F0007 - Phylum Zygomycota and the new classification - Univap

PhylumZygomycotaZygomycota DENR 1Zygomycota DENR 2Phylum ZygomycotaZygomycota DENR 3Recent phylogenetically basedreclassifications• Zygomycota, Zygomycotina, Zygomycetes andEntomophthorales– The taxonomic revision of the fungi (Hibbett et al., 2007)resulted in significant revision of the traditional view of themost ancestral groups of the nonflagellate fungi. Thephylum Zygomycota, subphylum Zygomycotina, and classZygomycetes disappeared in their widely understood senseto be replaced by the phylum Glomeromycota (forarbuscular mycorrhizal fungi) and a series of new subphylanot yet assigned to any phylum (because of the obviouslypolyphyletic nature of the zygomycetes as traditionallytreated).Zygomycota DENR 4Recent phylogenetically basedreclassifications• Zygomycota, Zygomycotina, Zygomycetes andEntomophthorales–The Entomophthorales is reclassified in the subphylumEntomophthoromycotina Humber (in Hibbett et al.2007); the other new subphyla in this group are theMucormycotina, Zoopagomycotina andKicxellomycotina. Where there had been some questionabout whether Basidiobolus and its close relatives shouldbe retained in the Entomophthorales or moved to a positioncloser to some of the blastocladialean watermolds, James etal. (2006) unequivocally retain Basidiobolus in an ancestralposition in the Entomophthorales.Zygomycota DENR 5Recent phylogenetically basedreclassifications• Zygomycota, Zygomycotina, Zygomycetes andEntomophthorales– Despite the short-term frustration of needing to deal withfungi belonging to these groups that the familiar conceptsof Zygomycota, Zygomycotina and Zygomycetes are newabandoned.Zygomycota DENR 61

Recent phylogenetically basedreclassifications• Zygomycota, Zygomycotina, Zygomycetes andEntomophthorales– Until such a time as the molecular studies clarify theoverall relationships among these fungi and establish a newset of phyla, my practical advice is to continue to use thesediscontinued phylum, subphylum and class names since (1)their meanings remain unambiguous in terms of the fungiincluded, and (2) journals may remain unwilling or unablefor some time still to handle the concepts of new subphylawith unassigned status (‘incertae sedis’).Zygomycota DENR 7Classificação HierárquicaReino FungiFilo ZygomycotaSubfilo MucormycotinaClasse ZygomycetesOrdem MucoralesFamilía MucoraceaeGênero MucorEspécie: Mucor mucedoZygomycota DENR 8Zygomycota• Duas Classes–Classe Zygomycetes–Classe TrichomycetesBased on 18S + 28S + 5.8SZygomycetesTrichomycetesFrom White et al. 2006. Mycologia98:872-884Zygomycota DENR 9Zygomycota DENR 10Zygomycota• Classe Zygomycetes– 10 ordens– 32 famílias– 124 gêneros– 870 espécies• Classe Trichomycetes– 3 ordens– 6 famílias– 55 gêneros– 218 espéciesZygomycota DENR 11– Phylum Zygomycota– Classe Zygomycetes» Ordem Mucorales» Ordem Entomophtorales» Ordem Zoopagales» Ordem Dimargaritales» Ordem Kickxellales» Ordem Endogonales» Ordem Glomales» Ordem MortiellalesZygomycota– Phylum Zygomycota– Classe Trichomycetes» Ordem Harpellales» Ordem Asellariales» Ordem EccrinalesThe order Glomales was removed in 2001 and elevated to PhylumGlomeromycota due their lack of Zygomycota zygospore DENR formation, their mycorrhizal 12habit, and lack of DNA sequence homology2

Zygomycota• Classe Zygomycetes– Abundantes– Distribuídos em todo mundo– Saprótrofos– Patógenos– Causa podridão nos frutos e madeirae cogumelos.Zygomycota• Classe Trichomycetes– Parasitas obrigatórios– Vivem nos intestinos dos insetos eoutros artrópodes (endosimbiontes).Zygomycota DENR 13Zygomycota DENR 14Zygomycetes• Esporangiósporo – típico esporonão sexual formado pelos membrosdesta divisão.Formado endogenamente dentro de umesporângio.O esporângio é formado em cima de umpedúnculo chamado esporangióforoMorangos cobertos Zygomycota com DENR micelio de Rhizopus 15Zygomycota DENR 16Mucor sp.sporangiumsporangiophoreZygomycetessporangiosporescolumellaRhizopusZygomycetes• A maioria dos esporângios produzvários esporangiósporos, entretanto,algumas espécies produzem poucosou apenas um. Este esporângioreduzido é chamado deesporangiolesMucorZygomycota DENR 17http://www.botany.utoronto.ca/ResearchLabs/MallochLab/Malloch/Moulds.htmlZygomycota DENR 183

Zygomycetes• Esporangio contendo 1-50 esporos• Merosporangio éesporangioles comesporos em sérieslinearesesporangiolesZygomycota DENR 19Zygomycota DENR 20sporangiosporessporangiophorecolumellaZygomycota DENR 21 Zygomycota DENR 22Microscopic features of Rhizopus spp. inculture. (A) Low-power magnification (×4) ofRhizopus demonstrates the nodal occurrence ofwell-developed rhizoids in this genus(arrowhead). Sporangiophores are long andunbranched, usually terminating in largeglobose sporangia. In this figure, the sporangiahave become deliquescent, releasing a plethoraof sporangiospores seen dispersed in thebackground. The naked, somewhat collapsedcolumellae remain at the distal end of thesporangiophores (arrows). The sporangiophorethemselves are pigmented light brown. Bar,200 µm. (B) Rhizoids originate directly at thebase of the sporangiophores, often from agnarled, pigmented knot at the node(arrowhead). Stolons extend laterally from thenode (long arrows). The naked columella haspartially collapsed back on the sporangiophore(asterisk). At this higher power ofmagnification, the round to ovalsporangiospore morphology is readilyappreciated (short arrows). Bar, 25 µm. (C) Anintact, mature globose sporangium is seen inthis photomicrograph (arrow). The sphericalcolumella is nearly obscured by the presence ofthe sporangiospores in the sporangial sack. Aflattened, bare columella is also present,illustrating well the slight apophysis that isoften seen in the Rhizopus spp. (arrowhead).Bar, 50 µm. (D) Upon deliquescence, smallsporangial membrane remnants may adhere atthe interface between the apophysis and thecolumella. These remnants are referred to asthe collarette and are well illustrated in thisphotomicrograph (arrowheads). Note also theClinical Microbiology Reviews, April 2000, p. 236-301, Vol. 13, No. 2very slight apophysis at the top of theZygomycetes in Human Disease Zygomycota DENR sporangiophore. This columella is intact 23 anddemonstrates the oval shape that may be seenJulie A. Ribes, Carolyn L. Vanover-Sams, and Doris J. Bakerin Rhizopus isolates. Bar, 25 µm.Clinical Microbiology Reviews, April 2000, p. 236-301, Vol. 13, No. 2Zygomycetes in Human DiseaseJulie A. Ribes, Carolyn L. Vanover-Sams, and Doris J. BakerReproductive structures of the Mucorales. (A) Sporangium. Development of asexual sporangiospore in sacks called sporangia is characteristic of the families Mucoraceae and Saksenaea.The aerial mycelium of these organisms terminate in swollen structures that develop into sporangial sacks and columellae. Sporangiospores develop asexually by free-cell cleavagewithin the sporangial membrane. At maturity, the sporangium of the Mucorales becomes deliquescent, releasing the sporangiospores. A related mechanism where sporangiospores arereleased from the sporangiospore by dissolution of a gelatinous plug is seen for Saksenaea vasiformis. The fungus pictured here demonstrates the sporangium produced by Mucor spp.Bar, 20 µm. (B) Merosporangia. Cylindrical or finger-like projections surround a swollen vesicle in this isolate of Syncephalastrum racemosum. A single row of sporangiospores forminside these tubular merosporangia (arrowhead). Spores may be released as entire merosporangial units or singly as the merosporangial membrane dissolves. This form ofreproduction is characteristic of S. racemosum. Bar, 20 µm. (C and D) Sporangiola. Sporangiola or conidia develop singly around a swollen vesicle on stalks called sterigmata. Singlecelled sporangiola (arrowhead), typically produced by members of the genus Cunninghamella (C), are often echinate and form on short sterigmata. Those produced by Cokeromycesrecurvatus (D) are multicelled (arrowhead) and occur on long recurving stalks. Bar, 20 µm. (E) Yeast. Several members of the order Mucorales are dimorphic. Yeast forms have beenidentified in vivo for some Mucor spp. as well as Cokeromyces recurvatus (pictured here). Yeast production in vitro often requires increased temperature of incubation, high carbondioxide tension, or anaerobic culture conditions. Bar, 20 µm. (F and G) Chlamydospores and gemmae. These asexual reproductive structures are derived from the vegetative hyphaeof certain species of the Mucorales. Chlamydospores may be formed intercalated with the mycelium (endogenous formation) (arrowhead in panel F), while gemmae are separated fromthe mycelium and often demonstrate yeast-like budding (exogenous formation) (G). Chlamydospores and gemmae are often considered together, since they may be difficult todifferentiate and are similarly derived. These are produced by some but not all members of the Mucorales. Their morphology may vary substantially but is not particularly useful forspecies determination (355). Bar, 40 µm. (H) Zygospores. This is the only form of sexual reproduction employed by the zygomycetes. Zygospores may form within a single isolatewithout mating (homothallic reproduction) or may require mating with an appropriately oriented mating strain (heterothallic reproduction). Zygospore morphology is oftencharacteristic for an organism when color, size, shape and surface decoration Zygomycota are taken into account. DENR Mating of two isolates to produce mature zygospores provides definitive 24taxonomic identification of an unknown isolate. The zygospores pictured here are from Cokeromyces recurvatus. Bar, 40 µm.4

Clinical Microbiology Reviews, April 2000, p. 236-301, Vol. 13, No. 2Zygomycetes in Human DiseaseJulie A. Ribes, Carolyn L. Vanover-Sams, and Doris J. BakerSchematic diagram labeling the morphologic structures seen inthe sporangium-producing Mucorales (A) Rhizopus spp. (B)Apophysomyces elegans.Zygomycota DENR 25Gross morphology of Rhizopus, Mucor, and Absidiaisolates in culture. (A) Rhizopus gross morphology onSABHI medium. Rhizopus spp. typically produce avery high, fibrous colony that rapidly fills the entirepetri dish. This isolate has expanded to the lid(known as a "lid lifter"). It has produced abundantpigmented sporangia, which are seen as the dark areaspeppering the otherwise pale mycelium. Thismorphology is characteristic of the Rhizopus spp. (B)Low-growing Mucor variant gross morphology onSABHI medium. Mucor spp. will show variation fromculture to culture. This particular isolate has produceda low-growing, fibrous colony morphology thatreadily demonstrates the "woolly" or floccose growthcharacteristic of the Mucoraceae. Pigmentation is alsovariable, both within and among the Mucor spp.Increased pigmentation is generally reflective of areasof the mycelium that are rich in sporangia. Dependingon the individual isolate, Mucor may be extremelyfloccose or low growing and may range from purewhite to shades of gray or brown. (C) Absidiacorymbifera gross colony morphology on SABHImedium. A. corymbifera produces a light-coloredmycelium, generally cream or gray. The pepperedappearance seen in the Rhizopus spp. is lacking despitethe production of abundant sporangia. The myceliumof this isolate is firmly plastered to the lid of the petridish, consistent with the lid-lifting properly of thisfungus. (D) A. corymbifera, reverse side of the cultureplate shown in panel C. The Mucoraceae are hyalinemolds that produce a pale reverse in culture onstandard media such as SABHI agar. Although someisolates such as Rhizopus spp. may have lightlypigmented hyphal elements, this is generally reflectedas a pale yellow or brown reverse and not the darklyClinical Microbiology Reviews, April 2000, p. 236-301, Vol. 13, No. 2 pigmented reverse of the dematiaceous fungi.Zygomycetes in Human DiseaseZygomycota DENR 26Julie A. Ribes, Carolyn L. Vanover-Sams, and Doris J. BakerGross morphology of Basidiobolus, Conidiobolus,and Mucor colonies in culture. (A) Basidiobolusmicrosporus colony morphology on SABHI agar.Dense, waxy, folded, or furrowed colonies areproduced on standard culture media. Coloniesare low growing, lacking the floccosemorphology seen in the typical isolate of theMucorales (see Mucor morphology in panel B).This isolate produced a brownish orange colonythat was pale on reverse. (B) Mucor colonymorphology on SABHI agar. The floccose or"woolly" colony morphology produced by mostof the Mucorales is well demonstrated in thisMucor isolate. Contrast the fibrous aerialmycelium with the glabrous morphology seenfor both Basidiobolus (A) and Conidiobolus (C).Basidiobolus microsporusThis difference in colony morphology is one ofthe distinguishing features between the Mucoralesand the Entomophthorales. (C) Conidioboluscoronatus colony morphology on Sabourauddextrose agar slant. Similar to Basidiobolus spp.,Conidiobolus spp. produce low-growing waxy (orsometimes powdery) folded and furrowedcolonies that lack aerial mycelium. Satellitecolonies arising from germination of ejectedsporangiospores has lead to confluent growth inthis tube containing a 6-week-old culture. (D)Conidiobolus coronatus tube culture, side view ofthe tube in panel C. Note the cloudy appearanceof the glass surface of the tube. This isproduced by the collection of a plethora offorcibly expelled sporangiospores which haveClinical Microbiology Reviews, April 2000, p. 236-301, Vol. 13, No. 2become encrusted on the inside surface of thetube. This opacification of the culture tube (orZygomycetes in Human Disease Zygomycota DENRpetri dish lid) is characteristic of this organism.27Julie A. Ribes, Carolyn L. Vanover-Sams, and Doris J. BakerZygomycetes• O processo da reproduçãosexual consiste da fusão de doisgametângios dando a origem aum zigosporo (esporo de repousocom parede espessa) dentro de umzigosporângioZygomycota DENR 28Compatibilidade Sexual• Regulamentado pela ácido trispórico, umferomônio sexual (Blakeslee, 1904):– Aumenta a secreção de determinados precursoresde ácido trispórico e beta-caroteno– Positivamente regulamenta a sua própria síntese,estimulando a taxa precursores da formação emculturas pareadas– Induz a formação zigosporangio– Reprime formação do esporangióforoZygomycota DENR 29Zygomycetes• Homotálico – requer apenas um talo(hifa) para reprodução sexual• Heterotálico – requer dois talos (hifas) desexos opostos para reprodução sexual,designadas mais (+) ou menos (-)– Sexual spore produced by conjugation when(+) hyphae e (-) fuse is calledzygosporangiumZygomycota DENR 305

+ -MyceliumplasmogamyProgametangiaSuspensorskaryogamyGametangiaZygoteZygosporangiumZygomycota DENR 32ZygomycetesHighly ornamentedzygosporangium ofMycotypha africana.Sexualreproduction.Scanningelectronmicrograph ofgametangialfusion in Mucormucedo.Zygomycota DENR 33Fusão de doisnúcleosZygosporangiumFusão docitoplasma dedoisprotoplastosZygomycota DENR 34ZygomycetesRhizopus stoloniferZygomycota DENR 35Zygomycota DENR 366

ZygomycetesZygomycota DENR 37 Zygomycota DENR 38ZygomycetesZygomycetesTypes ofZygosporangiaHeterotálicoHomotálicoZygomycota DENR 39http://www.botany.utoronto.ca/ResearchLabs/MallochLab/Malloch/Moulds/Zygospores_of_Mucorales.htmlClinical Microbiology Reviews, April 2000, p. 236-301, Vol. 13, No. 2ZygomycetesZygomycotain HumanDENRDisease40Julie A. Ribes, Carolyn L. Vanover-Sams, and Doris J. BakerZygomycetesZygomycota DENR 41Zygomycetes• Zygosporos– Podem suportar meio ambientes hostis até ascondições melhorarem e o novo esporangio éformado.– Parede celular espessa, normalmente hialina, mas aparede do zigosporangio é normalmentepigmentada o ornamentada.– Um zigosporo por zigosporangio– Germinação pela formação de uma hifa ouesporangioZygomycota DENR 427

Ordem MucoralesOrdem MucoralesZygomycota DENR 43• Maioria Saprótrofos–Solo, fezes e húmus–São os mais comumente isolados entreos fungos mais comuns em meio decultura – crescem extremamente rápido.–Causam podridão de frutos e grãos –Mucor, Rhizopus, Absidia• Rhizopus – bolor negro do pão.Zygomycota DENR 44Ordem Mucorales• Rhizopus stoloniferOrdem Mucorales•Algumspatógenos de plantas– Choanephora cucurbitarium• on flowers & fruits of cucurbits– Rhizopus stolonifer• Post-harvest pathogen of strawberries, sweet potatoes• Patógenos de animais (muromicose)– Absidia, Mucor, Rhizopus, Saksanea• Poucos micopatógenos – parasitasobrigatórios de outros fungosZygomycota DENR 45Zygomycota DENR 46Ordem Mucorales• Aplicações industriais–Produção de amilases, metabólitosecundários e ácidos orgânicos• Acido cítrico, ácido fumárico, ácido lático,ácido oxálico, e acido succínico• Produção de cortisona – Rhizopus stolonifer–Produção de pigmentosOrdem Mucorales• Aplicações industriais– Although most lactic acid is made usingbacteria, the final product of the fungalprocess is easier to purify.– Species of Rhizopus and Mucor have beenused not only to sacharify rice but also toproduce alcohol from the resulting sugars.Zygomycota DENR 47Zygomycota DENR 488

Ordem Mucorales• Aplicações industriais– Mucoraceous fungi contribute substantiallyto the nutritional value of the foods.– Meatlike flavors from plant materials arealso produced by mucoraceous fungi.Ordem Mucorales• Produção de alimentos asiáticos–Tofu ou sufu (Chinese cheese)• Um queijo produzido de soja pelafermentação usando Actinomucor elegans–Tempeh• Um produto solido fermentado de sojacom o Rhizopus oligosporusZygomycota DENR 49Zygomycota DENR 50Ordem Mucorales• Micélio cenocítico• Composição da parede de quitosan,quitina e ácido poliglucoronico• Clamidósporos podem ser formados• Chamados de fungos mucoraceousOrdem Mucorales• Esporângio–A maioria produz esporângiogloboso–A parede esporangial pode serpersistente ou frágil liberando osesporangiosporos.Zygomycota DENR 51Zygomycota DENR 52• SporangiaOrdem Mucorales• Apophysate– Subsporangial swelling• Nonapophysate– Lacking subsporangialswellingOrdem Mucorales• Esporangiosporos– Células simples– Uninucleados a multinucleados– Parede lisa ou ornamentada com espinhos,verrugas ou estrias.– Maioria produz esporos hialinos– Alguns produz esporos hialinos comapêndicesZygomycota DENR 53Zygomycota DENR 549

Ordem MucoralesOrdem MucoralesRhizopusstolonsrhizoidsZygomycota DENR 55http://www.botany.utoronto.ca/ResearchLabs/MallochLab/Malloch/Moulds.htmlZygomycota DENR 56Ordem MucoralesOrdem MucoralesRhizopusZygomycota DENR 57Zygomycota DENR 58Ordem MucoralesPhycomycesZygospore of PhycomycesZygomycota DENR 59Phycomyces crescendo em comida de gatoZygomycota DENR 6010

Phycomyces• The sensitivity of Phycomyces to light is trulyremarkable and compares favorably to that ofthe human eye.• As noted by Corrochano and Cerdá-Olmedo(1992), while many plants and fungi can detectfull moonlight, the human eye andPhycomyces can “see” stars.Zygomycota DENR 61• PilobolusOrdem Mucorales– Common fungus sporulating on dung– Sporangia with dark, thick, persistant wall– Characterized by forcibly discharged sporangia (>2 meters!)• Sporangiophores are phototropic (bend towards light)• Pilaira - similar morphology and ecology,lacks discharge mechanismZygomycota DENR 62Ordem MucoralesPilobolus spsporangiumPilobolus spsporangiophoresubstratetrophocystZygomycota DENR 63Zygomycota DENR 64Pilobolus spOrdem MucoralesZygomycota DENR 65Zygomycota DENR 6611

Zygomycota DENR 67 Zygomycota DENR 68Ordem MucoralesDoençasNo homemZygomycota DENR 69 Zygomycota DENR 70MucormicoseDoenças micóticas não sãocontagiosasRhizopusMucorAbsidiaZygomycota DENR 71Zygomycota DENR 7212

Mucormicose• Diabetes não controlada - FATALZygomycota DENR 73Mucormicose• Sinais Clínicos–Ketoacidosis - is a type of metabolic acidosiswhich is caused by high concentrations of ketonebodies, formed by the deamination of amino acids,and the breakdown of fatty acids. This is mostcommon in untreated type 1 diabetes mellitus,when the liver breaks down fat and proteins inresponse to a perceived need for respiratorysubstrate.Zygomycota DENR 74Mucormicose• Sinais Clínicos–Nasal stuffiness–Proptosis – olhos–Eschar – gangrena, úlcera, infecçãofúngicasZygomycota DENR 75Mucormicose• Características da infecçãopor Mucor–Afinidade pela invasão arterial–Infecção nasal ou dos sinos–Invasão para o cérebro pela placacribiforme–Rapidamente fatalZygomycota DENR 76Mucormicose• Tratamento–Controle da diabetes–Biopsia–Cultura–Cirurgia–Anfotericina BOrdem EntomophtoralesZygomycota DENR 77Zygomycota DENR 7813

Ordem Entomophthorales• Six families recognized based on:– Nuclear characters (size and number)– Mode of formation of resting spores• Representatives of 4 families– Entomophthoraceae– Basidiobolaceae Saprotrophs in soil or colonizers in guts ofamphibians and reptiles, facultative pathogen of vertebrates– Neozygitaceae Obligate pathogens of insects, especially Homoptera, and mites– Ancylistaceae Saprotrophs in soil, pathogens of insects and otherinvertebratesZygomycota DENR 79Ordem Entomophthorales• Principais gêneros da famíliaEntomophthoraceae– Entomophtora – patógeno de insetos– Massospora – patógeno de insetos– Basidiobolus haptosporus – patógenohumano - Subcutaneous Zygomicose– Entomophtora coronata – patógeno humanoe de insetosZygomycota DENR 80Ordem EntomophthoralesOrdem Entomophthorales• Includes insect, miteand spider pathogensand saprotrophicspecies; one genus isparasitic on algae,another on ferngametophyteshttp://users.telenet.be/roeland.libeer1/ongewZygomycota DENRervelden%20rest/vlieg%20met%20schimmel81%201.jpgZygomycota DENR 82Order EntomophthoralesZygomycota DENR 83Ordem Entomophthorales• Obligate pathogens ofarthropods• Entomophthora (‘insectdestroyer’)– Primary conidiadischarged in a cannonlikemanner whenconidiophore ruptures– E. muscae, often foundinfecting dead fliesclinging to windowsEntomophthora muscae from TomZygomycota DENR 84Volk’s website14

Entomophthora muscaeOrdem Entomophthorales• Primary conidia germinate directlyto form hyphae, or indirectly toform secondary conidia:• Passively dispersed secondaryconidia produced on long, thinconidiophores; with sticky apicalstructure called a haptor at theconidium spex.• Forcibly discharged secondaryconidia with mechanism similar toprimary conidiaZygomycota DENR 85From O’Donnell, 1979Zygomycota DENR 86Ordem EntomophthoralesFamília Neozygitaceae(image from Bioimages)Zygomycota DENR 87Entomophthora muscae• Obligate pathogens of insects, especiallyHomoptera, and mites• Neozygites– Primary conidia discharged by papillareversion, germinate to form passivelydispersed secondary conidia with haptor onlong thin conidiophores– Resting spores dark, ornamented, with twopores; formed inside hostZygomycota DENR 88NeozygitesResting spores inthrips bodyResting sporegerminating toproduce conidiumResting spores;note two poreswhere gametangiawere attachedPrimary conidiagerminate to formpassively disperspedconidium with stickyhaptor (arrow)Ordem Mortierellales• 10% of known zygomycetes (~100 spp.)• Characterized by thin, delicate,“arachnoid-like” mycelium, zonatecolonies and garlic-like odor• Sporangiophores either acolumellate, orwith rudimentary columella• Often form chlamydosporesZygomycota DENR 89Zygomycota DENR 9015

MortierellaOrdem MortierellalesNo columellaOrdem Kickxellales• One family and eight genera• Characterized by one-spored (or from 1to 30 may be present) sporangiolaformed on pseudophialides borne onsporocladia• Extensively branched, septate mycelium• Saprotrophs, common in soil and dungZygomycota DENR 91http://www.botany.utoronto.ca/ResearchLabs/MallochLab/Malloch/Moulds.htmlZygomycota DENR 92Ordem KickxellalesOrdem KickxellalespseudophialidessporocladiamerosporangiaZygomycota DENR 93From O’Donnell 1979Zygomycota DENR 94From O’Donnell 1979Ordem Dimargaritales• One family and four genera• Characterized by 2-spored merosporangiaformed on terminal inflated ampullae• Produce branched, septate hyphae withunusual, dumbbell-shaped septal plugs• Obligate mycoparasites of mucoraceousfungiOrdem DimargaritalesDimargarisZygomycota DENR 95Zygomycota DENR From O’Donnell 1979 9616

Ordem Zoopagales• Five families, 21 genera, 163 species• Coenocytic or septate hyphae• Conidia or multispored merosporangia• All members are obligate parasites of otherfungi or microscopic animals (amoebae,rotifers, nematodes)• Ectoparasitic, endoparasitic or predaceous– Haustoria formed in host in ectoparasitic andpredaceous speciesZygomycota DENR 97Ordem ZoopagalesSyncephalis (11) and Piptocephalis (12)Zygomycota DENR From O’Donnell 1979 98Classe TrichomycetesClasse TrichomycetesZygomycota DENR 99Zygomycota DENR 100Classe Trichomycetes• Widespread• Obligately associated with the guts ofarthropods with chewing mouthparts(=mandibulate) in freshwater, marine orterrestrial environments• The word “associated” is used here becausethe exact nature of the relationships betweenthese fungi and their host is not fullyunderstood.Zygomycota DENR 101Classe Trichomycetes• Most species considered commensals– Association is obligate and beneficial for thefungus, but the hosts does not appear to be harmed– Some species of Smittium cause mortality in theirhostsZygomycota DENR 10217

Classe Trichomycetes• Co-evolved with arthropod hosts for > 200million years• 56 genera in 4 orders• Lack mycelium; produce septae, branched thalliattached to chitinous lining of host by holdfasts• Name means “hair fungus” because of extensivethallus development in gut of host• Sexual reproduction known in one of four ordersZygomycota DENR 103Classe Trichomycetes• Asexual reproduction• Trichospores - elongated, single-spored,uninucleate sporangia with one to severalfilamentous appendages that developcoiled inside sporangiophore• Trichospores expelled outside host andmust be ingested by a new host in orderto germinateZygomycota DENR 104Classe TrichomycetesClasse TrichomycetesZygomycota DENR 105Smittiun culisetae thallus and trichosporesGenistelloides helicoides from hindgutof stonefly nymph. Developingtrichospores with coiled appendages.Zygomycota DENR 106Classe TrichomycetesClasse TrichomycetesZygomycota DENR 107Zygomycota DENR 10818

PhylumGlomeromycotaOrdem GlomalesZygomycota DENR 109The order Glomales was removed in 2001 and elevatedto Phylum Glomeromycota due their lack of zygosporeformation, their mycorrhizal habit, and lack of DNAZygomycota DENR 110sequence homologyZygomycota DENR 111 Zygomycota DENR 112Phylum Glomeromycota• Proposed by Schuβler, Schwarzottand Walker (2001; MycologicalResearch 105: 1413-21) based onSSU rRNA gene sequences, withfour orders, including GlomeralesZygomycota DENR 113Phylum Glomeromycota• Ocorrem dois tipos de fungos micorrizosque são diferenciados pela morfologia efisiologia.–Ectomicorrizos – envolve a raizexternamente – Basidiomycota–Endomicorrizos – invade profundamenteas raízes (vesicular-arbuscular mycorrhizae -VAM) – Ordem Glomales• Mycorrhiza means “fungus root”Zygomycota DENR 11419

Phylum GlomeromycotaBasidiomycotaGlomeromycotaZygomycota DENR 115• Order Endogonales– Restricted to saprotrophicand ectomycorrhizalspecies that occur in soiland plant material– Sporocarps composedonly of azygospores– Two genera, Endogoneand SclerogoneEndogone flammicoronahttp://www.natruffling.org/photo.htmZygomycota DENR 116Phylum GlomeromycotaTambém m chamados de “pea-truffles”Phylum GlomeromycotaEctomicorrizosOrder EndogonalesEndogone lactiflua is a small Glomeromycota truffle. This one is less than half an inch across.The spores are very large (to 200 microns; Zygomycota eg. 2/10ths DENRof a millimeter) and can be seen with 117the naked eye as the reddish-brown spots in the gleba. http://www.natruffling.org/photo.htmZygomycota DENR 118Phylum Glomeromycota• Ordem Glomales• EndomycorrhizaeArbuscularmycorrhizal (AM)fungi• Vesicular arbuscularmycorrhizal (VAM)fungiPhylum Glomeromycota• Order Glomales• Called endomycorrhizae because ofintracellular arbuscules, highlyconserved structures that are the point ofexchange between host plant and fungus• 80-90% (300,000) species of vascularplants form mycorrhizae with these fungiZygomycota DENR 119Zygomycota DENR 12020

Phylum Glomeromycota• Order Glomales• Arbuscules remain alive only for fewdays before disintegrating and beingdigested by the cells of the plant(Alexopoulos et al., 1996, p153).• In a healthy mycorrhizal relationshipthere is a continuous sequence ofdevelopment and disintegration ofPhylum Glomeromycota• Order Glomales• In return for a source of carbohydrates,VAM fungi appear to provide significantbenefits for their partners. Their hyphaeextend into the soil away from roots andgreatly increase the potential for theabsortion of water and the uptake ofphosphorus and other nutrients by the plant.arbuscules Zygomycota DENR 121Zygomycota DENR 122Phylum Glomeromycota• Order Glomales• It also been suggested that hyphae of VAMfungi may absorb and transfer metabolitesfrom other fungi, bacteria, actinomycetes,algae, and cyanobacteria in the rhizosphere totheir associated plants.• Also contribute to the resistance to certain rootpathogens, fungi and nematodes by productionof antibiotic substances.Zygomycota DENR 123Phylum GlomeromycotaEndomicorrizosZygomycota DENR 124Phylum Glomeromycota• Formam os esporos debaixo do solo e estãofrequentemente dentro de esporocarposmacroscópicos.Phylum Glomeromycota• Esporocarpos não são cultivados emmeio de cultura• Esporocarpos podem ter Zigósporos,Clamidósporos ou Azigósporos queficam envoltos por hifas estéril.Zygomycota DENR 125Zygomycota DENR 12621

Phylum Glomeromycota• Micorriza arbuscular (AM) écaracterizada pela formação de estruturasúnicas, como arbusculos e vesículas porfungos do filo Glomeromycota.• AM ajudam a capturar nutrientes, comofósforo e outros micronutrientes do solo.Phylum Glomeromycota• Pode ser dito que é mais rápido fazer uma listadas plantas que não formam associaçãomicorrizica do que aqueles que fazem.• Esta é uma simbiose altamente evoluída derelações mutualistas entre fungos e plantasencontradas.• A mais prevalente simbiose conhecida, e AM éencontrada em 80% das famílias de plantasvasculares hoje.Zygomycota DENR 127Zygomycota DENR 128Phylum Glomeromycota• Characteristics of AM Fungi– Hyphae• Within root (intraradical) and outside root (extraradical)– Arbuscules• Highly branched, thin-walled structures within host cell,short-lived, become digested by plant– Spores• Formed in soil or roots; asexual, variable in size andcolor between taxa, may contain hundreds of nuclei• Formed singly or in spore ballsRaiz contendo células corticais com arbúsculosZygomycota DENR 129Zygomycota DENR 130Phylum GlomeromycotaPhylum GlomeromycotaHyphaeArbusculesMedicago truncatula root stained with acid fuchsin showing arbuscules in cortical cells (arrows)Zygomycota DENR 131and vesicles (V). From Ann. Rev. Microbiol. 2005. 59:19-42.Zygomycota DENR 132Arbuscule in host plant cell22

Phylum GlomeromycotaSpore of Entrophospora withsporiferous sacculeArbusculesSporesConfocal microscope image of Glomus versiforme in Medicago truncatula root cellshowing a fully developed arbuscule Zygomycota (top) and arbuscule DENR in process of collapse133(bottom). From Ann. Rev. Microbiology 2005. 59: 19-42.Spores of Acaulospora withsporiferous sacculesZygomycota DENR 134SporesGigaspora Zygomycota and DENR Scutellospora135Zygomycota DENR 136Phylum Glomeromycota• Storage Organs•Vesicles– Ovoid, ellipsoid to irregular in shape, thin-walled,formed from hyphae in root cortex– Only in suborder Glomineae (VAM)• Auxiliary Cells– Clusters of thin-walled cells formed on hyphaeoutside the root– Only in suborder Gigasporinae (AM)Vesicles in host rootZygomycota DENR 137Auxilliary cells23