman DB, White MM. 2008. Trichomycetes from lentic and lotic aquatic habitats in Ontario, Canada. Botany 86:1449–1466.
   Google Scholar
• Terry MD. 2003. Phylogeny of the polyneopterous insects with emphasis on Plecoptera: molecular and morphological evidence [unpublished PhD dissertation]. Provo, Utah: Brigham Young University. 118 p. [cited 2013 Mar 11]. Available from: https://scholarsarchive.byu.edu/cgi/viewcontent.cgi?article=2133&context=etd
   Google Scholar
• Thomas MA, Walsh KA, Wolf MR, McPheron BA, Marden JH. 2000. Molecular phylogenetic analysis of evolutionary trends in stonefly wing structure and locomotor behavior. Proceedings of the National Academy of Sciences of the United States of America 97:13178–13183.
   Google Scholar
• Tretter ED, Johnson EM, Benny GL, Lichtwardt RW, Wang Y, Kandel P, Novak SJ, Smith JF, White MM. 2014. An eight-gene molecular phylogeny of the Kickxellomycotina, including the first phylogenetic placement of Asellariales. Mycologia 106:912–935.
   PubMed Web of Science ®Google Scholar
• 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 multi-gene analyses of the Kickxellomycotina. Persoonia 30:106–125.
   Google Scholar
• Valle LG. 2004. Tricomicets Ibèrics [doctoral dissertation]. Barcelona, Spain: Universitat Autonoma de Barcelona, Departament de Biologia Animal, de Biologia Vegetal i d’Ecologia, Botanica. 381 p. [cited 2013 Mar 11]. Available from: http://www.tesisenred.net/handle/10803/3704
   Google Scholar
• Valle LG. 2010. Description of zygospores in Tectimyces robustus and clarifications on homothallic species within Harpellales. Mycologia 102:384–391.
   Web of Science ®Google Scholar
• Valle LG. 2013. New and rare Harpellales from Portugal and northwestern Iberian Peninsula: discovering the hidden mycobiota of Galicia-Trás-os-Montes region. Mycologia 105:748–759.
   Web of Science ®Google Scholar
• Valle LG, Rossi W, Santamaria S. 2013. New species and new records of trichomycetes from Italy. Mycologia 105:712–727.
   Web of Science ®Google Scholar
• Valle LG, Rossi W, Santamaria S. 2014. Orphella intropus (Kickxellomycotina), a new insect endosymbiont with an unusual perforating holdfast and other trichomycetes from Italy. Mycologia 106:589–606.
   Web of Science ®Google Scholar
• Valle LG, Santamaria S. 2005. Zygospores as evidence of sexual reproduction in the genus Orphella. Mycologia 97:1335–1347.
   Web of Science ®Google Scholar
• Wang Y, Tretter ED, Johnson EM, Kandel P, Lichtwardt RW, Novak SJ, Smith JF, White MM. 2014. Using a five-gene phylogeny to test morphology-based hypotheses of Smittium and allies, endosymbiotic gut fungi (Harpellales) associated with arthropods. Molecular Phylogenetics and Evolution 79:23–41.
   Google Scholar
• Wang Y, Tretter ED, Lichtwardt RW, White MM. 2013. Overview of 75 years of Smittium research, establishing a new genus for Smittium culisetae, and prospects for future revisions of the “Smittium” clade. Mycologia 105:90–111.
   Web of Science ®Google Scholar
• Wang Y, White MM, Kvist S, Moncalvo J-M. 2016. Genome-wide survey of gut fungi (Harpellales) reveals the first horizontally transferred ubiquitin gene from a mosquito host. Molecular Biology and Evolution 33:2544–2554.
   Google Scholar
• White MM. 2006. Evolutionary implications of a rRNA-based phylogeny of Harpellales. Mycological Research 110:1011–1024.
   Google Scholar
• White MM, Cafaro MJ, Gottlieb AM. 2001. Taxonomy and systematics of Trichomycetes-past, present and future. In: Misra JK, Horn BW, eds. Trichomycetes and other fungal groups. Enfield, New Hampshire: Science Publishers. p. 27–37.
   Google Scholar
• White MM, James TY, O’Donnell K, Cafaro MJ, Tanabe Y, Sugiyama J. 2006a. Phylogeny of the Zygomycota based on nuclear ribosomal sequence data. Mycologia 98:872–884.
   PubMed Web of Science ®Google Scholar
• White MM, Lichtwardt RW. 2004. Fungal symbionts (Harpellales) in Norwegian aquatic insect larvae. Mycologia 96:891–910.
   Web of Science ®Google Scholar
• White MM, Lichtwardt RW, Colbo MH. 2006b. Confirmation and identification of parasitic stages of obligate endobionts (Harpellales) in blackflies (Simuliidae) by means of rRNA sequence data. Mycological Research 110:1070–1079.
   Google Scholar
• White MM, Siri A, Lichtwardt RW. 2006c. Trichomycete insect symbionts in Great Smoky Mountains National Park and vicinity. Mycologia 98:333–352.
   Google Scholar
• Wilgenbusch JC, Warren DL, Swofford DL. 2004. AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. [cited 2018 Feb 18]. Available from: http://ceb.csit.fsu.edu/awty
   Google Scholar
• Williams MC, Lichtwardt RW. 1987. Two new trichomycete species from Zapada spp. (stonefly) nymphs with an unusual distribution. Mycologia 79:473–478.
   Google Scholar
• Zwick P. 2000. Phylogenetic system and zoogeography of the Plecoptera. Annual Review of Entomology 45:709–746.
   PubMed Web of Science ®Google Scholar