Skip to main content
SpringerLink
Log in

Molecular Barcoding of Microscopic Fungi with Emphasis on the Mucoralean Genera Mucor and Rhizopus

  • Chapter
  • First Online:
Molecular Identification of Fungi

Abstract

A broad range of fungi were isolated from different geographic regions and substrates and identified according to traditional and modern methods. A total of 120 different isolates were assigned to the phyla, Basidiomycota with 8 isolates, Ascomycota with 75 isolates, and “Zygomycota” with 37 isolates. Although morphological characters were able to differentiate the isolates to their phyla and in most cases to the correct genera, a combination of several methods is always recommended because characterization and identification of unknown fungal isolates is highly error-prone if relying on single methods. Sequence-based identification turned out to be reliable for most Ascomycetes and Zygomycetes. But with the ongoing questionable trend to rely on sequences as first source information for species separation, the most serious problems are the annotation problems in public reference databases, the inconsistency of described taxa, and the available reference data.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abe A, Sone T, Sujaya I-N, Saito K, Oda Y, Asano K, Tomita F (2003) rDNA ITS sequences of Rhizopus oryzae: its application to classification and identification of lactic acid producers. Biosci Biotechnol Biochem 67:1725–1731

    Article  PubMed  CAS  Google Scholar 

  • Alastruey-Izquierdo A, Castelli MV, Cuesta I, Monzon A, Cuenca-Estrella M, Rodriguez-Tudela JL (2009) Activity of posaconazole and other antifungal agents against Mucorales strains identified by sequencing of internal transcribed spacers. Antimicrob Agents Chemother 53:1686–1689

    Article  PubMed  CAS  Google Scholar 

  • Alastruey-Izquierdo A, Hoffmann K, Hoog de GS, Rodriguez-Tudela JL, Voigt K, Bibashi E, Walther G (2010) Species recognition and clinical relevance of the zygomycetous genus Lichtheimia (syn. Mycocladus, Absidia pp). in revision

    Google Scholar 

  • Aliabadian M, Kaboli M, Nijman V, Vences M (2009) Molecular identification of birds: performance of distance-based DNA barcoding in three genes to delimit parapatric species. PloS ONE 4:e4119

    Article  CAS  Google Scholar 

  • Almyroudis N, Sutton D, Fothergill A, Rinaldi M, Kusne S (2007) In vitro susceptibilities of 217 clinical isolates of Zygomycetes to conventional and new antifungal agents. Antimicrob Agents Chemother 51:2587–2590

    Article  PubMed  CAS  Google Scholar 

  • Alvarez E, Sutton DA, Cano J, Fothergill AW, Stchigel A, Rinaldi MG, Guarro J (2009) Spectrum of zygomycete species identified from clinically significant specimens in the United States. J Clin Microbiol doi:101128/JCM00036-09

    Google Scholar 

  • Arnot DE, Roper C, Bayoumi RA (1993) Digital codes from hypervariable tandemly repeated DNA sequences in the Plasmodium falciparum circumsporozoite gene can genetically barcode isolates. Mol Biochem Parasitol 61:15–24

    Article  PubMed  CAS  Google Scholar 

  • Baayen RP, O’Donnell K, Bonants PJM, Cigelnik E, Kroon LPNM, Roebroeck EJA, Waalwijk C (2000) Gene genealogies and AFLP analyses in the Fusarium oxysporum complex identify monophyletic and nonmonophyletic formae speciales causing wilt and rot disease. Phytopathology 90:891–900

    Article  PubMed  CAS  Google Scholar 

  • Bal AM (2006) Importance of identication of zygomycetes in the era of newer antifungal agents. Transpl Infect Dis 8:122–123

    Article  PubMed  CAS  Google Scholar 

  • Balajee SA, Houbraken J, Verweij PE, Hong S-B, Yaghuchi T, Varga J, Samson RA (2007) Aspergillus species identification in the clinical setting. Stud Mycol 59:39–46

    Article  PubMed  CAS  Google Scholar 

  • Balajee SA, Borman AM, Brandt ME, Cano J, Cuenca-Estrella M, Dannaoui E, Guarro J, Haase G, Kibbler CC, Meyer W, O’Donnell K, Petti CA, Rodriguez-Tudela JL, Sutton D, Velegraki A, Wickes BL (2009) Sequence-based identification of Aspergillus, Fusarium and Mucorales in the clinical mycology laboratory: where are we and where should we go from here? J Clin Microbiol 47:877–884

    Article  PubMed  CAS  Google Scholar 

  • Benjamin RK (1979) Zygomycetes and their spores. In: Kendrick B (ed) The whole fungus the sexual-asexual synthesis. National Museum of Natural Science. National Museums of Canada and The Kananaskis Foundation Ottawa, Canada, pp 573–616

    Google Scholar 

  • Berbee LM, Taylor JW (2001) Fungal molecular evolution: gene trees and geologic time In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The Mycota, vol 7B. Systematics and evolution, Springer, Berlin, Germany, pp 229–245

    Chapter  Google Scholar 

  • Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome b sequences and mammals. J Mammal 82:960–973

    Article  Google Scholar 

  • Bridge PD, Roberts PJ, Spooner BM, Panchal G (2003) On the unreliability of published DNA sequences. New Phytol 160:43–48

    Article  CAS  Google Scholar 

  • Chase MW, Salamin N, Wilkinson M, Dunwell JM, Kesanakurthi RP, Haidar N, Svolainen V (2005) Land plants and DNA barcodes: short-term and long-term goals. Philos Trans R Soc London B 360:1889–1895

    Article  CAS  Google Scholar 

  • Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G (2004) Mycobank: an online initiative to launch mycology into the 21st century. Stud Mycol 50:19–22

    Google Scholar 

  • Cuenca-Estrella M, Gomez-Lopez A, Mellado E, Buitrago MJ, Monzon A, Rodriguez-Tudela JL (2006) Head-to-head comparison of the activities of currently available antifungal agents against 3, 378 Spanish clinical isolates of yeasts and filamentous fungi. Antimicrob Agents Chemother 50:917–921

    Article  PubMed  CAS  Google Scholar 

  • Dannaoui E, Meletiadis J, Mouton JW, Meis JF, Verweij PE, The Eurofung Network (2003) In vitro susceptibilities of Zygomycetes to conventional and new antifungals. J Antimicrob Chemother 51:45–52

    Article  PubMed  CAS  Google Scholar 

  • de Hoog GS, Guarro J, Gené J, Figueras MJ (2000) Atlas of clinical fungi. 2nd edn. Centraalbureau voor Schimmelcultures/University Rovira i Virgili, Utrecht, The Netherlands,/Reus, Spain

    Google Scholar 

  • Diwakar A, Dewan RK, Chowdhary A, Randhawa HS, Khanna G, Gaur SN (2007) Zygomycosis – a case report and overview of the disease in India. Mycoses 50:247–254

    Article  PubMed  Google Scholar 

  • Druzhinina IS, Kopchinskiy AG, Komon M, Bissett J, Szakacs G, Kubicek CP (2005) An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet Biol 42:813–828

    Article  PubMed  CAS  Google Scholar 

  • Ehrenberg CG (1820) De mycetogenesi as Acad C.L.C.N.C Praesidem Epistola Nova Acta Academiae Caesareae Leopoldino-Carolinae Germanicae. Naturae Curiosorum 10:159–222

    Google Scholar 

  • Einax E, Voigt K (2003) Oligonucleotide primers for the universal amplification of beta-tubulin genes facilitate phylogenetic analyses in the regnum Fungi. Org Divers Evol 3:185–194

    Article  Google Scholar 

  • Ellis JJ, Hesseltine CW (1965) The genus Absidia: globose-spored species. Mycologia 57:222–235

    Article  Google Scholar 

  • Ellis JJ, Hesseltine CW (1966) Species of Absidia with ovoid sporangiospores II. Sabouraudia 5:59–77

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits of phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fenchel T, Finlay BJ (2006) The diversity of microbes: resurgence of the phenotype. Philos Trans R Soc B 361:1965–1973

    Article  Google Scholar 

  • Fresenius G (1850) Mucor mucedo. Beiträge zur Mykologie 1:7

    Google Scholar 

  • Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423

    Article  Google Scholar 

  • Gams W, Bissett J (1998) Morphology and identification of Trichoderma In: Kubicek CP, Harman GE (eds) Trichoderma and Gliocladium. Basic Biology, Taxonomy and Genetics. Taylor and -Francis, London, UK, pp 3–34

    Google Scholar 

  • Geiser DM, Pitt JI, Taylor JW (1998) Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus. Proc Natl Acad Sci USA 95:388–393

    Article  PubMed  CAS  Google Scholar 

  • Geiser DM, Jimenez-Gasco MD, Kang SC, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) FUSARIUM–ID v 10: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473–479

    Article  CAS  Google Scholar 

  • Geiser DM, Klich MA, Frisvad JC, Peterson SW, Varga J, Samson RA (2007) The current status of species recognition and identification in Aspergillus. Stud Mycol 59:1–10

    Article  PubMed  CAS  Google Scholar 

  • Gherbawy Y, Hussien N (2009) Molecular characterization of Mucor circinelloides and Rhizopus stolonifer strains isolated from some Saudi fruits. Foodborne Pathog Dis 7(2) doi: 10.1089/fpd.2009.0359

    Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330

    PubMed  CAS  Google Scholar 

  • Greenberg RN, Scott LJ, Vaughn HH, Ribes JA (2004) Zygomycosis (mucormycosis): emerging clinical importance and new treatments. Curr Opin Infect Dis 17:517–525

    Article  PubMed  CAS  Google Scholar 

  • Hachmeister KA, Fung DY (1993) Tempeh: a mold-modified indigenous fermented food made from soybeans and/or ceral grains. Crit Rev Microbiol 19:137–188

    Article  PubMed  CAS  Google Scholar 

  • Hageskal G, Knutsen AK, Gaustad P, deHoog GS, Skaar I (2006) Diversity and significance of mold species in Norwegian drinking water. Appl Environ Microbiol 72:7586–7593

    Article  PubMed  CAS  Google Scholar 

  • Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95:641–655

    Article  Google Scholar 

  • Hawksworth DL (2001) The magnitude of fungal diversity: the 15 million species estimate revisited. Mycol Res 105:1422–1432

    Article  Google Scholar 

  • Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi? Phytopathology 87:888–891

    Article  PubMed  CAS  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identification through DNA barcodes. Proc R Soc Lond B 270:313–322

    Article  CAS  Google Scholar 

  • Hebert PDN, Stoeckle MA, Zemlak TS, Francis CM (2004a) Identification of birds through DNA barcodes. PLoS Biol 2:1657–1663

    Article  CAS  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004b) Ten species in one, DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    Article  PubMed  CAS  Google Scholar 

  • Helbig AJ, Seibold I (1999) Molecular phylogeny of Palearctic–African Acrocephalus and Hippolais warblers (Aves: Sylviidae). Mol Phylogenet Evol 11:246–260

    Article  PubMed  CAS  Google Scholar 

  • Hesseltine CW, Ellis JJ (1961) Notes on Mucorales, especially Absidia. Mycologia 53:406–426

    Article  Google Scholar 

  • Hesseltine CW, Ellis JJ (1964) The genus Absidia: Gongronella and cylindrical-spored species of Absidia. Mycologia 56:568–601

    Article  Google Scholar 

  • Hesseltine CW, Ellis JJ (1966) Species of Absidia with ovoid sporangiospores I. Mycologia 58:761–785

    Article  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbs 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 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

    Article  PubMed  Google Scholar 

  • Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244

    Article  PubMed  CAS  Google Scholar 

  • Higgins DG, Sharp PM (1989) Fast and sensitive multiple sequence alignments on a microcomputer. Comp Appl Biosciences 5:151–153

    CAS  Google Scholar 

  • Hoffmann K, Discher S, Voigt K (2007) Revision of the genus Absidia (Mucorales, Zygomycetes): based on physiological, phylogenetic and morphological characters: thermotolerant Absidia spp form a coherent group, the Mycocladiaceae fam nov. Mycol Res 111:1169–1183

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann K, Telle S, Walther G, Eckart M, Kirchmair M, Prillinger H, Prazenica A, Newcombe G, Dölz F, Papp T, Vágvölgyi C, deHoog S, Olsson L, Voigt K (2009a) Diversity, genotypic identification, ultrastructural and phylogenetic characterization of zygomycetes from different ecological habitats and climatic regions: limitations and utility of nuclear ribosomal DNA barcode markers. In: Gherbawy Y, Mach RL, Rai M (eds) Current advances in molecular mycology. Nova Science Publishers, Inc, New York, pp 263–312

    Google Scholar 

  • Hoffmann K, Walther G, Voigt K (2009b) Mycocladus vs Lichtheimia: a correction (Lichtheimiaceae fam. nov., Mucorales, Mucoromycotina). Mycol Res 113:277–278

    Google Scholar 

  • Hong SB, Go SJ, Shin HD, Frisvad JC, Samson RA (2005) Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97:1316–1329

    Article  PubMed  CAS  Google Scholar 

  • Hong SB, Cho HS, Shin HD, Frisvad JC, Samson RA (2006) Novel Neosartorya species isolated from soil in Korea. Int J Syst Evol Microbiol 56:477–486

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Iwen PC, Freifeld AG, Sigler L, Tarantolo SR (2005) Molecular identification of Rhizomucor pusillus as a cause of sinus-orbital zygomycosis in a patient with acute myelogenous leukaemia. J Clin Microbiol 43:5819–5821

    Article  PubMed  CAS  Google Scholar 

  • Iwen PC, Sigler L, Noel RK, Freifeld AG (2007) Mucor circinelloides was identified by molecular methods as a cause of primary cutaneous zygomycosis. J Clin Microbiol 45:636–640

    Article  PubMed  CAS  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox C, 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 J, 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 J, Vilgalys R (2006) Reconstructing the early evolution of the fungi using a six-gene phylogeny. Nature 443:818–822

    Article  PubMed  CAS  Google Scholar 

  • James TY, Letcher PM, Longcore JE, Mozley-Strandridge SE, Porter D, Powell MJ, Griffith GW, Vilgalys R (2007) A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98:860–871

    Article  Google Scholar 

  • Johnson NK, Cicero C (2004) New mitochondrial DNA data affirm the importance of Pleistocene speciation in North American birds. Evolution 58:1122–1130

    PubMed  Google Scholar 

  • Kirk PM, Cannon PF, David JC, Stalpers JA (2001) Ainsworth & Bisby´s Dictionary of the fungi, 9th edn. CABI Publishing, Wallingford, United Kingdom

    Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CABI Publishing, Wallingford, United Kingdom

    Google Scholar 

  • Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnHpsbA spacer region. PLoS ONE 2:e508

    Article  CAS  Google Scholar 

  • Kress WJ, Wurdack KJ, Zimmer EA, Weigt LA, Janzen DH (2005) Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci USA 102:8369–8374

    Article  PubMed  CAS  Google Scholar 

  • Lemer S, Aurelle D, Vigliola L, Durand JD, Borsa P (2007) Cytochrome b barcoding, molecular systematics and geographic differentiation in rabbitfishes (Siganidae). C R Biol 330:86–94

    Article  PubMed  CAS  Google Scholar 

  • Leslie JF, Summerell BA (2006) Fusarium laboratory manual, 1st edn. Ames, Iowa (ua), Blackwell Publishers, pp 1–388

    Google Scholar 

  • Liu X, Huang H, Zheng R (2008) Delimitation of Rhizopus varieties based on IGS rDNA. Sydowia 60:93–112

    Google Scholar 

  • Liou G, Chen S, Wei H, Lee F, Fu H, Yuan G, Stalpers JA (2007) Polyphasic approach to the taxonomy of the Rhizopus stolonifer group. Mycol Res 111:196–203

    Article  PubMed  Google Scholar 

  • Lopandic K, Prillinger H, Molnar O, Gimenez -Jurado G (1996) Molecular characterisation and genotypic identification of Metschnikowia species. Syst Appl Microbiol 19:393–402

    Article  Google Scholar 

  • Metellus P, Laghmari M, Fuentes S, Eusebio A, Adetchessi T, Ranque S, Bouvier C, Dufour H, Grisoli F (2008) Successful treatment of a giant isolated cerebral mucormycotic (zygomycotic) abscess using endoscopic debridement: case report and therapeutic considerations. Surg Neurol 69:510–515

    Article  PubMed  Google Scholar 

  • Meyer CP, Paulay G (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biol 3:2229–2238

    CAS  Google Scholar 

  • Michailides TJ, Spotts RA (1990) Postharvest diseases of pome and stone fruits caused by Mucor piriformis in the Pacific northwest and California. Plant Dis 74:537–543

    Article  Google Scholar 

  • Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 10:311–324

    Article  PubMed  CAS  Google Scholar 

  • Moritz C, Cicero C (2004) DNA barcoding: promise and pitfalls. PloS Biol 2:1529–1531

    Article  CAS  Google Scholar 

  • Newmaster SG, Fazekas AJ, Ragupathy S (2006) DNA barcoding in land plants: evaluation of rbcL in a multigene tiered approach. Can J Bot 84:335–341

    Article  CAS  Google Scholar 

  • Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson K-H, Kõljalg U (2006) Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PloS ONE 1:e59

    Article  CAS  Google Scholar 

  • Nucci M, Marr KA (2005) Emerging fungal diseases. Clin Infect Dis 41:521–526

    Article  PubMed  Google Scholar 

  • O’Donnell K (2000) Molecular phylogeny of the Nectria haematococca – Fusarium solani species complex. Mycologia 92:919–938

    Article  Google Scholar 

  • O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phyl Evol 7:103–116

    Article  Google Scholar 

  • O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493

    Article  Google Scholar 

  • O’Donnell K, Gherbawy Y, Schweigkofler W, Adler A, Prillinger H (1999) Comparative phylogenetic analysis of Fusarium oxysporum and related species from maize using DNA sequence and RAPD data. J Phytopathol 147:445–452

    Article  Google Scholar 

  • O’Donnell K, Kistler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci USA 97:7905–7910

    Article  PubMed  Google Scholar 

  • O’Donnell K, Lutzoni FM, Ward TJ, Benny GL (2001) Evolutionary relationships among mucoralean fungi (Zygomycota): evidence for family polyphyly on a large scale. Mycologia 93:286–296

    Article  Google Scholar 

  • Ogawa JM, Sonada RM, English H (1992) Postharvest diseases of tree fruit. In: Kumar J, Chaube HS, Singh US, Mukhopadhyay AN (eds) Plant diseases on international importance, vol III. Englewood Cliffs, Diseases of fruit crops Prentice Hall, pp 405–422

    Google Scholar 

  • Park MH, Sim CJ, Baek J, Min GS (2007) Identification of genes suitable for DNA barcoding of morphologically indistinguishable korean halichondriidae sponges. Mol Cells 23:220–227

    PubMed  CAS  Google Scholar 

  • Pegler DN (2000) Taxonomy, nomenclature and description of Armillaria. In: Fox RTV (ed) Armillaria Root Rot: biology and control of honey fungus. Intercept, Andover, pp 81–93

    Google Scholar 

  • Pringle A, Baker DM, Platt JL, Wares JP, Latge JP, Taylor JW (2005) Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59:1886–1899

    PubMed  CAS  Google Scholar 

  • Raper KB, Fennell DI (1965) The genus Aspergillus. Williams and Wilkins Company, Baltimore, pp 1–686

    Google Scholar 

  • Raper KB, Thom C (1949) Manual of the penicillia. Williams and Wilkins Company, Baltimore, pp 1–875

    Google Scholar 

  • Ribes JA, Vanover-Sams CL, Baker DJ (2000) Zygomycetes in human disease. Clin Microbiol Rev 13:236–301

    Article  PubMed  CAS  Google Scholar 

  • Roden MM, Theoklis TZ, Buchanan WL, Knudsen TA, Sarkisova TA, Schaufele RL, Sein M, Sein T, Chiou CC, Chu JH, Kontoyiannis DP, Walsh TJ (2005) Epidemiology and outcome of Zygomycosis: a review of 929 reported cases. Clin Infect Dis 41:634–653

    Article  PubMed  Google Scholar 

  • Rogers TR (2008) Treatment of zygomycosis: current and new options. J Antimicrob Chemother 61:35–40

    Article  CAS  Google Scholar 

  • Rogers JS, Swofford DL (1998) A fast method for approximating maximum likelihood of phylogentic trees from nucleotide sequences. Syst Biol 47:77–89

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Samson RA, Frisvad JC (eds) (2004) Penicillium subgenus Penicillium: new taxonomic schemes, mycotoxins and other extrolites. Stud Mycol 49:1–251

    Google Scholar 

  • Samson RA, Seifert KA, Kuijpers AFA, Houbraken JAMP, Frisvad JC (2004) Phylogenetic analysis of Penicillium subgenus Penicillium using partial beta-tubulin sequences. Stud Mycol 49:175–200

    Google Scholar 

  • Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans R Soc Lond B 360:1879–1888

    Article  CAS  Google Scholar 

  • Schipper MAA (1973) A study on variability in Mucor hiemalis and related species. Stud Mycol (Baarn) 4:1–40

    Google Scholar 

  • Schipper MAA (1975) Mucor mucedo, Mucor flavus and related species. Stud Mycol (Baarn) 10:1–33

    Google Scholar 

  • Schipper MAA (1976) Mucor circinelloides, Mucor racemosus and related species. Stud Mycol (Baarn) 12:1–40

    Google Scholar 

  • Schipper MAA (1984) A revision of the genus Rhizopus I The Rhizopus stolonifer-group and Rhizopus oryzae. Stud Mycol (Baarn) 25:1–19

    Google Scholar 

  • Schipper MAA (1990) Notes on Mucorales – I Observations on Absidia. Persoonia 14:133–149

    Google Scholar 

  • Schipper MAA, Stalpers JA (1984) A revision of the genus Rhizopus II The Rhizopus microsporus-group. Stud Mycol (Baarn) 25:20–34

    Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schwarz P, Bretagne S, Gantier J-C, García-Hermoso D, Lortholary O, Dromer F, Dannaoui E (2006) Molecular identification of Zygomycetes from culture and experimentally infected tissues. J Clin Microbiol 44:340–349

    Article  PubMed  CAS  Google Scholar 

  • Seifert KA, Samson RA, deWaard JR, Houbraken J, Lévesque CA, Moncalvo J-M, Louis-Seize G, Hebert PDN (2007) Prospects for fungus identification using CO1 DNA barcodes, with Penicillium as a test case. PNAS 104:3901–3906

    Article  PubMed  CAS  Google Scholar 

  • Singh J, Rimek D, Kappe R (2005) In vitro susceptibility of 15 strains of Zygomycetes to nine antifungal agents as determined by the NCCLS M38-A microdilution method. Mycoses 48:246–250

    Article  PubMed  CAS  Google Scholar 

  • Skouboe P, Boysen M, Pedersen LH, Frisvad JC, Rossen L (1996) Identification of penicillium species using the internal transcribed spacer (ITS) regions. In: Rossen L, Rubio V, Dawson MT, Frisvad JC (eds) Fungal identification techniques. European Commission, Brussels, Belgium, pp 160–164

    Google Scholar 

  • Skouboe P, Frisvad JC, Taylor JW, Lauritsen D, Boysen M, Rossen L (1999) Phylogenetic analysis of nucleotide sequences from the ITS region of terverticillate Penicillium species. Mycol Res 103:873–881

    Article  CAS  Google Scholar 

  • Sugiyama J (1998) Relatedness, phylogeny, and evolution of the fungi. Mycoscience 39:487–511

    Article  Google Scholar 

  • Summerbell RC, Moore MK, Starink–Willemse M, Van Iperen A (2007) ITS barcodes for Trichophyton tonsurans and T equinum. Med Mycol 45:193–200

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (1998) PAUP*: phylogenetic analysis using parsimony (*and other methods) version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Tavares ES, Baker AJ (2008) Single mitochondrial gene barcodes reliably identify sister-species in diverse clades of birds. BMC Evol Biol 8:81

    Article  PubMed  CAS  Google Scholar 

  • Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21–32

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Trifilio SM, Bennett CL, Yarnold PR, McKoy JM, Parada J, Mehta J, Chamilos G, Palella F, Kennedy L, Mullane K, Tallman MS, Evens A, Scheetz MH, Blum W, Kontoyiannis DP (2007) Breakthrough zygomycosis after voriconazole administration among patients with hematologic malignancies who receive hematopoietic stem-cell transplants or intensive chemotherapy. Bone Marrow Transplant 39:425–429

    Article  PubMed  CAS  Google Scholar 

  • Valentini A, Pompanon F, Taberlet P (2009) DNA barcoding for ecologists. Trends Ecol Evol 24:110–117

    Article  PubMed  Google Scholar 

  • van de Peer Y, Baldauf SL, Doolittle WF, Meyer A (2000) An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate calibrated evolutionary distances. J Mol Evol 51:565–576

    PubMed  Google Scholar 

  • Vences M, Thomas M, Bonett RM, Vieites DR (2005) Deciphering amphibian diversity through DNA barcoding: chances and challenges. PhilOS Trans Soc Lond B 360:1859–1868

    Article  CAS  Google Scholar 

  • Vogelstein B, Gillespie D (1979) Preparative and analytical purification of DNA from agarose. Proc Natl Acad Sci USA 76:615–619

    Article  PubMed  CAS  Google Scholar 

  • Voigt K, Wöstemeyer J (2001) Phylogeny and origin of 82 zygomycetes from all 54 genera of the Mucorales and Mortierellales based on combined analysis of actin and translation elongation factor EF-1alpha genes. Gene 270:113–120

    Article  PubMed  CAS  Google Scholar 

  • Voigt K, Cigelnik E, O’Donnell K (1999) Phylogeny and PCR identification of clinical important Zygomycetes based on nuclear ribosomal-DNA sequence data. J Clin Microbiol 37:3957–3964

    PubMed  CAS  Google Scholar 

  • Voigt K, Hoffmann K, Einax E, Eckart M, Papp T, Vágvölgyi L, Olsson L (2009) Revision of the family structure of the Mucorales (Mucoromycotina, Zygomycetes) based on multigene-genealogies: Phylogenetic analyses suggest a bigeneric phycomycetaceae with spinellus as sister group to phycomyces. In: Gherbawy Y, Mach RL, Rai M (eds) Current advances in molecular mycology. Nova Science, New York, pp 263–312

    Google Scholar 

  • Walsh TJ, Groll A, Hiemenz J, Fleming R, Roilides E, Anaissie E (2004) Infections due to emerging and uncommon medically important fungal pathogens. Clin Microbiol Infect 10:48–66

    Article  PubMed  Google Scholar 

  • Weitzman I, McGough DA, Rinaldi MG, Della-Lata P (1996) Rhizopus schipperae, sp nov, a new agent of zygomycosis. Mycotaxon 59:217–225

    Google Scholar 

  • Wheeler QD (2004) Taxonomic triage and the proverty of phylogeny. Philos Trans R Soc B 359:571–583

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (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. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • White MM, James TY, O’Donnell K, Cafaro MJ, Tanabe Y, Sugiyama J (2006) Phylogeny of the Zygomycota based on nuclear ribosomal sequence data. Mycologia 98:872–884

    Article  PubMed  Google Scholar 

  • Wiemers M, Fiedler K (2007) Does the DNA barcoding gap exist? – a case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zool 4:8

    Article  PubMed  CAS  Google Scholar 

  • Wollenweber HW, Reinking OA (1935) Die Fusarien, ihre Beschreibung. Schadwirkung und Bekämpfung Parey, Berlin, pp 1–355

    Google Scholar 

  • Woo PC, Zhen H, Cai JJ, Yu J, Lau SK, Wang J, Teng JL, Wong SS, Tse RH, Chen R, Yang H, Lui B, Yuen KY (2003) The mitochondrial genome of the thermal dimorphic fungus Penicillium marneffei is more closely related to those of molds than yeasts. FEBS Lett 555:56–477

    Article  CAS  Google Scholar 

  • Yarlett N, Orpin CG, Munn EA, Yarlett NC, Greenwood CA (1986) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 15:729–739

    Google Scholar 

  • Zheng RY, Chen GQ, Liu XY (2000) Rhizopus americanus stat. nov. Mycosystema 19:473–477

    Google Scholar 

  • Zheng RY, Chen GQ, Huang H, Liu XY (2007) A monograph of Rhizopus. Sydowia 59:273–372

    Google Scholar 

  • Zycha H (1935) Pilze II. Mucorineae. Krypt Fl Mark Brandenburg 6a, Leipzig

    Google Scholar 

  • Zycha H, Siepmann R, Linnemann G (1969) Mucorales. eine beschreibung aller gattungen und arten dieser pilzgruppe. J Cramer, Lehre

    Google Scholar 

Download references

Acknowledgements

The authors wish to thank Martin Kirchmair (University of Innsbruck, Austria) who kindly provided the zygomycetes strains FSU6510-6527 and Roman Schwarz (Medizinisches Versorgungszentrum, Mönchengladbach, Germany) who kindly provided the zygomycetes strains FSU6529, FSU6530, FSU6250-6252, FSU6274.

Author information

Authors and Affiliations

  1. Botany Department, Faculty of Science, South Valley University, 83523, Qena, Egypt

    Youssuf Gherbawy & Claudia Kesselboth

  2. Institute of Microbiology, School of Biology and Pharmacy, University of Jena, Neugasse 25, 07743, Jena, Germany

    Kerstin Hoffmann

  3. Biological Sciences Department, Faculty of Science, Taif University, 888, Taif, Kingdom of Saudi Arabia

    Hesham Elhariry

Authors
  1. Youssuf Gherbawy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Kesselboth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hesham Elhariry
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kerstin Hoffmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kerstin Hoffmann .

Editor information

Editors and Affiliations

  1. Fac. Science, Dept. Botany, South Valley University, Qena, Egypt

    Youssuf Gherbawy

  2. School of Biology and Pharmacy, Institute of Microbiology, University of Jena, Neugasse 24, Jena, 07743, Germany

    Kerstin Voigt

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Gherbawy, Y., Kesselboth, C., Elhariry, H., Hoffmann, K. (2010). Molecular Barcoding of Microscopic Fungi with Emphasis on the Mucoralean Genera Mucor and Rhizopus . In: Gherbawy, Y., Voigt, K. (eds) Molecular Identification of Fungi. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-05042-8_11

Download citation

Publish with us

Policies and ethics

Search

Navigation