609
Views
27
CrossRef citations to date
0
Altmetric
Review Article

Critical applications of Mucor circinelloides within a biorefinery context

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 555-570 | Received 15 May 2018, Accepted 03 Feb 2019, Published online: 31 Mar 2019

References

  • Zhang Y, Adams IP, Ratledge C. Malic enzyme: the controlling activity for lipid production? Overexpression of malic enzyme in Mucor circinelloides leads to a 2.5-fold increase in lipid accumulation. Microbiology. 2007;153:2013–2025.
  • Morin-Sardin S, Nodet P, Coton E, et al. Mucor: a Janus-faced fungal genus with human health impact and industrial applications. Fungal Biol Rev. 2017;31:12–32.
  • Ratledge C. Single cell oils-have they a biotechnological future? Trends Biotechnol. 1993;11:278–284.
  • Wynn JP, Hamid AA, Li Y, et al. Biochemical events leading to the diversion of carbon into storage lipids in the oleaginous fungi Mucor circinelloides and Mortierella alpina. Microbiology. 2001;147:2857–2864.
  • Ratledge C, Cohen Z. Microbial and algal oils: do they have a future for biodiesel or as commodity oils? Lipid Technol. 2008;20:155–160.
  • Corrochano LM, Kuo A, Marcet-Houben M, et al. Expansion of signal transduction pathways in fungi by extensive genome duplication. Curr Biol. 2016;26:1577–1584.
  • van Heeswijck R, Roncero M. High frequency transformation of Mucor with recombinant plasmid DNA. Carlsberg Res Commun. 1984;49:691.
  • Gutiérrez A, López-García S, Garre V. High reliability transformation of the basal fungus Mucor circinelloides by electroporation. J Microbiol Meth. 2011;84:442–446.
  • Dower WJ, Miller JF, Ragsdale CW. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988;16:6127–6145.
  • Botham PA, Ratledge C. A biochemical explanation for lipid accumulation in Candida 107 and other oleaginous micro-organisms. Microbiology. 1979;114:361–375.
  • Magdum SS, Minde GP, Adhyapak US, et al. Competence evaluation of mycodiesel production by oleaginous fungal strains: Mucor circinelloides and Gliocladium roseum. Int J Energ Environ. 2015;6:377–382.
  • Huang C, Chen XF, Xiong L, et al. Single cell oil production from low-cost substrates: the possibility and potential of its industrialization. Biotechnol Adv. 2013;31:129–139.
  • Carvalho AKF, Rivaldi JD, Barbosa JC, et al. Biosynthesis, characterization and enzymatic transesterification of single cell oil of Mucor circinelloides–A sustainable pathway for biofuel production. Bioresource Technol. 2015;181:47–53.
  • Vicente G, Bautista LF, Gutiérrez FJ, et al. Direct transformation of fungal biomass from submerged cultures into biodiesel. Energy Fuels. 2010;24:3173–3178.
  • Antczak MS, Kubiak A, Antczak T, et al. Enzymatic biodiesel synthesis–key factors affecting efficiency of the process. Renew Energ. 2009;34:1185–1194.
  • Xia C, Zhang J, Zhang W, et al. A new cultivation method for microbial oil production: cell pelletization and lipid accumulation by Mucor circinelloides. Biotechnol Biofuels. 2011;4:15.
  • Carvalho AKF, Bento HBS, Izário Filho HJ, et al. Approaches to convert Mucor circinelloides lipid into biodiesel by enzymatic synthesis assisted by microwave irradiations. Renew Energ. 2018;125:747–754.
  • Carvalho AKF, Bento HBS, Reis CER, et al. Sustainable enzymatic approaches in a fungal lipid biorefinery based in sugarcane bagasse hydrolysate as carbon source. Bioresource Technol. 2019;276:269–275.
  • Szczęsna-Antczak M, Antczak T, Piotrowicz-Wasiak M, et al. Relationships between lipases and lipids in mycelia of two Mucor strains. Enzyme Microb Tech. 2006;39:1214–1222.
  • Carvalho AKF, Bento HBS, Rivaldi JD, et al. Direct transesterification of Mucor circinelloides biomass for biodiesel production: effect of carbon sources on the accumulation of fungal lipids and biofuel properties. Fuel. 2018;234:789–796.
  • Bento HBS, Carvalho AKF, Reis CER, et al. Microbial biodiesel production: from sucrose-based carbon sources to alkyl esters via enzymatic transesterification. Process Saf Environ Prot. 2019;121:349–356.
  • Papagianni M. Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv. 2004;22:189–259.
  • Reis CER, Zhang J, Hu B. Lipid accumulation by pelletized culture of Mucor circinelloides on corn stover hydrolysate. Appl Biochem Biotechnol. 2014;174:411–423.
  • Vicente G, Fernando Bautista L, Rodriguez R, et al. Biodiesel production from biomass of an oleaginous fungus. Biochem Engin J. 2009;48:22–27.
  • Carvalho AKF, da Conceição LRV, Silva JPV, et al. Biodiesel production from Mucor circinelloides using ethanol and heteropolyacid in one and two-step transesterification. Fuel. 2017;202:503–511.
  • Arima K, Yu J, Iwasaki S, et al. Milk-clotting enzyme from microorganisms: v. purification and crystallization of Mucor Rennin from Mucor pusillus var. Lindt. Appl Microbiol. 1968;16:1727–1733.
  • Wang HL. Release of proteinase from mycelium of Mucor hiemalis. J Bacteriol. 1967;93:1800–1810.
  • Salgado JAG, Kangwa M, Fernandez-Lahore M. Cloning and expression of an active aspartic proteinase from Mucor circinelloides in Pichia pastoris. BMC Microbiol. 2013;13:250.
  • Thakur A, Pahwa R, Singh S, et al. Production, purification, and characterization of polygalacturonase from Mucor circinelloides ITCC 6025. Enzyme Res. 2010;2010:1.
  • Alves MH, Campos-Takaki GM, Porto ALF, et al. Screening of Mucor spp. for the production of amylase, lipase, polygalacturonase and protease. Braz J Microbiol. 2002;33:325–330.
  • Kamat S, Khot M, Zinjarde S, et al. Coupled production of single cell oil as biodiesel feedstock, xylitol and xylanase from sugarcane bagasse in a biorefinery concept using fungi from the tropical mangrove wetlands. Bioresource Technol. 2013;135:246–253.
  • Saha BC. Production, purification and properties of endoglucanase from a newly isolated strain of Mucor circinelloides. Process Biochem. 2004;39:1871–1876.
  • Szczęsna-Antczak M, Struszczyk-Świta K, Rzyska M, et al. Oil accumulation and in situ trans/esterification by lipolytic fungal biomass. Bioresource Technol. 2018;265:110–118.
  • Andrade GSS, Carvalho AKF, Romero CM, et al. Mucor circinelloides whole-cells as a biocatalyst for the production of ethyl esters based on babassu oil. Bioprocess Biosyst Eng. 2014;37:2539–2548.
  • Cortez DV, De Castro HF, Andrade GSS. Potential catalytic of mycelium-bound lipase of filamentous fungi in biotransformation processes. Quim Nova. 2017;40:85–96.
  • Andrade GSS, Freitas L, Oliveira PC, et al. Screening, immobilization and utilization of whole cell biocatalysts to mediate the ethanolysis of babassu oil. J Mol Catal B-Enzym. 2012;84:183–188.
  • Adlercreutz P. Immobilisation and application of lipases in organic media. Chem Soc Rev. 2013;42:6406–6436.
  • Carvalho AKF, Faria ELP, Rivaldi JD, et al. Performance of whole-cells lipase derived from Mucor circinelloides as a catalyst in the ethanolysis of non-edible vegetable oils under batch and continuous run conditions. Ind Crops Prod. 2015;67:287–294.
  • Tang X, Chen H, Chen YQ, et al. Comparison of biochemical activities between high and low lipid-producing strains of Mucor circinelloides: an explanation for the high oleaginicity of strain WJ11. PLoS One. 2015;10:e0128396.
  • Zan X, Tang X, Chu L, et al. Dual functions of Lip6 and its regulation of lipid metabolism in the oleaginous fungus Mucor circinelloides. J Agric Food Chem. 2018;66:2796–2804.
  • Zan X, Tang X, Chu L, et al. Lipase genes in Mucor circinelloides: identification, sub-cellular location, phylogenetic analysis and expression profiling during growth and lipid accumulation. J Ind Microbiol Biotechnol. 2016;43:1467–1480.
  • Ye Y, Gan J, Hu B. Screening of phosphorus-accumulating fungi and their potential for phosphorus removal from waste streams. Appl Biochem Biotechnol. 2015;177:1127–1136.
  • Zhang X, Yang H, Cui Z. Mucor circinelloides: efficiency of bioremediation response to heavy metal pollution. Toxicol Res. 2017;6:442–447.
  • Cui Z, Zhang X, Yang H, et al. Bioremediation of heavy metal pollution utilizing composite microbial agent of Mucor circinelloides, Actinomucor sp. and Mortierella sp. J Environ Chem Eng. 2017;5:3616–3621.
  • He Q, Rajendran A, Gan J, et al. Phosphorus recovery from dairy manure wastewater by fungal biomass treatment. Water Environ J. [cited 2018 Oct 1]. DOI:10.1111/wej.12421
  • Rajendran A, Hu B. Mycoalgae biofilm: development of a novel platform technology using algae and fungal cultures. Biotechnol Biofuels. 2016;9:112.
  • Rajendran A, Fox T, Reis CR, et al. Deposition of manure nutrients in a novel mycoalgae biofilm for nutrient management. Biocatal Agric Biotechnol. 2018;14:120–128.
  • Rajendran A, Fox T, Hu B. Nutrient recovery from ethanol co‐products by a novel mycoalgae biofilm: attached cultures of symbiotic fungi and algae. J Chem Technol Biotechnol. 2017;92:1766–1776.
  • Sankaran S, Khanal SK, Jasti N, et al. Use of filamentous fungi for wastewater treatment and production of high value fungal byproducts: a review. Crit Rev Env Sci Technol. 2010;40:400–449.
  • Mitra D, Rasmussen ML, Chand P, et al. Value-added oil and animal feed production from corn-ethanol stillage using the oleaginous fungus Mucor circinelloides. Bioresource Technol. 2012;107:368–375.
  • Reis C, Bento H, Alves T, et al. Vinasse treatment within the sugarcane-ethanol industry using ozone combined with anaerobic and aerobic microbial processes. Environments. 2019;6:5.
  • Rodrı́guez A, Cuesta A, Esteban MA, et al. The effect of dietary administration of the fungus Mucor circinelloides on non-specific immune responses of gilthead seabream. Fish Shellfish Immun. 2004;16:241–249.
  • Sajid M, Prabjeet S, Samoon MH, et al. Effect of dietary chitosan on non-specific immune response and growth of Cyprinus carpio challenged with Aeromonas hydrophila. Int Aquat Res. 2010;2:77–85.
  • Singh R, Paul D, Jain RK. Biofilms: implications in bioremediation. Trends Microbiol. 2006;14:389–397.
  • Priya VS, Philip L. Treatment of volatile organic compounds in pharmaceutical wastewater using submerged aerated biological filter. Chem Eng J. 2015;266:309–319.
  • Barnharst T, Rajendran A, Hu B. Bioremediation of synthetic intensive aquaculture wastewater by a novel feed-grade composite biofilm. Int Biodeterior Biodegrad. 2018;126:131–142.
  • Lee SC, Li A, Calo S, et al. Calcineurin plays key roles in the dimorphic transition and virulence of the human pathogenic zygomycete Mucor circinelloides. PLoS Pathogens. 2013;9:e1003625.
  • Lee SC, Li A, Calo S, et al. Calcineurin orchestrates dimorphic transitions, antifungal drug responses and host–pathogen interactions of the pathogenic mucoralean fungus Mucor circinelloides. Mol Microbiol. 2015;97:844–865.
  • Wolff AM, Appel KF, Petersen JB, et al. Identification and analysis of genes involved in the control of dimorphism in Mucor circinelloides (syn. racemosus). FEMS Yeast Res. 2002;2:203–213.
  • Ruiz-Vázquez RM, Nicolás FE, Torres-Martínez S, et al. Distinct RNAi pathways in the regulation of physiology and development in the fungus Mucor circinelloides. Adv Genet. 2015;91:55–102.
  • Buchon N, Vaury C. RNAi: a defensive RNA-silencing against viruses and transposable elements. Heredity. 2006;96:195.
  • Nicolás FE, Ruiz-Vázquez RM. Functional diversity of RNAi-associated sRNAs in fungi. Int J Mol Sci. 2013;14:15348–15360.
  • Bartnicki-Garcia S, Nickerson WJ. Induction of yeast-like development in Mucor by carbon dioxide. J Bacteriol. 1962;84:829–840.
  • Bartnicki-García S. III,. Mold-yeast dimorphism of Mucor. Bacteriol Rev. 1963;27:293.
  • McIntyre M, Breum J, Arnau J, et al. Growth physiology and dimorphism of Mucor circinelloides (syn. racemosus) during submerged batch cultivation. Appl Biochem Biotech. 2002;58:495–502.
  • Orlowski M. Mucor dimorphism. Microbiol Rev. 1991;55:234–258.
  • Lübbehüsen TL, Nielsen J, McIntyre M. Aerobic and anaerobic ethanol production by Mucor circinelloides during submerged growth. Appl Microbiol Biot. 2004;63:543–548.
  • van Dijken JP, Weusthuis RA, Pronk JT. Kinetics of growth and sugar consumption in yeasts. Antonie Van Leeuwenhoek. 1993;63:343–352.
  • Van Urk H, Voll WSL, Scheffers WA, et al. Transient-state analysis of metabolic fluxes in Crabtree-positive and Crabtree-negative yeasts. Appl Environ Microbiol. 1990;56:281–287.
  • Nagy G, Farkas A, Csernetics Á, et al. Transcription of the three HMG-CoA reductase genes of Mucor circinelloides. BMC Microbiol. 2014;14:93.
  • Enrique A, Papp T, Breum J, et al. Strain and culture conditions improvement for β-carotene production with Mucor. Microbial processes and products. 2005;18:239–256.
  • Zhang Y, Navarro E, Cánovas-Márquez JT, et al. A new regulatory mechanism controlling carotenogenesis in the fungus Mucor circinelloides as a target to generate β-carotene over-producing strains by genetic engineering. Microb Cell Fact. 2016;15:99.
  • Gultom SO, Hu B. Review of microalgae harvesting via co-pelletization with filamentous fungus. Energies. 2013;6:5921–5939.
  • Gultom SO, Zamalloa C, Hu B. Microalgae harvest through fungal pelletization—co-culture of Chlorella vulgaris and Aspergillus niger. Energies. 2014;7:4417–4429.
  • Zhang J, Hu B. A novel method to harvest microalgae via co-culture of filamentous fungi to form cell pellets. Bioresour Technol. 2012;114:529–535.
  • Čertík M, Adamechová Z, Guothová L. Simultaneous enrichment of cereals with polyunsaturated fatty acids and pigments by fungal solid state fermentations. J Biotechnol. 2013;168:130–134.
  • Rodríguez-Frómeta RA, Gutiérrez A, Torres-Martínez S, et al. Malic enzyme activity is not the only bottleneck for lipid accumulation in the oleaginous fungus Mucor circinelloides. Appl Microbiol Biotechnol. 2013;97:3063–3072.
  • Mysyakina IS, Funtikova NS. Metabolic characteristics and lipid composition of yeastlike cells and mycelium of Mucor circinelloides var. lusitanicus INMI grown at a high glucose content in the medium. Mikrobiologiia. 2008;77:407–411.
  • Song Y, Wynn JP, Li Y, et al. A pre-genetic study of the isoforms of malic enzyme associated with lipid accumulation in Mucor circinelloides. Microbiology. 2001;147:1507–1515.
  • Jackson FM, Fraser T, Smith MA, et al. Biosynthesis of C18 polyunsaturated fatty acids in microsomal membrane preparations from the filamentous fungus Mucor circinelloides. Eur J Biochem. 1998;252:513–519.
  • Jackson FM, Michaelson L, Fraser TCM, et al. Biosynthesis of triacylglycerol in the filamentous fungus Mucor circinelloides. Microbiology. 1998;144:2639–2645.
  • Botha A, Kock JLF, Coetzee DJ, et al. Physiological properties and fatty acid composition in Mucor circinelloides f. circinelloides. Antonie Van Leeuwenhoek. 1997;71:201–206.
  • Čertík M, Balteszov L, Šajbidor J. Lipid formation and γ‐linolenic acid production by Mucorales fungi grown on sunflower oil. Lett Appl Microbiol. 1997;25:101–105.
  • Du Preez JC, Immelman M, Kilian SG. The utilization of short-chain monocarboxylic acids as carbon sources for the production of gamma-linolenic acid by Mucor strains in fed-batch culture. World J Microbiol Biotechnol. 1996;12:68–72.
  • Aggelis G, Komaitis M, Papanikolaou S, et al. A mathematical model for the study of lipid accumulation in oleaginous microorganisms. I. Lipid accumulation during growth of Mucor circinelloides CBS 172-27 on a vegetable oil. Grasas y Aceites. 1995;46:169.
  • Roux MP, Kock JLF, Botha A, et al. Mucor-a source of cocoa butter and gamma-linolenic acid. World J Microbiol Biotechnol. 1994;10:417–422.
  • Kendrick A, Ratledge C. Desaturation of polyunsaturated fatty acids in Mucor circinelloides and the involvement of a novel membrane bound malic enzyme. Eur J Biochem. 1992;209:667–673.
  • Zhao L, Cánovas-Márquez JT, Tang X, et al. Role of malate transporter in lipid accumulation of oleaginous fungus Mucor circinelloides. Appl Microbiol Biotechnol. 2016;100:1297–1305.
  • Zhang L, Zhang H, Song Y. Identification and characterization of diacylglycerol acyltransferase from oleaginous fungus Mucor circinelloides. J Agric Food Chem. 2018;66:674–681.
  • Romagnolo A, Spina F, Poli A, et al. Old yellow enzyme homologues in Mucor circinelloides: expression profile and biotransformation. Sci Rep. 2017;7:12093.
  • Dotsenko AS, Dotsenko GS, Senko OV, et al. Complex effect of lignocellulosic biomass pretreatment with 1-butyl-3-methylimidazolium chloride ionic liquid on various aspects of ethanol and fumaric acid production by immobilized cells within SSF. Bioresour Technol. 2018;250:429–438.
  • Takano M, Hoshino K. Direct ethanol production from rice straw by coculture with two high-performing fungi. Front Chem Sci Eng. 2012;6:139–145.
  • Huang Y, Busk PK, Grell MN, et al. Identification of a β-glucosidase from the Mucor circinelloides genome by peptide pattern recognition. Enzyme Microb Technol. 2014;67:47–52.
  • Shimonaka A, Koga J, Baba Y, et al. Specific characteristics of family 45 endoglucanases from Mucorales in the use of textiles and laundry. Biosci Biotechnol Biochem. 2006;70:1013–1016.
  • Zan X, Tang X, Zhao L, et al. Bioinformatical analysis and preliminary study of the role of lipase in lipid metabolism in Mucor circinelloides. RSC Adv. 2016;6:60673–60682.
  • Catucci G, Romagnolo A, Spina F, et al. Enzyme-substrate matching in biocatalysis: in silico studies to predict substrate preference of ten putative ene-reductases from Mucor circinelloides MUT44. J Mol Catal B Enzym. 2016;131:94–100.
  • Szczęsna-Antczak M, Szeląg J, Stańczyk Ł, et al. Engineering of lipase-catalyzed transesterification reaction media using water and diethylamine. Biocatal Biotransformation. 2016;34:253–264.
  • Regado MA, Cristóvão BM, Moutinho CG, et al. Flavour development via lipolysis of milk fats: changes in free fatty acid pool. Int J Food Sci Technol. 2007;42:961–968.
  • Andrade VS, Sarubbo LA, Fukushima K, et al. Production of extracellular proteases by Mucor circinelloides using D-glucose as carbon source/substrate. Braz J Microbiol. 2002;33:106–110.
  • Sathya R, Pradeep BV, Angayarkanni J, et al. Production of milk clotting protease by a local isolate of Mucor circinelloides under SSF using agro-industrial wastes. Biotechnol Bioproc E. 2009;14:788–794.
  • Thanh VN, Mai LT, Tuan DA. Microbial diversity of traditional Vietnamese alcohol fermentation starters (banh men) as determined by PCR-mediated DGGE. Int J Food Microbiol. 2008;128:268–273.
  • Barbosa-Silveira AA, Okada K, de Campos-Takaki GM. Cultural conditions and antioxidant activity of astaxanthin produced by Mucor circinelloides f. circinelloides. Int J Agr Pol Res. 2015;3:60–66.
  • Hameed A, Hussain SA, Yang J, et al. Antioxidants potential of the filamentous fungi (Mucor circinelloides). Nutrients. 2017;9:1101.
  • Zhang Y, Chen H, Navarro E, et al. Generation of lycopene-overproducing strains of the fungus Mucor circinelloides reveals important aspects of lycopene formation and accumulation. Biotechnol Lett. 2017;39:439–446.
  • Csernetics Á, Tóth E, Farkas A, et al. Expression of Xanthophyllomyces dendrorhous cytochrome-P450 hydroxylase and reductase in Mucor circinelloides. World J Microbiol Biotechnol. 2015;31:321–336.
  • Nicolás-Molina FE, Navarro E, Ruiz-Vázquez RM. Lycopene over-accumulation by disruption of the negative regulator gene crgA in Mucor circinelloides. Appl Microbiol Biotechnol. 2008;78:131–137.
  • Shan L, Jiao K, Yin M, et al. Biotransformation of 5-en-3β-ol steroids by Mucor circinelloides lusitanicus. Biocatal Biotransformation. 2016;34:83–88.
  • Hollmann M, Razzazi-Fazeli E, Grajewski J, et al. Detection of 3-nitropropionic acid and cytotoxicity in Mucor circinelloides. Mycotoxin Res. 2008;24:140–150.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.