Phylogeny of the Zygomycota based on nuclear ribosomal sequence data.

The Zygomycota is an ecologically heterogenous assemblage of nonzoosporic fungi comprising two classes, Zygomycetes and Trichomycetes. Phylogenetic analyses have suggested that the phylum is polyphyletic; two of four orders of Trichomycetes are related to the Mesomycetozoa (protists) that diverged near the fungal/animal split. Current circumscription of the Zygomycota includes only orders with representatives that produce zygospores. We present a molecular-based phylogeny including recognized representatives of the Zygomycetes and Trichomycetes with a combined dataset for nuclear rRNA 18S (SSU), 5.8S and 28S (LSU) genes. Tree reconstruction by Bayesian analyses suggests the Zygomycota is paraphyletic. Although 12 clades were identified only some of these correspond to the nine orders of Zygomycota currently recognized. A large superordinal clade, comprising the Dimargaritales, Harpellales, Kickxellales and Zoopagales, grouping together many symbiotic fungi, also is identified in part by a unique septal structure. Although Harpellales and Kickxellales are not monophyletic, these lineages are distinct from the Mucorales, Endogonales and Mortierellales, which appear more closely related to the Ascomycota + Basidiomycota + Glomeromycota. The final major group, the insect-associated Entomophthorales, appears to be polyphyletic. In the present analyses Basidiobolus and Neozygites group within Zygomycota but not with the Entomophthorales. Clades are discussed with special reference to traditional classifications, mapping morphological characters and ecology, where possible, as a snapshot of our current phylogenetic perspective of the Zygomycota.

[1]  M. L. Elgart,et al.  Zygomycosis. , 2020, Dermatologic clinics.

[2]  Peter M. Letcher,et al.  A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). , 2006, Mycologia.

[3]  Kenji Matsuura,et al.  Reconstructing the early evolution of Fungi using a six-gene phylogeny , 2006, Nature.

[4]  M. White Evolutionary implications of a rRNA-based phylogeny of Harpellales. , 2006, Mycological research.

[5]  M. White,et al.  Confirmation and identification of parasitic stages of obligate endobionts (Harpellales) in blackflies (Simuliidae) by means of rRNA sequence data. , 2006, Mycological research.

[6]  S. Santamaría,et al.  Zygospores as evidence of sexual reproduction in the genus Orphella. , 2005 .

[7]  S. Santamaría,et al.  Zygospores as evidence of sexual reproduction in the genus Orphella , 2005, Mycologia.

[8]  C. Hertweck,et al.  Pathogenic fungus harbours endosymbiotic bacteria for toxin production , 2005, Nature.

[9]  J. Sugiyama,et al.  Evolutionary relationships among basal fungi (Chytridiomycota and Zygomycota): Insights from molecular phylogenetics. , 2005, The Journal of general and applied microbiology.

[10]  S. Adl,et al.  The New Higher Level Classification of Eukaryotes with Emphasis on the Taxonomy of Protists , 2005, The Journal of eukaryotic microbiology.

[11]  L. Mahadevan,et al.  Physical Limits and Design Principles for Plant and Fungal Movements , 2005, Science.

[12]  M. Nout,et al.  Tempe fermentation, innovation and functionality: update into the third millenium , 2005, Journal of applied microbiology.

[13]  M. Cafaro Eccrinales (Trichomycetes) are not fungi, but a clade of protists at the early divergence of animals and fungi. , 2005, Molecular phylogenetics and evolution.

[14]  J. Bergsten A review of long‐branch attraction , 2005, Cladistics : the international journal of the Willi Hennig Society.

[15]  B. Lang,et al.  Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms , 2005, Nucleic acids research.

[16]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[17]  D. Hibbett,et al.  Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. , 2004, American journal of botany.

[18]  Y. Kurihara,et al.  Two novel kickxellalean fungi, Mycoëmilia scoparia gen. sp. nov. and Ramicandelaber brevisporus sp. nov. , 2004, Mycological research.

[19]  M. White,et al.  Fungal symbionts (Harpellales) in Norwegian aquatic insect larvae. , 2004, Mycologia.

[20]  M. White,et al.  Fungal symbionts (Harpellales) in Norwegian aquatic insect larvae , 2004 .

[21]  J. Sugiyama,et al.  Molecular phylogeny of Zygomycota based on EF-1alpha and RPB1 sequences: limitations and utility of alternative markers to rDNA. , 2004, Molecular phylogenetics and evolution.

[22]  M. Blackwell,et al.  Lobosporangium, a new name for Echinosporangium Malloch, and Gamsiella, a new genus for Mortierella multidivaricata , 2004, Mycologia.

[23]  T. Helgason,et al.  Phylogeny of the Glomerales and Diversisporales (fungi: Glomeromycota) from actin and elongation factor 1-alpha sequences. , 2003, FEMS microbiology letters.

[24]  P. Keeling Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of microsporidia , 2003 .

[25]  W. Gams,et al.  Delimitation of Umbelopsis (Mucorales, Umbelopsidaceae fam. nov.) based on ITS sequence and RFLP data. , 2003, Mycological research.

[26]  B Franz Lang,et al.  Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. , 2002, Molecular biology and evolution.

[27]  Daniel Schwarzott,et al.  A new fungal phylum, the Glomeromycota: phylogeny and evolution * * Dedicated to Manfred Kluge (Tech , 2001 .

[28]  E. Cerdá-Olmedo Phycomyces and the biology of light and color. , 2001, FEMS microbiology reviews.

[29]  Y. Degawa,et al.  A new genus Myconymphaea (Kickxellales) with peculiar septal plugs * * Contributions to Sugadaira Mo , 2001 .

[30]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[31]  Y. Ogawa,et al.  Ramicandelaber, a new genus of the Kickxellales, Zygomycetes , 2001 .

[32]  F. Lutzoni,et al.  Evolutionary relationships among mucoralean fungi (Zygomycota): Evidence for family polyphyly on a large scale , 2001 .

[33]  M. White,et al.  Taxonomy and Systematics of Trichomycetes -Past, Present and Future , 2001 .

[34]  R. Lichtwardt,et al.  Molecular variation within and among species of Harpellales , 2001 .

[35]  K. O’Donnell,et al.  Amoebidium parasiticum is a protozoan, not a Trichomycete. , 2000 .

[36]  D. Hibbett,et al.  Phylogenetic species recognition and species concepts in fungi. , 2000, Fungal genetics and biology : FG & B.

[37]  K. O’Donnell,et al.  Molecular phylogeny of parasitic zygomycota (Dimargaritales, zoopagales) based on nuclear small subunit ribosomal DNA sequences. , 2000, Molecular phylogenetics and evolution.

[38]  Timothy Y. James,et al.  Molecular phylogenetics of the Chytridiomycota supports the utility of ultrastructural data in chytrid systematics , 2000 .

[39]  J. Ribes,et al.  Zygomycetes in human disease. , 2000, Clinical microbiology reviews.

[40]  M. White Legerioides, a new genus of Harpellales in isopods and other Trichomycetes from New England, USA , 1999 .

[41]  R. Lichtwardt,et al.  Trichomycetes in Argentinean aquatic insect larvae , 1999 .

[42]  M. Cafaro Baltomyces, a new genus of gut-inhabiting fungus in an isopod , 1999 .

[43]  J. Sugiyama Relatedness, phylogeny, and evolution of the fungi , 1998 .

[44]  A. B. Jensen,et al.  Relationships of the insect-pathogenic order Entomophthorales (Zygomycota, Fungi) based on phylogenetic analyses of nuclear small subunit ribosomal DNA sequences (SSU rDNA). , 1998, Fungal genetics and biology : FG & B.

[45]  T. Cavalier-smith,et al.  A revised six‐kingdom system of life , 1998, Biological reviews of the Cambridge Philosophical Society.

[46]  E. Boa,et al.  Ainsworth and Bisby's Dictionary of the Fungi , 1998 .

[47]  K. O’Donnell,et al.  Phylogenetic relationships among the Harpellales and Kickxellales , 1998 .

[48]  S. Santamaría,et al.  Two new species of Orphella from Spain , 1998 .

[49]  M. Saikawa,et al.  Electron microscopy of two trichomycetous fungi attached to the hindgut lining of pill bugs , 1997 .

[50]  R. Gutell,et al.  A novel clade of protistan parasites near the animal-fungal divergence. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  H. Gehrig,et al.  Geosiphon pyriforme, a fungus forming endocytobiosis withNostoc (Cyanobacteria), is an ancestral member of the glomales: Evidence by SSU rRNA Analysis , 1996, Journal of Molecular Evolution.

[52]  J. Sugiyama,et al.  Phylogenetic divergence of the entomophthoralean fungi: Evidence from nuclear 18S ribosomal RNA gene sequences , 1995 .

[53]  D. Hibbett,et al.  Evolutionary relationships within the fungi: analyses of nuclear small subunit rRNA sequences. , 1992, Molecular phylogenetics and evolution.

[54]  C. Hesseltine Zygomycetes in food fermentations , 1991 .

[55]  M. Blackwell,et al.  LIFE HISTORY AND ARTHROPOD DISPERSAL OF A COPROPHILOUS STYLOPAGE , 1991 .

[56]  R. Carruthers,et al.  Fungi as naturally occurring entomopathogens. , 1990 .

[57]  R. Lichtwardt,et al.  The Trichomycetes: Fungal Associates of Arthropods , 1986 .

[58]  P. Jeffries Mycoparasitism within the Zygomycetes , 1985 .

[59]  I. Heath,et al.  THE STRUCTURE AND CYCLE OF THE NUCLEUS-ASSOCIATED ORGANELLE IN TWO SPECIES OF BASIDIOBOLUS , 1985 .

[60]  W. Walker 5S Ribosomal RNA Sequences from Zygomycotina and Evolutionary Implications , 1984 .

[61]  J. Anderson,et al.  Insect-Fungus Symbiosis: Nutrition, Mutualism and Commensalism , 1981 .

[62]  K. O’Donnell Zygomycetes in Culture , 1980 .

[63]  S. Moss,et al.  Phyletic Considerations of the Harpellales and Asellariales (Trichomycetes, Zygomycotina) and the Kickxellales (Zygomycetes, Zygomycotina) , 1978 .

[64]  G. Ainsworth,et al.  A taxonomic review with keys : basidiomycetes and lower fungi , 1974 .

[65]  R. N. Lester,et al.  Immunological studies on the fungal genus Smittium (Trichomycetes). , 1972, Mycologia.

[66]  F. Moreau Les Champignons. Tome II. Systematique , 1955 .

[67]  L. Haley Introductory Mycology , 1953, The Yale Journal of Biology and Medicine.

[68]  L. G. Valle Asellariales ( Trichomycetes ) from the Iberian Peninsula , 2006 .

[69]  P. Keeling,et al.  The fungal roots of microsporidian parasites. , 2005 .

[70]  Maria José Figueras,et al.  Atlas of clinical fungi. , 2005 .

[71]  L. Mendoza,et al.  The class mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. , 2002, Annual review of microbiology.

[72]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[73]  M. White,et al.  The Classification and Phylogeny of the Trichomycetes and Zygomycetes , 2001 .

[74]  T. Cavalier-smith What are Fungi , 2001 .

[75]  J. Palmer,et al.  Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. , 2000, Molecular biology and evolution.

[76]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[77]  I. Sanders Evolutionary genetics: No sex please, we're fungi , 1999, Nature.

[78]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[79]  S. Moss Harpellales (Trichomycetes); mycobionts of insecta , 1998 .

[80]  K. Nicholas,et al.  GeneDoc: Analysis and visualization of genetic variation , 1997 .

[81]  M. T. Hampton Atlas of Clinical Fungi , 1997 .

[82]  D. Pegler,et al.  Genera of Endogonales , 1996 .

[83]  G. Benny,et al.  Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae , 1990 .

[84]  R. Humber Synopsis of a revised classification for the Entomophthorales (Zygomycotina) , 1989 .

[85]  R. Kenneth,et al.  A reclassification of Entomophthora turbinata in Thaxterosporium gen. nov., Neozygitaceae fam. nov. (Zygomycetes: Entomophthorales) , 1987 .

[86]  H. D. Burges Microbial control of pests and plant diseases 1970-1980 , 1981 .

[87]  R. Humber An alternative view of certain taxonomic criteria used in the Entomophthorales (Zygomycetes) [Fungi, insect pathogens] , 1981 .

[88]  C. Ingold The biology of Mucor and its allies , 1978 .

[89]  W. Gams A key to the species of Mortierella , 1977 .

[90]  Richard K. Benjamin Addenda to "The Merosporangiferous Mucorales" , 1961 .

[91]  R. K. Benjamin Sexuality in the Kickxellaceae , 1958 .