Skip to main content

15 Genetic and Metabolic Aspects of Primary and Secondary Metabolism of the Zygomycetes

  • Chapter
  • First Online:

Part of the book series: The Mycota ((MYCOTA,volume III))

Abstract

Basal lineages of the kingdom of fungi comprise terrestrial and aquatic fungi, which are traditionally summarized as Chytridiomycota and Zygomycota in a colloquial sense. The zygomycetes build up the most basal lineage among the terrestrial fungi. As the earliest fungi to conquer terrestrial habitats, they facilitated early coevolution with other land-dwelling microorganisms with implications on the primary and secondary metabolism which is adaptive to the life in soil. Advances in next-generation genome sequencing allow us to gain a new layer of knowledge with respect to their metabolism and its regulation. Recent revisions of the metabolic potential of zygomycetes using genome mining suggested a hidden potential for the production of secondary metabolites. First insights suggest a revision of our understanding of the importance and mode of action of metabolic pathways revealing a fascinating potential to produce novel natural compounds. The aim of this review is to draw attention to the zygomycetes as a unique fungal group and to inspire the scientific community to explore its potential as participants in complex ecosystems for innovative metabolic regulatory frameworks and novel compounds.

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

Buying options

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

Learn about institutional subscriptions

References

  • Abe A, Oda Y, Asano K, Sone T (2007) Rhizopus delemar is the proper name for Rhizopus oryzae fumaric-malic acid producers. Mycologia 99:714–722

    Article  PubMed  CAS  Google Scholar 

  • Álvarez V, Rodríguez-Sáiz M, de la Fuente JL, Gudiña EJ, Godio RP, Martín JF, Barredo JL (2006) The crtS gene of Xanthophyllomyces dendrorhous encodes a novel cytochrome-P450 hydroxylase involved in the conversion of β-carotene into astaxanthin and other xanthophylls. Fungal Genet Biol 43:261–272

    Article  PubMed  CAS  Google Scholar 

  • Anonymus (2007) Product focus: maleic anhydride. Chem Week 39

    Google Scholar 

  • Appel KF, Wolff AM, Arnau J (2004) A multicopy vector system for genetic studies in Mucor circinelloides and other zygomycetes. Mol Genet Genomics 271:595–602

    Article  PubMed  CAS  Google Scholar 

  • Arrach N, Fernández-Martín R, Cerdá-Olmedo E, Avalos J (2001) A single gene for lycopene cyclase, phytoene synthase, and regulation of carotene biosynthesis in Phycomyces. Proc Natl Acad Sci USA 98:1687–1692

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Azeke MA, Greiner R, Jany KD (2011) Purification and characterization of two intracellular phytases from the tempeh fungus Rhizopus oligosporus. J Food Biochem 35:213–227

    Article  CAS  Google Scholar 

  • Bai DM, Li SZ, Liu ZL, Cui ZF (2008) Enhanced L-(+)-lactic acid production by an adapted strain of Rhizopus oryzae using corncob hydrolysate. Appl Biochem Biotechnol 144:79–85

    Article  PubMed  CAS  Google Scholar 

  • Bartnicki-Garcia S (1968) Control of dimorphism in Mucor by hexoses: inhibition of hyphal morphogenesis. J Bacteriol 96:1586–1594

    PubMed Central  PubMed  CAS  Google Scholar 

  • Beg QK, Kapoor M, Mahajan L, Hoondal GS (2001) Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 56:326–338

    Article  PubMed  CAS  Google Scholar 

  • Benny GL, Humber RA, Voigt K (2014) Zygomycetous Fungi: phylum Entomophthoromycota and subphyla Kickxellomycotina, Mortierellomycotina, Mucoromycotina, and Zoopagomycotina. In: McLaughlin DJ, Spatafora JW (eds) The Mycota, vol VIIA, 2nd edn, Systematics and evolution. Springer, Berlin, pp 209–250, Chapter 8

    Google Scholar 

  • Bianciotto V, Lumini E, Bonfante P, Vandamme P (2003) “Candidatus Glomeribacter gigasporarum” gen. nov, sp. nov., an endosymbiont of arbuscular mycorrhizal fungi. Int J Syst Evol Microbiol 53:121–124

    Article  PubMed  CAS  Google Scholar 

  • Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn of symbiosis between plants and fungi. Biol Lett 7:574–577

    Article  PubMed Central  PubMed  Google Scholar 

  • Bitar D, Van Cauteren D, Lanternier F, Dannaoui E, Che D, Dromer F, Desenclos JC, Lortholary O (2009) Increasing incidence of zygomycosis (mucormycosis), France, 1997-2006. Emerg Infect Dis 15:1395–1401

    Article  PubMed Central  PubMed  Google Scholar 

  • Bonito G, Gryganskyi A, Hameed K, Schadt C, Pelletier D, Schaefer A, Tuskan G, Labbe J, Martin F, Doktycz M, LaButti K, Ohm R, Grigoriev I, Vilgalys R (2013) Co-evolution of Mortierella elongata and its endosymbiotic bacterium. In: Abstracts submitted for presentation at the 2013 APS-MSA joint meeting, Austin, TX (2013-08-10–2013-08-14). St. Paul. American Phytopathological Society. Phytopathology 103 (6, Suppl 2):18–19 Presented at APS-MSA Joint Meeting

    Google Scholar 

  • Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32

    Article  PubMed  CAS  Google Scholar 

  • Bulut S, Elibol M, Ozer D (2009) Optimization of process parameters and culture medium for L-(+)-lactic acid production by Rhizopus oryzae. J Chem Eng Jpn 42:589–595

    Article  CAS  Google Scholar 

  • Burmester A, Richter M, Schultze K, Voelz K, Schachtschabel D, Boland W, Wöstemeyer J, Schimek C (2007) Cleavage of β-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated β-carotene oxygenase. Fungal Genet Biol 44:1096–1108

    Article  PubMed  CAS  Google Scholar 

  • Cao NJ, Du JX, Gong CS, Tsao GT (1996) Simultaneous production and recovery of fumaric acid from immobilized Rhizopus oryzae with a rotary biofilm contractor and adsorption column. Appl Environ Microbiol 62:2926–2931

    PubMed Central  PubMed  CAS  Google Scholar 

  • Casadevall A, Pirofski L (2001) Host-pathogen interactions. The attributes of virulence. J Infect Dis 184(3):337–344

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? BioSystems 14:461–481

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti A, Chatterjee SS, Shivaprakash MR (2008) Overview of opportunistic fungal infections in India. Nihon Ishinkin Gakkai Zasshi 49:165–172

    Article  PubMed  Google Scholar 

  • Chakrabarti A, Chatterjee SS, Das A, Panda N, Shivaprakash MR, Kaur A, Varma SC, Singhi S, Bhansali A, Sakhuja V (2009) Invasive zygomycosis in India: experience in a tertiary care hospital. Postgrad Med J 85:573–581

    Article  PubMed  CAS  Google Scholar 

  • Chamilos G, Lewis RE, Kontoyiannis DP (2007) Multidrug-resistant endosymbiotic bacteria account for the emergence of zygomycosis: a hypothesis. Fungal Genet Biol 44(2):88–92

    Article  PubMed  CAS  Google Scholar 

  • Chang Y, Wang S, Sekimoto S, Aerts AL, Choi C, Clum A, LaButti KM, Lindquist EA, Yee Ngan C, Ohm RA, Salamov AA, Grigoriev IV, Spatafora JW, Berbee ML (2015) Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol 7(6):1590–1601

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chatzifragkou A, Makri A, Belka A, Bellou S, Mavrou M, Mastoridou M, Mystrioti P, Onjaro G, Aggelis G, Papanikolaou S (2011) Biotechnological conversions of biodiesel derived waste glycerol by yeast and fungal species. Energy 36:1097–1108

    Article  CAS  Google Scholar 

  • Chaudhuri S, Ghosh S, Bhattacharyya DK, Bandyopadhyay S (1998) Effect of mustard meal on the production of arachidonic acid by Mortierella elongata SC-208. J Am Oil Chem Soc 75:1053–1055

    CAS  Google Scholar 

  • Chayakulkeeree M, Ghannoum MA, Perfect JR (2006) Zygomycosis: the re-emerging fungal infection. Eur J Clin Microbiol Infect Dis 25:215–229

    Article  PubMed  CAS  Google Scholar 

  • Csernetics Á, Nagy G, Iturriaga EA, Szekeres A, Eslava AP, Vágvölgyi CS, Papp T (2011) Expression of three isoprenoid biosynthesis genes and their effects on the carotenoid production of the zygomycete Mucor circinelloides. Fungal Genet Biol 48:696–703

    Article  PubMed  CAS  Google Scholar 

  • Csernetics Á, Tóth E, Farkas A, Nagy G, Bencsik O, Vágvölgyi C, Papp T (2015) Expression of Xanthophyllomyces dendrorhous cytochrome-P450 hydroxylase and reductase in Mucor circinelloides. World J Microbiol Biotechnol 31:321–336

    Article  PubMed  CAS  Google Scholar 

  • Czempinski K, Kruft V, Wöstemeyer J, Burmester A (1996) 4-dihydromethyltrisporate dehydrogenase from Mucor mucedo, an enzyme of the sexual hormone pathway:purification, and cloning of the corresponding gene. Microbiology 142:2647–2654

    Article  PubMed  CAS  Google Scholar 

  • de Azevedo Santiago AL, de Souza Motta CM (2008) Isolation of Mucorales from processed maize (Zea mays L.) and screening for protease activity. Braz J Microbiol 39:698–700

    Article  PubMed Central  PubMed  Google Scholar 

  • de Hoog GS, Guarro J, Genè J, Figueras MJ (2000) Zygomycota. In: Atlas of clinical fungi, pp 58–124, Centraalbureau voor Schimmelcultures, Universitat Rovira I Virgili, Utrecht, The Netherlands

    Google Scholar 

  • de Hoog GS, Ibrahim AS, Voigt K (2014) Emerging zygomycetes: an emerging problem in the clinical laboratory. Mycoses 57(Suppl 3):1

    Article  PubMed Central  PubMed  Google Scholar 

  • Dedyukhina E, Chistyakova T, Vainshtein M (2011) Biosynthesis of arachidonic acid by micromycetes (review). Appl Biochem Microbiol 47:109–117

    Article  CAS  Google Scholar 

  • Delalibera I Jr, Hajek AE, Humber RA (2003) Use of cell culture media for cultivation of the mite pathogenic fungi Neozygites tanajoae and Neozygites floridana. J Invertebr Pathol 84:119–127

    Article  PubMed  Google Scholar 

  • Deng Y, Li S, Xu Q, Gao M, Huang H (2012) Production of fumaric acid by simultaneous saccharification and fermentation of starchy materials with 2-deoxyglucose-resistant mutant strains of Rhizopus oryzae. Bioresour Technol 107:363–367

    Article  PubMed  CAS  Google Scholar 

  • Dolatabadi S, de Hoog GS, Meis JF, Walther G (2014a) Species boundaries and nomenclature of Rhizopus arrhizus (syn. R. oryzae). Mycoses 57:108–127

    Article  PubMed  CAS  Google Scholar 

  • Dolatabadi S, Walther G, van den Ende AHGG, de Hoog GS (2014b) Diversity and delimitation of Rhizopus microsporus. Fungal Div 64:145–163

    Article  Google Scholar 

  • Dufossé L (2006) Microbial production of food grade pigments. Food Technol Biotechnol 44:313–321

    Google Scholar 

  • Dufossé L (2008) Pigments from microalgae and microorganisms: sources of food colorants. In: Sociaciu C (ed) Food colorants, chemical and functional properties. CRC Press, Boca Raton, FL, pp 399–427

    Google Scholar 

  • Dyal SD, Narine SS (2005) Implications for the use of Mortierella fungi in the industrial production of essential fatty acids. Food Res Int 38:445–467

    Article  CAS  Google Scholar 

  • Dyal SD, Bouzidi L, Narine SS (2005) Maximizing the production of γ-linolenic acid in Mortierella ramanniana var. ramanniana as a function of pH, temperature and carbon source, nitrogen source, metal ions and oil supplementation. Food Res Int 38:815–829

    Article  CAS  Google Scholar 

  • Fakas S, Papanikolaou S, Batsos A, Galiotou-Panayotou M, Mallouchos A, Aggelis G (2009) Evaluating renewable carbon sources as substrates for single cell oil production by Cunninghamella echinulata and Mortierella isabellina. Biomass Bioenergy 33:573–580

    Article  CAS  Google Scholar 

  • Ferreira JA, Lennartsson PR, Edebo L, Taherzadeh MJ (2013) Zygomycetes-based biorefinery: Present status and future prospects. Bioresour Technol 135:523–532

    Article  PubMed  CAS  Google Scholar 

  • Fujimura R, Nishimura A, Ohshima S, Sato Y, Nishizawa T, Oshima K, Hattori M, Narisawa K, Ohta H (2014) Draft Genome Sequence of the Betaproteobacterial Endosymbiont Associated with the Fungus Mortierella elongata FMR23-6. Genome Announc 2(6):e01272-14

    Article  PubMed Central  PubMed  Google Scholar 

  • Gao D, Zeng J, Zheng Y, Yu X, Chen S (2013) Microbial lipid production from xylose by Mortierella isabellina. Bioresour Technol 133:315–321

    Article  PubMed  CAS  Google Scholar 

  • Garre V, Barredo JL, Iturriaga EA (2015) Transformation of Mucor circinelloides f. lusitanicus protoplasts. In: van den Berg MA, Maruthachalam K (eds) Genetic transformation systems in fungi, Volume 1. Springer International Publishing, pp 49–59

    Google Scholar 

  • Ghignone S, Salvioli A, Anca I, Lumini E, Ortu G, Petiti L, Cruveiller S, Bianciotto V, Piffanelli P, Lanfranco L, Bonfante P (2012) The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions. ISME J 6(1):136–145

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Goldberg I, Rokem JS, Pines O (2006) Organic acids: old metabolites, new themes. J Chem Tech Biotechnol 81:1601–1611

    Article  CAS  Google Scholar 

  • Gooday GW (1974) Fungal sex hormones. Annu Rev Biochem 43:35–49

    Article  PubMed  CAS  Google Scholar 

  • Gopinath SCB, Anbu P, Lakshmipriya T, Hilda A (2013) Strategies to characterize fungal lipases for applications in medicine and dairy industry. Biomed Res Int 2013:1545–1549

    Article  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 

  • Grundschober A, Tuor U, Aebi M (1998) In vitro cultivation and sporulation of Neozygites parvispora (Zygomycetes: Entomophthorales). Syst Appl Microbiol 21:461–469

    Article  Google Scholar 

  • Gryganskyi AP, Lee SC, Litvintseva AP, Smith ME, Bonito G, Porter T, Anishchenko IM, Heitman J, Vilgalys R (2010) Structure, function, and phylogeny of the mating locus in the Rhizopus oryzae complex. PLoS One 5(12), e15273

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Guo Y, Yan Q, Jiang Z, Teng C, Wang X (2010) Efficient production of lactic acid from sucrose and corncob hydrolysate by a newly isolated Rhizopus oryzae GY18. J Ind Microbiol Biotechnol 37:1137–1143

    Article  PubMed  CAS  Google Scholar 

  • Gutiérrez A, López-García S, Garre V (2011) High reliability transformation of the basal fungus Mucor circinelloides by electroporation. J Microbiol Met 84:442–446

    Article  CAS  Google Scholar 

  • Hawksworth DL (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. MycoKeys 1:7–20

    Article  Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    Article  PubMed  CAS  Google Scholar 

  • Hesseltine CW (1983) Microbiology of oriental fermented foods. Annu Rev Microbiol 37:575–601

    Article  PubMed  CAS  Google Scholar 

  • Hesseltine CW (1991) Zygomycetes in food fermentations. Mycologist 5:162–169

    Article  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson O, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch T, 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 K, Köljalb U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto R, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schuessler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang A, Weir A, Weiss M, White M, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547

    Article  PubMed  Google Scholar 

  • Hoffmann K, Telle S, Walther G, Eckart M, Kirchmair M, Prillinger HJ, Prazenica A, Newcombe G, Dölz F, Papp T, Vágvölgyi C, de Hoog S, Olsson L, Voigt K (2009) 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, New York, pp 263–312

    Google Scholar 

  • Hoffmann K, Voigt K, Kirk PM (2011) Mortierellomycotina subphyl. nov. based on multi-gene genealogies. Mycotaxon 115:353–363

    Article  Google Scholar 

  • Hoffmann K, Pawlowska J, Walther G, Wrzosek M, de Hoog GS, Benny GL, Kirk PM, Voigt K (2013) The family structure of the Mucorales: a synoptic revision based on comprehensive multigene-genealogies. Persoonia 30:57–76

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hou C (2008) Production of arachidonic acid and dihomo-linolenic acid from glycerol by oil-producing filamentous fungi, Mortierella in the ARS culture collection. J Ind Microbiol Biotechnol 35:501–506

    Article  PubMed  CAS  Google Scholar 

  • Huang C, Chen XF, Xiong L, Chen XD, Ma LL, Chen Y (2013) Single cell oil production from low-cost substrates: the possibility and potential of its industrialization. Biotechnol Adv 31(2):129–139

    Article  PubMed  CAS  Google Scholar 

  • Ibrahim AS (2011) Host cell invasion in mucormycosis: role of iron. Curr Opin Microbiol 14:406–411

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ibrahim AS, Gebremariam T, Liu M, Chamilos G, Kontoyiannis DP, Mink R, Kwon-Chung KJ, Fu Y, Skory CD, Edwards JE Jr, Spellberg B (2008) Bacterial Endosymbiosis is widely present among Zygomycetes but does not contribute to the pathogenesis of mucormycosis. J Infect Dis 198:1083–1090

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ikubo S, Takigawa N, Ueoka H, Kiura K, Tabata M, Shibayama T, Chikamori M, Aoe K, Matsushita A, Harada M (1999) In vitro evaluation of antimicrotubule agents in human small-cell lung cancer cell lines. Anticancer Res 19:3985–3988

    PubMed  CAS  Google Scholar 

  • Iturriaga EA, Díaz-Mínguez JM, Benito EP, Álvarez MI, Eslava AP (1992) Heterologous transformation of Mucor circinelloides with the Phycomyces blakesleeanus leu1 gene. Curr Genet 21:215–223

    Article  PubMed  CAS  Google Scholar 

  • Iturriaga EA, Velayos A, Eslava AP (2000) The structure and function of the genes involved in the biosynthesis of carotenoids in the Mucorales. Biotechnol Bioprocess Eng 5:263–274

    Article  CAS  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 AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of the fungi using a six-gene phylogeny. Nature 443:818–822

    Article  PubMed  CAS  Google Scholar 

  • Jang HD, Lin YY, Yang SS (2000) Polyunsaturated fatty acid production with Mortierella alpina by solid substrate fermentation. Bot Bull Acad Sin 41:41–48

    CAS  Google Scholar 

  • Jennessen J, Nielsen KF, Houbraken J, Lyhne EK, Schnürer J, Frisvad JC, Samson RA (2005) Secondary metabolite and mycotoxin production by the Rhizopus microsporus group. J Agric Food Chem 53(5):1833–1840

    Article  PubMed  CAS  Google Scholar 

  • Jin B, Yin P, Ma Y, Zhao L (2005) Production of lactic acid and fungal biomass by Rhizopus fungi from food processing waste water. J Ind Microbiol Biotechnol 32:678–686

    Article  PubMed  CAS  Google Scholar 

  • Jones SK Jr, Bennett RJ (2011) Fungal mating pheromones: choreographing the dating game. Fungal Genet Biol 48:668–676

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Karimi K, Zamani A (2013) Mucor indicus: biology and industrial application perspectives: a review. Biotechnol Adv 31:466–481

    Article  PubMed  CAS  Google Scholar 

  • Kauffman CA (2004) Zygomycosis: reemergence of an old pathogen. Clin Infect Dis 39:588–590

    Article  PubMed  Google Scholar 

  • Kavadia A, Komaitis M, Chevalot I, Blanchard F, Marc I, Aggelis G (2001) Lipid and gamma-linolenic acid accumulation in strains of zygomycetes growing on glucose. J Am Oil Chem Soc 78:341–346

    Article  CAS  Google Scholar 

  • Kloer DP, Ruch S, Al-Babili S, Beyer P, Schulz GE (2005) The structure of a retinal-forming carotenoid oxygenase. Science 8:267–269

    Article  CAS  Google Scholar 

  • Krisch J, Takó M, Papp T, Vágvölyi C (2010) Characteristics and potential use of β-glucosidases from Zygomycetes. In: Méndez-Vilas a (ed.) Current research, technology and education topics in applied microbiology and microbial biotechnology, Formatex Research Center, pp 891-896.

    Google Scholar 

  • Krizsán K, Bencsik O, Nyilasi I, Galgóczy L, Vágvölgyi C, Papp T (2010) Effect of the sesterterpene-type metabolites, ophiobolins A and B, on zygomycetes fungi. FEMS Microbiol Lett 313:135–140

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Jang Y, Lee YM, Lee J, Lee H, Kim GH, Kim JJ (2011) Rice straw-decomposing fungi and their cellulolytic and xylanolytic enzymes. J Microbiol Biotechnol 21:1322–1329

    Article  PubMed  CAS  Google Scholar 

  • Lee SC, Billmyre RB, Li A, Carson S, Sykes SM, Huh EY, Mieczkowski P, Ko DC, Cuomo CA, Heitman J (2014) Analysis of a food-borne fungal pathogen outbreak: virulence and genome of a Mucor circinelloides isolate from yogurt. mBio 5(4):e01390-14

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lennartsson PR, Karimi K, Edebo L, Taherzadeh MJ (2009) Effects of different growth forms of Mucor indicus on cultivation on dilute-acid lignocellulosic hydrolyzate, inhibitor tolerance, and cell wall composition. J Biotechnol 143:255–261

    Article  PubMed  CAS  Google Scholar 

  • Lichtwardt RW, Manier JF (1978) Validation of the Harpellales and Asellariales. Mycotaxon 7:441–442

    Google Scholar 

  • Liu XJ, Liu RS, Li HM, Tang YJ (2012) Lycopene production from synthetic medium by Blakeslea trispora NRRL2895(+) and 2896(-) in a stirred-tank fermenter. Bioprocess Biosyst Eng 35:739–749

    Article  PubMed  CAS  Google Scholar 

  • Lukács GY, Papp T, Somogyvári F, Csernetics Á, Nyilasi I, Vágvölgyi CS (2009) Cloning of the Rhizomucor miehei 3-hydroxy-3-methylglutaryl-coenzyme A reductase gene and its heterologous expression in Mucor circinelloides. Ant Leeuwenhoek 95:55–64

    Article  CAS  Google Scholar 

  • Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, Idnurm A, Lang BF, Sone T, Abe A, Calvo SE, Corrochano LM, Engels R, Fu J, Hansberg W, Kim JM, Kodira CD, Koehrsen MJ, Liu B, Miranda-Saavedra D, O’Leary S, Ortiz-Castellanos L, Poulter R, Rodriguez-Romero J, Ruiz-Herrera J, Shen YQ, Zeng Q, Galagan J, Birren BW, Cuomo CA, Wickes BL (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5, e1000549

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Medina HR, Cerdá-Olmedo E, Al-Babili S (2011) Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 82(1):199–208

    Article  PubMed  CAS  Google Scholar 

  • Mehta BJ, Salgado LM, Bejarano ER, Cerdá-Olmedo E (1997) New mutants of Phycomyces blakesleeanus for beta-carotene production. Appl Environ Microbiol 63:3657–3661

    PubMed Central  PubMed  CAS  Google Scholar 

  • Mendoza L, Vilela R, Voelz K, Ibrahim AS, Voigt K, Lee SC (2014) Human fungal pathogens of Mucorales and Entomophthorales, Chapter 27. In: Casadevall A, Mitchell AP, Berman J, Kwon-Chung KJ, Perfect JR, Heitman J (eds) Cold spring harbor perspectives: fungal pathogens. Cold Spring Harbor Press, Cold Spring Harb Perspect Med 5(4) pii: a019562

    Google Scholar 

  • Meussen BJ, de Graaff LH, Sanders JP, Weusthuis RA (2012) Metabolic engineering of Rhizopus oryzae for the production of platform chemicals. Appl Microbiol Biotechnol 94:875–886

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Millati R, Edebo L, Taherzadeh MJ (2005) Performance of Rhizopus, Rhizomucor, and Mucor in ethanol production from glucose, xylose, and wood hydrolyzates. Enzyme Microb Technol 36:294–300

    Article  CAS  Google Scholar 

  • Monteiro de Souza P, de Oliveira Magalhães P (2010) Application of microbial α-amylase in industry – a review. Braz J Microbiol 41(4):850–861

    CAS  Google Scholar 

  • Morace G, Borghi E (2012) invasive mold infections: virulence and pathogenesis of mucorales. Int J Microbiol 2012, Article ID 349278, 5 p

    Google Scholar 

  • Moss ST (1975) Commensalism of the trichomycetes. In: Batra LR (ed) Insect-fungus symbiosis: nutrition, mutualism and commensalism. Allanheld, Osmun & Co., Montclair, pp 175–227

    Google Scholar 

  • Mullaney EJ, Ullah AH (2003) The term phytase comprises several different classes of enzymes. Biochem Biophys Res Commun 312:179–184

    Article  PubMed  CAS  Google Scholar 

  • Mullaney EJ, Daly CB, Ullah AH (2000) Advances in phytase research. Adv Appl Microbiol 47:157–199

    Article  PubMed  CAS  Google Scholar 

  • Münchberg U, Wagner L, Spielberg ET, Voigt K, Rösch P, Popp J (2012) Spatially resolved investigation of the oil composition in single intact hyphae of Mortierella spp. with micro-Raman spectroscopy. Biochim Biophys Acta 1831:341–349

    Article  PubMed  CAS  Google Scholar 

  • Münchberg U, Wagner L, Rohrer C, Voigt K, Jahreis G, Rösch P, Popp J (2015) Quantitative assessment of the degree of lipid unsaturation in intact Mortierella by Raman microspectroscopy. Anal Bioanal Chem 407:3303–3311

    Article  PubMed  CAS  Google Scholar 

  • Nagy LG, Petkovits T, Kovács GM, Voigt K, Vágvölgyi C, Papp T (2011) Where is the unseen fungal diversity hidden? A study of Mortierella reveals a large contribution of reference collections to the identification of fungal environmental sequences. New Phytol 191:789–794

    Article  PubMed  Google Scholar 

  • Nagy G, Farkas A, Csernetics Á, Bencsik O, Szekeres A, Nyilasi I, Vágvölgyi CS, Papp T (2014) Transcription analysis of the three HMG-CoA reductase genes of Mucor circinelloides. BMC Microbiol 14:93

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nahas E (1988) Control of lipase production by Rhizopus oligosporus under various growth conditions. J Gen Microbiol 134:227–233

    CAS  Google Scholar 

  • Navarro E, Lorca-Pascual JM, Quiles-Rosillo MD, Nicolas FE, Garre V, Torres-Martinez S, Ruiz-Vazquez RM (2001) A negative regulator of light-inducible carotenogenesis in Mucor circinelloides. Mol Gen Genomics 266:463–470

    Article  CAS  Google Scholar 

  • Navarro E, Peñaranda A, Hansberg W, Torres-Martínez S, Garre V (2013) A white collar 1-like protein mediates opposite regulatory functions in Mucor circinelloides. Fungal Genet Biol 52:42–52

    Article  PubMed  CAS  Google Scholar 

  • Nicolás-Molina FE, Navarro E, Ruiz-Vázquez RM (2008) Lycopene over-accumulation by disruption of the negative regulator gene crgA in Mucor circinelloides. Appl Microbiol Biotechnol 78:131–137

    Article  PubMed  CAS  Google Scholar 

  • Nout MJR, Kiers JL (2005) Tempeh fermentation, innovation and functionality: update into the third millennium. J Appl Microbiol 98:789–805

    Article  PubMed  CAS  Google Scholar 

  • Nützmann HW, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F, Gacek A, Schümann J, Hertweck C, Strauss J, Brakhage AA (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci USA 108(34):14282–14287

    Article  PubMed Central  PubMed  Google Scholar 

  • Nützmann HW, Schroeckh V, Brakhage AA (2012) Regulatory cross talk and microbial induction of fungal secondary metabolite gene clusters. Methods Enzymol 517:325–341

    Article  PubMed  Google Scholar 

  • Obraztsova IN, Prados N, Holzmann K, Avalos J, Cerda-Olmedo E (2004) Genetic damage following introduction of DNA in Phycomyces. Fungal Genet Biol 41:68–180

    Article  CAS  Google Scholar 

  • Orlowsky M (1991) Mucor dimorphism. Microbiol Rev 55:234–258

    Google Scholar 

  • Osmani SA, Scrutton MC (1985) The sub-cellular localisation and regulatory properties of pyruvate carboxylase from Rhizopus arrhizus. Eur J Biochem 147:119–128

    Article  PubMed  CAS  Google Scholar 

  • Overman SA, Romano AH (1969) Pyruvate carboxylase of Rhizopus nigricans and its role in fumaric acid production. Biochem Biophys Res Commun 37:457–463

    Article  PubMed  CAS  Google Scholar 

  • Papp T, Velayos A, Bartók T, Eslava AP, Vágvölgyi CS, Iturriaga EA (2006) Heterologous expression of astaxanthin biosynthesis genes in Mucor circinelloides. Appl Microbiol Biotechnol 69:526–531

    Article  PubMed  CAS  Google Scholar 

  • Papp T, Csernetics Á, Nyilasi I, Ábrók M, Vágvölgyi CS (2010) Genetic transformation of Zygomycetes fungi. In: Rai MK, Kövics GJ (eds) Progress in mycology. Springer, Netherlands, pp 75–94

    Chapter  Google Scholar 

  • Papp T, Hoffmann K, Nyilasi I, Petkovits T, Wagner L, Vágvölgyi C, Voigt K (2011) Mortierella. In: Liu D (ed) Molecular detection of human fungal pathogens. Taylor & Francis CRC Press, pp 749–758

    Google Scholar 

  • Papp T, Csernetics Á, Nagy G, Bencsik O, Iturriaga EA, Eslava AP, Vágvölgyi CS (2013) Canthaxanthin production with modified Mucor circinelloides strains. Appl Microbiol Biotechnol 97:4937–4950

    Article  PubMed  CAS  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 10:763–775

    Article  CAS  Google Scholar 

  • Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888

    Article  PubMed  CAS  Google Scholar 

  • Partida-Martinez LP, Bandemer S, Rüchel R, Dannaoui E, Hertweck C (2008) Lack of evidence of endosymbiotic toxin-producing bacteria in clinical Rhizopus isolates. Mycoses 51(3):266–269

    Article  PubMed  CAS  Google Scholar 

  • Petrič S, Hakki T, Bernhardt R, Zigon D, Crešnar B (2010) Discovery of a steroid 11α-hydroxylase from Rhizopus oryzae and its biotechnological application. J Biotechnol 150:428–437

    Article  PubMed  CAS  Google Scholar 

  • Polaino S, Herrador MM, Cerdá-Olmedo E, Barrero AF (2010) Splitting of beta-carotene in the sexual interaction of Phycomyces. Org Biomol Chem 8(19):4229–4231

    Article  PubMed  CAS  Google Scholar 

  • Poliakov E, Gentleman S, Cunningham FX Jr, Miller-Ihli NJ, Redmond TM (2005) Key role of conserved histidines in recombinant mouse beta-carotene 15´15-monooxygenase-1 activity. J Biol Chem 280:29217–29223

    Article  PubMed  CAS  Google Scholar 

  • Pritchard GG (1971) An NAD + -independent L-lactate dehydrogenase from Rhizopus oryzae. Biochim Biophys Acta 250:25–34

    Article  PubMed  CAS  Google Scholar 

  • Pritchard GG (1973) Factors affecting the activity and synthesis of NAD dependent lactate dehydrogenase in Rhizopus oryzae. J Gen Microbiol 78:125–137

    Article  CAS  Google Scholar 

  • Quiles-Rosillo MD, Ruiz-Vázquez RM, Torres-Martínez S, Garre V (2003) Cloning, characterization and heterologous expression of the Blakeslea trispora gene encoding orotidine-5P-monophosphate decarboxylase. FEMS Microbiol Lett 222:229–236

    Article  PubMed  CAS  Google Scholar 

  • Ratledge C (2004) Fatty acid biosynthesis in microorganisms being used for Single Cell Oil production. Biochimie 86:807–815

    Article  PubMed  CAS  Google Scholar 

  • Ratledge C, Wynn JP (2002) The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51:1–51

    Article  PubMed  CAS  Google Scholar 

  • Revuelta JL, Eslava AP (1983) A new gene (carC) involved in the regulation of carotenogenesis in Phycomyces. Mol Gen Genet 192:225–229

    Article  CAS  Google Scholar 

  • Ribes JA, Vanover-Sams CL, Baker DJ (2000) Zygomycetes in human disease. Clin Microbiol Rev 13(2):236–301

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Roa Engel CA, Straathof AJ, Zijlmans TW, van Gulik WM, van der Wielen LA (2008) Fumaric acid production by fermentation. Appl Microbiol Biotechnol 78:379–389

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rodríguez-Ortiz R, Michielse C, Rep M, Limón MC, Avalos J (2012) Genetic basis of carotenoid overproduction in Fusarium oxysporum. Fungal Genet Biol 49:684–696

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Sáiz M, Paz B, de la Fuente JL, López-Nieto MJ, Cabri W, Barredo JL (2004) Blakeslea trispora genes for carotene biosynthesis. Appl Environ Microbiol 70:5589–5594

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rodríquez-Sáiz M, de la Fuente JL, Barredo JL (2012) Metabolic engineering of Mucor circinelloides for zeaxanthin production. Methods Mol Biol 898:133–151

    Article  CAS  Google Scholar 

  • Roncero MIG, Cerdá-Olmedo E (1982) Genetics of carotene biosynthesis in Phycomyces. Curr Genet 5:5–8

    Article  PubMed  CAS  Google Scholar 

  • Rothhardt J, Schwartze V, Voigt K (2011) Entomophthorales. In: Liu D (ed) Molecular detection of human fungal pathogens. Taylor & Francis CRC Press, pp 723–734

    Google Scholar 

  • Ruiz-Hidalgo MJ, Benito EP, Sandmann G, Eslava AP (1997) The phytoene dehydrogenase gene of Phycomyces: regulation of its expression by blue light and vitamin A. Mol Gen Genet 253:734–744

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Hidalgo MJ, Eslava AP, Alvarez MI, Benito EP (1999) Heterologous expression of the Phycomyces blakesleeanus phytoene dehydrogenase gene (carB) in Mucor circinelloides. Curr Microbiol 39:259–264

    Article  PubMed  CAS  Google Scholar 

  • Sahadevan Y, Richter-Fecken M, Kaerger K, Voigt K, Boland W (2013) Early and late trisporoids differentially regulate β-carotene production and gene transcript Levels in the mucoralean fungi Blakeslea trispora and Mucor mucedo. Appl Environ Microbiol 79(23):7466–7475

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Saito K, Saito A, Ohnishi M, Oda Y (2004) Genetic diversity in Rhizopus oryzae strains as revealed by the sequence of lactate dehydrogenase genes. Arch Microbiol 182:30–36

    Article  PubMed  CAS  Google Scholar 

  • Sajbidor J, Certik M, Dobronova S (1988) Influence of different carbon sources on growth, lipid content and fatty acid composition in four strains belonging to Mucorales. Biotechnol Lett 10:347–350

    Article  CAS  Google Scholar 

  • Salgado LM, Bejarano ER, Cerdá-Olmedo E (1989) Carotene superproducing mutants of Phycomyces blakesleeanus. Exp Mycol 13:332–336

    Article  CAS  Google Scholar 

  • Sanz C, Velayos A, Álvarez MI, Benito EP, Eslava AP (2011) Functional analysis of the Phycomyces carRA gene encoding the enzymes phytoene synthase and lycopene cyclase. PLos One 6:e23102

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sato Y, Narisawa K, Tsuruta K, Umezu M, Nishizawa T, Tanaka K, Yamaguchi K, Komatsuzaki M, Ohta H (2010) Detection of Betaproteobacteria inside the mycelium of the fungus Mortierella elongata. Microbes Environ 25(4):321–324

    Article  PubMed  Google Scholar 

  • Sautour M, Soares Mansur C, Divies C, Bensoussan M, Dantigny P (2002) Comparison of the effects of temperature and water activity on growth rate of food spoilage moulds. J Ind Microbiol Biotechnol 28:311–315

    Article  PubMed  CAS  Google Scholar 

  • Scarborough CL, Ferrari J, Godfray HC (2005) Aphid protected from pathogen by endosymbiont. Science 310(5755):1781

    Article  PubMed  CAS  Google Scholar 

  • Schachtschabel D, Schimek C, Wöstemeyer J, Boland W (2005) Biological activity of trisporoids and trisporoid analogues in Mucor mucedo (-). Phytochemistry 66(11):1358–1365

    Article  PubMed  CAS  Google Scholar 

  • Schachtschabel D, David A, Menzel KD, Schimek C, Wöstemeyer J, Boland W (2008) Cooperative biosynthesis of trisporoids by the (+) and (-) mating types of the zygomycete Blakeslea trispora. ChemBioChem 9(18):3004–3012

    Article  PubMed  CAS  Google Scholar 

  • Schimek C, Wöstemeyer J (2009) Carotene derivatives in sexual communication of zygomycete fungi. Phytochemistry 70:1867–1875

    Article  PubMed  CAS  Google Scholar 

  • Schimek C, Kleppe K, Saleem AR, Voigt K, Burmester A, Wöstemeyer J (2003) Sexual reactions in Mortierellales are mediated by the trisporic acid system. Mycol Res 107:736–747

    Article  PubMed  CAS  Google Scholar 

  • Schroeckh V, Scherlach K, Nützmann HW, Shelest E, Schmidt-Heck W, Schuemann J, Martin K, Hertweck C, Brakhage AA (2009) Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA 106(34):14558–14563

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872

    Article  PubMed  CAS  Google Scholar 

  • Schwartze VU, Winter S, Shelest E, Marcet-Houben M, Horn F, Wehner S, Linde J, Valiante V, Sammeth M, Riege K, Nowrousian M, Kaerger K, Jacobsen ID, Marz M, Brakhage AA, Gabaldón T, Böcker S, Voigt K (2014) Gene expansion shapes genome architecture in the human pathogen Lichtheimia corymbifera: an evolutionary genomics analysis in the ancient terrestrial Mucorales (Mucoromycotina). PLoS Genet 10(8):e1004496. doi:10.1371/journal.pgen.1004496

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Serrano I, Lopes da Silva T, Carlos Roseiro J (2001) Ethanol-induced dimorphism and lipid composition changes in Mucor fragilis CCMI 142. Lett Appl Microbiol 33:89–93

    Article  PubMed  CAS  Google Scholar 

  • Sharifia M, Karimi K, Taherzadeh MJ (2008) Production of ethanol by filamentous and yeast-like forms of Mucor indicus from fructose, glucose, sucrose, and molasses. J Ind Microbiol Biotechnol 35:1253–1259

    Article  PubMed  CAS  Google Scholar 

  • Shelest E (2008) Transcription factors in fungi. FEMS Microbiol Lett 286:145–151

    Article  PubMed  CAS  Google Scholar 

  • Shelest E, Voigt K (2014) Genomics to study basal lineage fungal biology: phylogenomics suggests a common origin. In: Nowrousian M (ed) The Mycota, vol XIII, 2nd edn, Fungal genomics. Springer, Berlin, pp 31–60

    Google Scholar 

  • Sigel R, Sigel A, Sigel H (2007) The ubiquitous roles of cytochrome P450 proteins: metal ions in life sciences. Wiley, New York. ISBN 0-470-01672-8

    Book  Google Scholar 

  • Silva F, Torres-Martinez S, Garre V (2006) Distinct white collar-1 genes control specific light responses in Mucor circinelloides. Mol Microbiol 61:1023–1037

    Article  PubMed  CAS  Google Scholar 

  • Silva F, Navarro E, Peñaranda A, Murcia-Flores L, Torres-Martínez S, Garre V (2008) A RING-finger protein regulates carotenogenesis via proteolysis-independent ubiquitylation of a white collar-1-like activator. Mol Microbiol 70:1026–1036

    PubMed  CAS  Google Scholar 

  • Simon L, Bousquet J, Lévesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and co-incidence with vascular land plants. Nature 363:67–69

    Article  Google Scholar 

  • Skory CD (2000) Isolation and expression of lactate dehydrogenase genes from Rhizopus oryzae. Appl Environ Microbiol 66:2343–2348

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Spano LA, Medeiros J, Mandels M (1976) Enzymatic hydrolysis of cellulose wastes to glucose. Resour Recover Conserv 1:279–294

    Article  CAS  Google Scholar 

  • Stredansky M, Conti E, Stredanska S, Zanetti F (2000) γ-Linolenic acid production with Thamnidium elegans by solid-state fermentation on apple pomace. Bioresour Technol 73:41–45

    Article  CAS  Google Scholar 

  • Sun J, Sun XX, Tang PW, Yuan QP (2012) Molecular cloning and functional expression of two key carotene synthetic genes derived from Blakeslea trispora into E. coli for increased β-carotene production. Biotechnol Lett 34:2077–2082

    Article  PubMed  CAS  Google Scholar 

  • Tagua VG, Medina HR, Martín-Domínguez R, Eslava AP, Corrochano LM, Cerdá-Olmedo E, Idnurm A (2012) A gene for carotene cleavage required for pheromone biosynthesis and carotene regulation in the fungus Phycomyces blakesleeanus. Fungal Genet Biol 49(5):398–404

    Article  PubMed  CAS  Google Scholar 

  • Takahashi Y, Moiseyev G, Chen Y, Ma JX (2005) Identification of conserved histidines and glutamic acid as key residues for isomerohydrolase activity of RPE65, an enzyme of the visual cycle in the retinal pigment epithelium. FEBS Lett 579:5414–5418

    Article  PubMed  CAS  Google Scholar 

  • Torres-Martínez S, Murillo FJ, Cerdá-Olmedo E (1980) Genetics of locopene cyclization and substrate transfer in beta-carotene biosynthesis in Phycomyces. Genet Res 36:299–946

    Article  PubMed  Google Scholar 

  • Tsuruo T, Oh-hara T, Iida H, Tsukagoshi S, Sato Z, Matsuda I, Iwasaki S, Okuda S, Shimizu F, Sasagawa K, Fukami M, Fukada K, Arakawa M (1986) Rhizoxin, a macrocyclic lactone antibiotic, as a new antitumor agent against human and murine tumor cells and their vincristine-resistant sublines. Cancer Res 46:381–385

    PubMed  CAS  Google Scholar 

  • van der Westhuizen JPJ, Kock JLF, Botha A, Botes PJ (1994) The distribution of the ω3- and ω 6-series of cellular long-chain fatty acids in fungi. Sys Appl Microbiol 17:327–345

    Article  Google Scholar 

  • van Heeswijck R, Roncero MIG (1984) High frequency transformation of Mucor with recombinant plasmid DNA. Carlsberg Res Commun 49:691–702

    Article  Google Scholar 

  • Velayos A, Blasco JL, Alvarez MI, Iturriaga EA, Eslava AP (2000a) Blue-light regulation of the phytoene dehydrogenase (carB) gene expression in Mucor circinelloides. Planta 210:938–946

    Article  PubMed  CAS  Google Scholar 

  • Velayos A, Eslava AP, Iturriaga EA (2000b) A bifunctional enzyme with lycopene cyclase and phytoene synthase activities is encoded by the carRP gene of Mucor circinelloides. Eur J Biochem 267:1–12

    Article  Google Scholar 

  • Velayos A, Papp T, Aguilar-Elena R, Fuentes-Vicente M, Eslava AP, Iturriaga EA, Álvarez MI (2003) Expression of the carG gene, encoding geranylgeranyl pyrophosphate synthase, is up-regulated by blue light in Mucor circinelloides. Curr Genet 43:112–120

    PubMed  CAS  Google Scholar 

  • Velayos A, Fuentes-Vicente M, Aguilar-Elena R, Eslava AP, Iturriaga EA (2004) A novel fungal prenyl diphosphate synthase in the dimorphic zygomycete Mucor circinelloides. Curr Genet 45:371–377

    Article  PubMed  CAS  Google Scholar 

  • Vially G, Marchal R, Guilbert N (2010) L(+) Lactate production from carbohydrates and lignocellulosic materials by Rhizopus oryzae UMIP 4.77. World J Microb Biot 26:607–614

    Article  CAS  Google Scholar 

  • Voigt K (2012) Zygomycota. In: Frey W (ed) Syllabus of plant families – A. Engler’s Syllabus der Pflanzenfamilien. Part 1/1: Blue-green algae, Myxomycetes and Myxomycete-like organisms, Phytoparasitic protists, Heterotrophic Heterokontobionta and Fungi p.p. Borntraeger Verlag, Stuttgart, pp 130–162

    Google Scholar 

  • Voigt K, de Hoog GS (2013) The zygomycetes in a phylogenetic perspective. Special issue Persoonia: molecular phylogeny and evolution of fungi, vol. 30. Naturalis Biodiversity Center Leiden and Centraalbureau voor Schimmelcultures Utrecht, The Netherlands, p 125

    Google Scholar 

  • Voigt K, Kirk PM (2014) 136. FUNGI | Classification of the zygomycetes: reappraisal as coherent class based on a comparison between traditional versus molecular systematics. In: Batt CA, Tortorello ML (eds) Encyclopedia of food microbiology, Vol 2. Elsevier, Academic, pp 54–67

    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-1α genes. Gene 270:113–120

    Article  PubMed  CAS  Google Scholar 

  • Voigt K, Hoffmann K, Einax E, Eckart M, Papp T, Vágvölgyi C, 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, New York, pp 313–332

    Google Scholar 

  • Voigt K, Marano AV, Gleason F (2013) Ecological and economical importance of parasitic and zoosporic true fungi. In: Kempken F (ed) The Mycota, vol XI, 2nd edn, Agricultural applications. Springer, Berlin, pp 243–270

    Google Scholar 

  • Wagner L, Stielow B, Hoffmann K, Petkovits T, Papp T, Vágvölgyi C, de Hoog GS, Verkley G, Voigt K (2013) A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA. Persoonia 30:77–93

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang GY, Keasling JD (2002) Amplification of HMG-CoA reductase production enhances carotenoid accumulation in Neurospora crassa. Metab Eng 4:193–201

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Chen W, Feng Y, Ren Y, Gu Z et al (2011) Genome characterization of the oleaginous fungus Mortierella alpina. PLoS One 6:e28319

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang D, Wu R, Xu Y, Li M (2013) Draft genome sequence of Rhizopus chinensis CCTCCM201021, used for brewing traditional Chinese alcoholic beverages. Genome Announc 1(2), e0019512

    PubMed  Google Scholar 

  • Werpy T, Petersen G (2004) Top value added chemicals from biomass, vol 1, Results of screening for potential candidates from sugars and synthesis gas. US Department of Energy, Washington, DC

    Google Scholar 

  • Wetzel J, Scheibner O, Burmester A, Schimek C, Wöstemeyer J (2009) 4-Dihydrotrisporin-dehydrogenase, an enzyme of the sex hormone pathway of Mucor mucedo: purification, cloning of the corresponding gene, and developmental expression. Eukaryotic Cell 8:88–95

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • White JD, Blakemore PR, Green NJ et al (2002) Total synthesis of rhizoxin D, a potent antimitotic agent from the fungus Rhizopus chinensis. J Org Chem 67:7750–7760

    Article  PubMed  CAS  Google Scholar 

  • Whittaker RH (1969) New concepts of kingdoms of organisms. Science 163:150–160

    Article  PubMed  CAS  Google Scholar 

  • Wikandari R, Millati R, Lennartsson PR, Harmayani E, Taherzadeh MJ (2012) Isolation and characterization of zygomycetes fungi from tempeh for ethanol production and biomass applications. Appl Biochem Biotechnol 167:1501–1512

    Article  PubMed  CAS  Google Scholar 

  • Willke T, Vorlop KD (2004) Industrial bioconversion of renewable resources as an alternative to conventional chemistry. Appl Microbiol Biotechnol 66:131–142

    Article  PubMed  CAS  Google Scholar 

  • Wolff AM, Arnau J (2002) Cloning of glyceraldehyde-3-phosphate dehydrogenase-encoding genes in Mucor circinelloides (Syn. racemosus) and use of the gpd1 promoter for recombinant protein production. Fungal Genet Biol 35:21–29

    Article  PubMed  CAS  Google Scholar 

  • Wöstemeyer J, Burmester A, Wöstemeyer A, Schultze K, Voigt K (2002) Gene transfer in the fungal host-parasite system Absidia glauca-Parasitella parasitica depends on infection. In: Syvanen M, Kado CI (eds) Horizontal gene transfer, 2nd edn. Academic, San Diego, CA, pp 241–247, Chapter 21

    Chapter  Google Scholar 

  • Wöstemeyer J, Grünler A, Schimek C, Voigt K (2005) Genetic regulation of carotenoid biosynthesis in fungi. In: Applied mycology and biotechnology Vol 5: Genes and genomics. Elsevier, pp 257–274

    Google Scholar 

  • Yen HW, Lee YC (2010) Production of lactic acid from raw sweet potato powders by rhizopus oryzae immobilized in sodium alginate capsules. Appl Biochem Biotechnol 162:607–615

    Article  PubMed  CAS  Google Scholar 

  • Zeng J, Zheng Y, Yu X, Yu L, Gao D, Chen S (2013) Lignocellulosic biomass as a carbohydrate source for lipid production by Mortierella isabellina. Bioresour Technol 128:385–391

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZY, Jin B, Kelly JM (2007) Production of lactic acid from renewable materials by Rhizopus fungi. Biochem Eng J 35:251–263

    Article  CAS  Google Scholar 

  • Zorn H, Langhoff S, Scheibner M, Berger RG (2003) Cleavage of β-carotene to flavor compounds by fungi. Appl Microbiol Biotechnol 62(4):331–336

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kerstin Voigt .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Voigt, K. et al. (2016). 15 Genetic and Metabolic Aspects of Primary and Secondary Metabolism of the Zygomycetes. In: Hoffmeister, D. (eds) Biochemistry and Molecular Biology. The Mycota, vol III. Springer, Cham. https://doi.org/10.1007/978-3-319-27790-5_15

Download citation

Publish with us

Policies and ethics