Skip to main content
Log in

Mucoromycota fungi as powerful cell factories for modern biorefinery

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Biorefinery employing fungi can be a strategy for valorizing low-cost rest materials, by-products and wastes into several valuable bioproducts through the fungal fermentation. Mucoromycota fungi are soil fungi with a highly versatile metabolic system that positions them as powerful microbial cell factories for biorefinery applications. Lipids, pigments, chitin/chitosan, polyphosphates, ethanol, organic acids and enzymes are main Mucoromycota products that can be refined from the fermentation process and applied in nutrition, chemical or biofuel industries. In addition, Mucoromycota biomass can be used as it is for specific purposes, such as feed. Mucoromycota fungi can be employed in developing co-production processes, whereby several intra- and extracellular products are simultaneously formed in a single fermentation process, and, thus, economic viability of the process can be improved. This mini review provides a comprehensive overview over the recent advances in the production of valuable metabolites by Mucoromycota fungi and fermentation strategies which could be potentially applied in the industrial biorefinery settings.

Key points

• Biorefineries utilizing Mucoromycota fungi as production cell factories can provide a wide range of bioproducts.

• Mucoromycota fungi are able to perform co-production of various metabolites in a single fermentation process.

• Versatile metabolism of Mucoromycota allows valorization of a various low-cost substrates such as wastes and rest materials.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. https://cheeseconnection.net/product/marzyme-supreme-rennet/

  2. https://biosolutions.novozymes.com.

  3. https://www.takabio.com/en/catalogue-enzymes.

  4. https://www.novozymes.com/en.

  5. https://www.takabio.com/en/catalogue-enzymes/

  6. https://www.takabio.com/en/gamme-sumizyme/

  7. Artistry™ Intensive Skincare Renewing Peel | Skin Care | Amway.

  8. https://www.antoinettealexander.com/products/enzyme-exfoliator.

  9. DSM Animal Nutrition & Health | DSM.

  10. https://patents.google.com/patent/US20110237813h3.

  11. https://www.sigmaaldrich.com/CZ/en/product/sigma/sml0982?context = product.

  12. https://www.dsm.com/corporate/news/news-archive/2011/46–11-dsm-completes-acquisition-of-vitatene-s-a-u.html.

  13. https://www.lycored.com/beta-carotene/

References

  • Abasian L, Shafiei Alavijeh R, Satari B, Karimi K (2020) Sustainable and effective chitosan production by dimorphic fungus Mucor rouxii via replacing yeast extract with fungal extract. Appl Biochem Biotechnol 191(2):666–678. https://doi.org/10.1007/s12010-019-03220-w

    Article  PubMed  CAS  Google Scholar 

  • Abo Elsoud MM, El Kady EM (2019) Current trends in fungal biosynthesis of chitin and chitosan. Bullet Nat Res Centre 43(1):59. https://doi.org/10.1186/s42269-019-0105-y

    Article  Google Scholar 

  • Aghbashlo M, Tabatabaei M, Karimi K, Mohammadi M (2017) Effect of phosphate concentration on exergetic-based sustainability parameters of glucose fermentation by Ethanolic Mucor indicus. Sustainab Prod Consumpt 9:28–36

    Article  Google Scholar 

  • Alves MH, Campos-Takaki GM, Porto ALF, Milanez AI (2002) Screening of Mucor spp. for the production of amylase, lipase, polygalacturonase and protease. Braz J Microbiol 33:325–330

    Article  CAS  Google Scholar 

  • Asachi R, Karimi K (2013) Enhanced ethanol and chitosan production from wheat straw by Mucor indicus with minimal nutrient consumption. Process Biochem 48(10):1524–1531. https://doi.org/10.1016/j.procbio.2013.07.013

    Article  CAS  Google Scholar 

  • Baba Y, Shimonaka A, Koga J, Kubota H, Kono T (2005) Alternative splicing produces two endoglucanases with one or two carbohydrate-binding modules in Mucor circinelloides. J Bacteriol 187(9):3045–3051

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barnharst T, Rajendran A, Hu B (2018) Bioremediation of synthetic intensive aquaculture wastewater by a novel feed-grade composite biofilm. Int Biodeterior Biodegradation 126:131–142. https://doi.org/10.1016/j.ibiod.2017.10.007

    Article  CAS  Google Scholar 

  • Barnharst T, Sun X, Rajendran A, Urriola P, Shurson G, Hu B (2021) Enhanced protein and amino acids of corn–ethanol co-product by Mucor indicus and Rhizopus oryzae. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449-021-02580-0

    Article  PubMed  Google Scholar 

  • Bartnicki-Garcia S, Nickerson WJ (1962) Isolation, composition, and structure of cell walls of filamentous and yeast-like forms of Mucor rouxii. Biochem Biophys Acta 58(1):102–119. https://doi.org/10.1016/0006-3002(62)90822-3

    Article  PubMed  CAS  Google Scholar 

  • Beever RE, Burns D (1981) Phosphorus uptake, storage and utilization by fungi Advances in botanical research. vol 8. Elsevier, pp 127–219

  • Beheshti H, Karimi K (2016) Ethanol and value-added byproducts from rice straw by dimorphic fungus Mucor hiemalis. Eng Life Sci 16(8):750–761. https://doi.org/10.1002/elsc.201600023

    Article  CAS  Google Scholar 

  • Bellou S, Makri A, Sarris D, Michos K, Rentoumi P, Celik A, Papanikolaou S, Aggelis G (2014) The olive mill wastewater as substrate for single cell oil production by Zygomycetes. J Biotechnol 170:50–59

    Article  PubMed  CAS  Google Scholar 

  • Benabda O, M’hir S, Kasmi M, Mnif W, Hamdi M (2019) Optimization of protease and amylase production by Rhizopus oryzae cultivated on bread waste using solid-state fermentation. J Chem 2019

  • Berbee ML, Taylor JW (2001) Fungal molecular evolution: gene trees and geologic time Systematics and evolution. Springer, pp 229–245

  • Bokade P, Purohit HJ, Bajaj A (2021) Myco-remediation of chlorinated pesticides: insights into fungal metabolic system. Indian J Microbiol 61(3):237–249. https://doi.org/10.1007/s12088-021-00940-8

    Article  PubMed  CAS  Google Scholar 

  • Brennan PJ, Griffin PFS, Lösel DM, Tyrrell D (1975) The lipids of fungi. Prog Chem Fats Other Lipids 14:49–89. https://doi.org/10.1016/0079-6832(75)90002-6

    Article  Google Scholar 

  • Carvalho AKF, Bento HB, Reis CE, De Castro HF (2019) Sustainable enzymatic approaches in a fungal lipid biorefinery based in sugarcane bagasse hydrolysate as carbon source. Biores Technol 276:269–275

    Article  CAS  Google Scholar 

  • Carvalho AKF, Bento HB, Rivaldi JD, de Castro HF (2018) Direct transesterification of Mucor circinelloides biomass for biodiesel production: effect of carbon sources on the accumulation of fungal lipids and biofuel properties. Fuel 234:789–796

    Article  CAS  Google Scholar 

  • Čertík M, Balteszov L, Šajbidor J (1997) Lipid formation and γ-linolenic acid production by Mucorales fungi grown on sunflower oil. Lett Appl Microbiol 25(2):101–105

    Article  Google Scholar 

  • Chan LG, Cohen JL, Ozturk G, Hennebelle M, Taha AY, LN de Moura Bell JM (2018) Bioconversion of cheese whey permeate into fungal oil by Mucor circinelloides. J Biol Eng 12(1):1-14

  • Chang L, Tang X, Lu H, Zhang H, Chen YQ, Chen H, Chen W (2019) Role of adenosine monophosphate deaminase during fatty acid accumulation in oleaginous fungus Mortierella alpina. J Agric Food Chem 67(34):9551–9559. https://doi.org/10.1021/acs.jafc.9b03603

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S, Chatterjee S, Chatterjee BP, Guha AK (2009) Influence of plant growth hormones on the growth of Mucor rouxii and chitosan production. Microbiol Res 164(3):347–351. https://doi.org/10.1016/j.micres.2007.05.003

    Article  PubMed  CAS  Google Scholar 

  • Chauve M, Mathis H, Huc D, Casanave D, Monot F, Lopes Ferreira N (2010) Comparative kinetic analysis of two fungal β-glucosidases. Biotechnol Biofuels 3(1):3. https://doi.org/10.1186/1754-6834-3-3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choi Y-N, Cho HU, Utomo JC, Shin DY, Kim HK, Park JM (2016) Efficient harvesting of Synechocystis sp. PCC 6803 with filamentous fungal pellets. J Appl Phycol 28(4):2225–2231. https://doi.org/10.1007/s10811-015-0787-y

    Article  CAS  Google Scholar 

  • Choudhari SM, Ananthanarayan L, Singhal RS (2008) Use of metabolic stimulators and inhibitors for enhanced production of β-carotene and lycopene by Blakeslea trispora NRRL 2895 and 2896. Biores Technol 99(8):3166–3173

    Article  CAS  Google Scholar 

  • Chowdhary K, Prasad U, Sharma S (2018) Role of fungi in biorefinery: a perspective Fungal Biorefineries. Springer, pp 1–20

  • Corrochano LM, Garre V (2010) Photobiology in the Zygomycota: multiple photoreceptor genes for complex responses to light. Fungal Genet Biol 47(11):893–899. https://doi.org/10.1016/j.fgb.2010.04.007

    Article  PubMed  CAS  Google Scholar 

  • Csernetics Á, Nagy G, Iturriaga EA, Szekeres A, Eslava AP, Vágvölgyi C, 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(7):696–703

    Article  PubMed  CAS  Google Scholar 

  • Davis LL, Bartnicki-Garcia S (1984) Chitosan synthesis by the tandem action of chitin synthetase and chitin deacetylase from Mucor rouxii. Biochemistry 23(6):1065–1073. https://doi.org/10.1021/bi00301a005

    Article  CAS  Google Scholar 

  • Demir M, Gündes AG (2020) Single‐cell oil production by Mortierella isabellina DSM 1414 using different sugars as carbon source. Biotechnol Prog 36(6):e3050

  • Deng F, Aita GM (2018) Fumaric acid production by Rhizopus oryzae ATCC® 20344™ from lignocellulosic syrup. BioEnergy Res 11(2):330–340

    Article  CAS  Google Scholar 

  • Dexter Y, Cooke R (1984) Fatty acids, sterols and carotenoids of the psychrophile Mucor strictus and some mesophilic Mucor species. Trans Br Mycol Soc 83(3):455–461

    Article  CAS  Google Scholar 

  • Dulf FV, Vodnar DC, Toşa MI, Dulf E-H (2020) Simultaneous enrichment of grape pomace with γ-linolenic acid and carotenoids by solid-state fermentation with Zygomycetes fungi and antioxidant potential of the bioprocessed substrates. Food Chem 310:125927

  • Dzurendová S, Shapaval V, Tafintseva V, Kohler A, Byrtusová D, Szotkowski M, Márová I, Zimmermann B (2021) Assessment of biotechnologically important filamentous fungal biomass by Fourier transform Raman spectroscopy. Int J Mol Sci 22(13):6710

    Article  PubMed  PubMed Central  Google Scholar 

  • Dzurendova S, Zimmermann B, Kohler A, Reitzel K, Nielsen UG, Leivers S, Horn SJ, Shapaval V (2021) Calcium affects polyphosphate and lipid accumulation in Mucoromycota fungi. J Fungi 7(4):300

    Article  CAS  Google Scholar 

  • Dzurendova S, Zimmermann B, Kohler A, Tafintseva V, Slany O, Certik M, Shapaval V (2020a) Microcultivation and FTIR spectroscopy-based screening revealed a nutrient-induced co-production of high-value metabolites in oleaginous Mucoromycota fungi. PloS one 15(6):e0234870

  • Dzurendova S, Zimmermann B, Tafintseva V, Kohler A, Ekeberg D, Shapaval V (2020) The influence of phosphorus source and the nature of nitrogen substrate on the biomass production and lipid accumulation in oleaginous Mucoromycota fungi. Appl Microbiol Biotechnol 104(18):8065–8076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dzurendova S, Zimmermann B, Tafintseva V, Kohler A, Horn SJ, Shapaval V (2020) Metal and phosphate ions show remarkable influence on the biomass production and lipid accumulation in oleaginous Mucor circinelloides. J Fungi 6(4):260

    Article  CAS  Google Scholar 

  • Economou CN, Aggelis G, Pavlou S, Vayenas DV (2011) Single cell oil production from rice hulls hydrolysate. Biores Technol 102(20):9737–9742

    Article  CAS  Google Scholar 

  • Economou CN, Makri A, Aggelis G, Pavlou S, Vayenas D (2010) Semi-solid state fermentation of sweet sorghum for the biotechnological production of single cell oil. Biores Technol 101(4):1385–1388

    Article  CAS  Google Scholar 

  • Fakas S, Makri A, Mavromati M, Tselepi M, Aggelis G (2009) Fatty acid composition in lipid fractions lengthwise the mycelium of Mortierella isabellina and lipid production by solid state fermentation. Biores Technol 100(23):6118–6120

    Article  CAS  Google Scholar 

  • Feng Y, Chen Z, Liu N, Zhao H, Cui C, Zhao M (2014) Changes in fatty acid composition and lipid profile during koji fermentation and their relationships with soy sauce flavour. Food Chem 158:438–444

    Article  PubMed  CAS  Google Scholar 

  • Ferreira JA, Lennartsson PR, Edebo L, Taherzadeh MJ (2013) Zygomycetes-based biorefinery: present status and future prospects. Biores Technol 135:523–532. https://doi.org/10.1016/j.biortech.2012.09.064

    Article  CAS  Google Scholar 

  • Fraser PD, Ruiz-Hidalgo MJ, Lopez-Matas MA, Alvarez MI, Eslava AP, Bramley PM (1996) Carotenoid biosynthesis in wild type and mutant strains of Mucor circinelloides. Biochimica et Biophysica Acta (BBA)-General Subjects 1289(2):203–208

  • Fu YQ, Li S, Chen Y, Xu Q, Huang H, Sheng XY (2010) Enhancement of fumaric acid production by Rhizopus oryzae using a two-stage dissolved oxygen control strategy. Appl Biochem Biotechnol 162(4):1031–1038. https://doi.org/10.1007/s12010-009-8831-5

    Article  PubMed  CAS  Google Scholar 

  • Ghormade V, Pathan E, Deshpande M (2017) Can fungi compete with marine sources for chitosan production? Int J Biol Macromol 104:1415–1421

    Article  PubMed  CAS  Google Scholar 

  • Gulati HK, Chadha BS, Saini HS (2007) Production of feed enzymes (phytase and plant cell wall hydrolyzing enzymes) by Mucor indicus MTCC 6333: purification and characterization of phytase. Folia Microbiol 52(5):491. https://doi.org/10.1007/BF02932109

    Article  CAS  Google Scholar 

  • Gultom S, Hu B (2013) Review of microalgae harvesting via co-pelletization with filamentous fungus. Energies 6(11):5921–5939. https://doi.org/10.3390/en6115921

    Article  Google Scholar 

  • Hamzah F, Idris A, Rashid R, Ming S (2009) Lactic acid production from microwave-alkali pre-treated empty fruit bunches fibre using Rhizopus oryzae pellet. J Appl Sci 9(17):3086–3091

    Article  CAS  Google Scholar 

  • Hashem AH, Suleiman WB, Abu-Elrish GM, El-Sheikh HH (2021) Consolidated bioprocessing of sugarcane bagasse to microbial oil by newly isolated Oleaginous Fungus: Mortierella wolfii. Arab J Sci Eng 46(1):199–211

    Article  CAS  Google Scholar 

  • Hassan SS, Tiwari BK, Williams GA, Jaiswal AK (2020) Bioprocessing of brewers’ spent grain for production of xylanopectinolytic enzymes by Mucor sp. Biores Technol Rep 9:100371. https://doi.org/10.1016/j.biteb.2019.100371

    Article  Google Scholar 

  • He Q, Rajendran A, Gan J, Lin H, Felt CA, Hu B (2019) Phosphorus recovery from dairy manure wastewater by fungal biomass treatment. Water Environ J 33(4):508–517

    Article  CAS  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(5532):1129–1133

    Article  PubMed  CAS  Google Scholar 

  • Hu K-J, Hu J-L, Ho K-P, Yeung K-W (2004) Screening of fungi for chitosan producers, and copper adsorption capacity of fungal chitosan and chitosanaceous materials. Carbohyd Polym 58(1):45–52. https://doi.org/10.1016/j.carbpol.2004.06.015

    Article  CAS  Google Scholar 

  • Ibarruri J, Cebrián M, Hernández I (2021) Valorisation of fruit and vegetable discards by fungal submerged and solid-state fermentation for alternative feed ingredients production. J Environ Manag 281:111901

  • Iturriaga E, Papp T, Breum J, Arnau J, Arturo P (2005) Strain and culture conditions improvement for β-carotene production with Mucor microbial processes and products. Springer, pp 239–256

  • James A, Casida L Jr (1964) Accumulation of phosphorus compounds by Mucor racemosus. J Bacteriol 87(1):150–155

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jones M, Kujundzic M, John S, Bismarck A (2020) Crab vs. mushroom: a review of crustacean and fungal chitin in wound treatment. Mar Drugs 18(1):64. https://doi.org/10.3390/md18010064

    Article  PubMed Central  CAS  Google Scholar 

  • Kamoun O, Muralitharan G, Belghith H, Gargouri A, Trigui-Lahiani H (2019) Suitable carbon sources selection and ranking for biodiesel production by oleaginous Mucor circinelloides using multi-criteria analysis approach. Fuel 257:116117

  • Karahalil E, Coban HB, Turhan I (2019) A current approach to the control of filamentous fungal growth in media: microparticle enhanced cultivation technique. Crit Rev Biotechnol 39(2):192–201

    Article  PubMed  CAS  Google Scholar 

  • Karimi K, Zamani A (2013) Mucor indicus: biology and industrial application perspectives: a review. Biotechnol Adv 31(4):466–481. https://doi.org/10.1016/j.biotechadv.2013.01.009

    Article  PubMed  CAS  Google Scholar 

  • Karimi S, Mahboobi Soofiani N, Lundh T, Mahboubi A, Kiessling A, Taherzadeh MJ (2019) Evaluation of filamentous fungal biomass cultivated on vinasse as an alternative nutrient source of fish feed: protein, lipid, and mineral composition. Fermentation 5(4):99

    Article  CAS  Google Scholar 

  • Kato Y, Nomura T, Ogita S, Takano M, Hoshino K (2013) Two new β-glucosidases from ethanol-fermenting fungus Mucor circinelloides NBRC 4572: enzyme purification, functional characterization, and molecular cloning of the gene. Appl Microbiol Biotechnol 97(23):10045–10056. https://doi.org/10.1007/s00253-013-5210-5

    Article  PubMed  CAS  Google Scholar 

  • Khanafari A, Tayari K, Emami M (2008) Light requirement for the carotenoids production by Mucor hiemalis

  • Kim WJ, Lee WG, Theodore K, Chang HN (2001) Optimization of culture conditions and continuous production of chitosan by the fungi Absidia Coerulea. Biotechnol Bioproc Eng 6(1):6–10. https://doi.org/10.1007/BF02942243

    Article  CAS  Google Scholar 

  • Klempová T, Slaný O, Šišmiš M, Marcinčák S, Čertík M (2020) Dual production of polyunsaturated fatty acids and beta-carotene with Mucor wosnessenskii by the process of solid-state fermentation using agro-industrial waste. J Biotechnol 311:1–11. https://doi.org/10.1016/j.jbiotec.2020.02.006

    Article  PubMed  CAS  Google Scholar 

  • Kooloth Valappil P, Rajasree KP, Abraham A, Christopher M, Sukumaran RK (2019) Characterization of a glucose tolerant β-glucosidase from Aspergillus unguis with high potential as a blend-in for biomass hydrolyzing enzyme cocktails. Biotech Lett 41(10):1201–1211. https://doi.org/10.1007/s10529-019-02724-z

    Article  CAS  Google Scholar 

  • Kosa G, Zimmermann B, Kohler A, Ekeberg D, Afseth NK, Mounier J, Shapaval V (2018) High-throughput screening of Mucoromycota fungi for production of low-and high-value lipids. Biotechnol Biofuels 11(1):1–17

    Article  Google Scholar 

  • Krisch J, Bencsik O, Papp T, Vágvölgyi C, Takó M (2012) Characterization of a β-glucosidase with transgalactosylation capacity from the zygomycete Rhizomucor miehei. Biores Technol 114:555–560. https://doi.org/10.1016/j.biortech.2012.02.117

    Article  CAS  Google Scholar 

  • Krisch J, Takó M, Papp T, Vágvölgyi C (2010) Characteristics and potential use of β-glucosidases from Zygomycetes. Curr Res Technol Educ Topics Appl Microbiol Microb Biotechnol 2:891–896

    Google Scholar 

  • Kupski L, Pagnussatt FA, Buffon JG, Furlong EB (2014) Endoglucanase and total cellulase from newly isolated Rhizopus oryzae and Trichoderma reesei: production, characterization, and thermal stability. Appl Biochem Biotechnol 172(1):458–468

    Article  PubMed  CAS  Google Scholar 

  • Kyle DJ (2010) Future development of single cell oils single cell oils. Elsevier, pp 439–451

  • Kyle DJ, Ratledge C (1992) Industrial applications of single cell oils. AOCS Publishing

  • Lebreton A, Meslet-Cladière L, Morin-Sardin S, Coton E, Jany J-L, Barbier G, Corre E (2019) Comparative analysis of five Mucor species transcriptomes. Genomics 111(6):1306–1314. https://doi.org/10.1016/j.ygeno.2018.09.003

    Article  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(4):255–261. https://doi.org/10.1016/j.jbiotec.2009.07.011

    Article  PubMed  CAS  Google Scholar 

  • Lennartsson PR, Niklasson C, Taherzadeh MJ (2011) A pilot study on lignocelluloses to ethanol and fish feed using NMMO pretreatment and cultivation with zygomycetes in an air-lift reactor. Biores Technol 102(6):4425–4432

    Article  CAS  Google Scholar 

  • Li L, Jin N (2020) Effect of nitrogen concentration on the growth and fatty acid content of Mortierella alpina. Int J Agric Biol 24(4):838–848

    CAS  Google Scholar 

  • Lima e Silva TA, Tambourgi EB, de Campos Takaki GM (2013) Inorganic polyphosphate accumulation by Cunninghamella elegans (UCP 542) and its influence in the decolorization of textile azo dye Orange II. Clean Technol Environ Policy 15(1):179-184

  • Lopez S, Bermudez B, Montserrat-de la Paz S, Jaramillo S, Varela LM, Ortega-Gomez A, Abia R, Muriana FJG (2014) Membrane composition and dynamics: a target of bioactive virgin olive oil constituents. Biochimica et Biophysica Acta (BBA) - Biomembranes 1838(6):1638–1656. https://doi.org/10.1016/j.bbamem.2014.01.007

  • Mackinney G, Nakayama T, Buss C, Chichester C (1952) Carotenoid production in Phycomyces. J Am Chem Soc 74(13):3456–3457

    Article  CAS  Google Scholar 

  • Mamani LDG, Magalhães AI Jr, Ruan Z, de Carvalho JC, Soccol CR (2019) Industrial production, patent landscape, and market trends of arachidonic acid-rich oil of Mortierella alpina. Biotechnol Res Innov 3(1):103–119

    Article  Google Scholar 

  • Martău GA, Mihai M, Vodnar DC (2019) The use of chitosan, alginate, and pectin in the biomedical and food sector—biocompatibility, bioadhesiveness, and biodegradability. Polymers 11(11):1837

  • Mehta BJ, Salgado LM, Bejarano ER, Cerdá-Olmedo E (1997) New mutants of Phycomyces blakesleeanus for (beta)-carotene production. Appl Environ Microbiol 63(9):3657–3661

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mhlongo S, Ezeokoli OT, Roopnarain A, Ndaba B, Sekoai PT, Habimana O, Pohl CH (2021) The potential of single-cell oils derived from filamentous fungi as alternative feedstock sources for biodiesel production. Front Microbiol 12:57

    Article  Google Scholar 

  • Mironov AA, Nemashkalov VA, Stepanova NN, Kamzolova SV, Rymowicz W, Morgunov IG (2018) The effect of pH and temperature on arachidonic acid production by glycerol-grown Mortierella alpina NRRL-A-10995. Fermentation 4(1):17

    Article  Google Scholar 

  • Miyoshi H, Shimura K, Watanabe K, Onodera K (1992) Characterization of some fungal chitosans. Biosci Biotechnol Biochem 56(12):1901–1905. https://doi.org/10.1271/bbb.56.1901

    Article  CAS  Google Scholar 

  • Mohamed H, El-Shanawany A-R, Shah AM, Nazir Y, Naz T, Ullah S, Mustafa K, Song Y (2020) Comparative analysis of different isolated oleaginous Mucoromycota fungi for their γ-linolenic acid and carotenoid production. BioMed Res Int 2020

  • Mohammadi M, Zamani A, Karimi K (2013) Effect of phosphate on glucosamine production by ethanolic fungus Mucor indicus. Appl Biochem Biotechnol 171(6):1465–1472. https://doi.org/10.1007/s12010-013-0440-7

    Article  PubMed  CAS  Google Scholar 

  • Mosqueda-Cano G, Gutiérrez-Corona JF (1995) Environmental and developmental regulation of carotenogenesis in the dimorphic fungus Mucor rouxii. Curr Microbiol 31(3):141–145

    Article  CAS  Google Scholar 

  • Muniraj IK, Uthandi SK, Hu Z, Xiao L, Zhan X (2015) Microbial lipid production from renewable and waste materials for second-generation biodiesel feedstock. Environ Technol Rev 4(1):1–16

    Article  CAS  Google Scholar 

  • Murashima K, Nishimura T, Nakamura Y, Koga J, Moriya T, Sumida N, Yaguchi T, Kono T (2002) Purification and characterization of new endo-1,4-β-d-glucanases from Rhizopus oryzae. Enzyme Microb Technol 30(3):319–326. https://doi.org/10.1016/S0141-0229(01)00513-0

    Article  CAS  Google Scholar 

  • Nagy G, Vaz AG, Szebenyi C, Takó M, Tóth EJ, Csernetics Á, Bencsik O, Szekeres A, Homa M, Ayaydin F (2019) CRISPR-Cas9-mediated disruption of the HMG-CoA reductase genes of Mucor circinelloides and subcellular localization of the encoded enzymes. Fungal Genet Biol 129:30–39

    Article  PubMed  CAS  Google Scholar 

  • Naude A, Nicol W (2018) Malic acid production through the whole-cell hydration of fumaric acid with immobilised Rhizopus oryzae. Biochem Eng J 137:152–161

    Article  CAS  Google Scholar 

  • Naz T, Nazir Y, Nosheen S, Ullah S, Halim H, Fazili ABA, Li S, Mustafa K, Mohamed H, Yang W (2020a) Redirecting metabolic flux towards the mevalonate pathway for enhanced β-carotene production in M. circinelloides CBS 277.49. BioMed Res Int 2020

  • Naz T, Nosheen S, Li S, Nazir Y, Mustafa K, Liu Q, Garre V, Song Y (2020b) Comparative analysis of β-carotene production by Mucor circinelloides strains CBS 277.49 and WJ11 under light and dark conditions. Metabolites 10(1):38

  • Papp T, Csernetics Á, Nagy G, Bencsik O, Iturriaga EA, Eslava AP, Vágvölgyi C (2013) Canthaxanthin production with modified Mucor circinelloides strains. Appl Microbiol Biotechnol 97(11):4937–4950

    Article  PubMed  CAS  Google Scholar 

  • Papp T, Velayos A, Bartók T, Eslava AP, Vágvölgyi C, Iturriaga EA (2006) Heterologous expression of astaxanthin biosynthesis genes in Mucor circinelloides. Appl Microbiol Biotechnol 69(5):526–531

    Article  PubMed  CAS  Google Scholar 

  • Patel A, Karageorgou D, Rova E, Katapodis P, Rova U, Christakopoulos P, Matsakas L (2020) An overview of potential oleaginous microorganisms and their role in biodiesel and omega-3 fatty acid-based industries. Microorganisms 8(3):434

    Article  PubMed Central  CAS  Google Scholar 

  • Pawłowska J, Okrasińska A, Kisło K, Aleksandrzak-Piekarczyk T, Szatraj K, Dolatabadi S, Muszewska A (2019) Carbon assimilation profiles of mucoralean fungi show their metabolic versatility. Sci Rep 9(1):11864. https://doi.org/10.1038/s41598-019-48296-w

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rajendran A, Fox T, Hu B (2017) Nutrient recovery from ethanol co-products by a novel mycoalgae biofilm: attached cultures of symbiotic fungi and algae. J Chem Technol Biotechnol 92(7):1766–1776. https://doi.org/10.1002/jctb.5177

    Article  CAS  Google Scholar 

  • Rajendran A, Hu B (2016) Mycoalgae biofilm: development of a novel platform technology using algae and fungal cultures. Biotechnol Biofuels 9(1):1–13

    Article  CAS  Google Scholar 

  • Ratledge C (1988) Biochemistry, stoichiometry, substrates and economics. Single cell oil 1

  • Ratledge C (1993) Single cell oils—have they a biotechnological future? Trends Biotechnol 11(7):278–284

    Article  PubMed  CAS  Google Scholar 

  • Ravi Kumar MNV (2000) A review of chitin and chitosan applications. React Funct Polym 46(1):1–27. https://doi.org/10.1016/S1381-5148(00)00038-9

    Article  Google Scholar 

  • Riou C, Salmon J-M, Vallier M-J, Günata Z, Barre P (1998) Purification, characterization, and substrate specificity of a novel highly glucose-tolerant β-glucosidase from Aspergillus oryzae. Appl Environ Microbiol 64(10):3607–3614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roa Engel CA, Straathof AJJ, Zijlmans TW, van Gulik WM, van der Wielen LAM (2008) Fumaric acid production by fermentation. Appl Microbiol Biotechnol 78(3):379–389. https://doi.org/10.1007/s00253-007-1341-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rodrigues Reis C, Ogero D’Otaviano L, Rajendran A, Hu B (2018) Co-culture of filamentous feed-grade fungi and microalgae as an alternative to increase feeding value of ethanol coproducts. Fermentation 4(4):86. https://doi.org/10.3390/fermentation4040086

    Article  CAS  Google Scholar 

  • Rodrigues Reis CE, Rajendran A, Silva MB, Hu B, de Castro HF (2018) The application of microbial consortia in a biorefinery context: understanding the importance of artificial lichens. In: Singh OV, Chandel AK (eds) Sustainable biotechnology—enzymatic resources of renewable energy. Springer International Publishing, Cham, pp 423–437

    Chapter  Google Scholar 

  • Ruan Z, Zanotti M, Wang X, Ducey C, Liu Y (2012) Evaluation of lipid accumulation from lignocellulosic sugars by Mortierella isabellina for biodiesel production. Biores Technol 110:198–205

    Article  CAS  Google Scholar 

  • Rusdan IH, Kusnadi J (2017) Production of mozzarella cheese using rennin enzyme from Mucor miehei grown at rice bran molasses medium. In: IOP Conference Series: Materials Science and Engineering. vol 193. IOP Publishing, p 012011

  • Safaei Z, Karimi K, Zamani A (2016) Impact of phosphate, potassium, yeast extract, and trace metals on chitosan and metabolite production by Mucor indicus. Int J Mol Sci 17(9). https://doi.org/10.3390/ijms17091429

  • Saha BC (2004) Production, purification and properties of endoglucanase from a newly isolated strain of Mucor circinelloides. Process Biochem 39(12):1871–1876. https://doi.org/10.1016/j.procbio.2003.09.013

    Article  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  PubMed Central  CAS  Google Scholar 

  • Sahlan M, Hermansyah H, Wijarnako A, Gozan M, Lischer K, Ahmudi A, Pujianto P (2020) Ethanol production by encapsulated Rhizopus oryzae from oil palm empty fruit bunch. Evergreen 7(1):92–96

    Article  CAS  Google Scholar 

  • Sandmann G (1994) Carotenoid biosynthesis in microorganisms and plants. Eur J Biochem 223(1):7–24

    Article  PubMed  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(8):e23102

  • Satari B, Karimi K (2018) Mucoralean fungi for sustainable production of bioethanol and biologically active molecules. Appl Microbiol Biotechnol 102(3):1097–1117. https://doi.org/10.1007/s00253-017-8691-9

    Article  PubMed  CAS  Google Scholar 

  • Satari B, Karimi K, Taherzadeh MJ, Zamani A (2016) Co-production of fungal biomass derived constituents and ethanol from citrus wastes free sugars without auxiliary nutrients in airlift bioreactor. Int J Mol Sci 17(3):302

    Article  PubMed  PubMed Central  Google Scholar 

  • Satari B, Karimi K, Zamani A (2016) Oil, chitosan, and ethanol production by dimorphic fungus Mucor indicus from different lignocelluloses. J Chem Technol Biotechnol 91(6):1835–1843

    Article  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 

  • Shafiei Alavijeh R, Karimi K, van den Berg C (2020) An integrated and optimized process for cleaner production of ethanol and biodiesel from corn stover by Mucor indicus. J Clean Prod 249:119321. https://doi.org/10.1016/j.jclepro.2019.119321

    Article  CAS  Google Scholar 

  • Shari’a AEdN, Nascimento AEd, Lima MABd, Campos-Takaki GMd, Souza Wd (2002) Polyphosphate in Zygomycetes: a cytochemical study. Braz J Microbiol 33:119–126

    Article  Google Scholar 

  • Shimonaka A, Baba Y, Koga J, Nakane A, Kubota H, Kono T (2004) Molecular cloning of a gene encoding endo-β-D-1, 4-glucanase PCE1 from Phycomyces nitens. Biosci Biotechnol Biochem 68(11):2299–2305

    Article  PubMed  CAS  Google Scholar 

  • Shimonaka A, Koga J, Baba Y, Nishimura T, Murashima K, Kubota H, Kono T (2006) Specific characteristics of family 45 endoglucanases from Mucorales in the use of textiles and laundry. Biosci Biotechnol Biochem 70(4):1013–1016

    Article  PubMed  CAS  Google Scholar 

  • Skory C (2004) Lactic acid production by Rhizopus oryzae transformants with modified lactate dehydrogenase activity. Appl Microbiol Biotechnol 64(2):237–242

    Article  PubMed  CAS  Google Scholar 

  • Slaný O, Klempová T, Marcinčák S, Čertík M (2020) Production of high-value bioproducts enriched with γ-linolenic acid and β-carotene by filamentous fungi Umbelopsis isabellina using solid-state fermentations. Ann Microbiol 70(1):1–11

    Google Scholar 

  • Slaný O, Klempová T, Shapaval V, Zimmermann B, Kohler A, Čertík M (2020) Biotransformation of animal fat-by products into ARA-enriched fermented bioproducts by solid-state fermentation of Mortierella alpina. J Fungi 6(4):236

    Article  Google Scholar 

  • Souza Filho PF, Zamani A, Taherzadeh MJ (2017) Production of edible fungi from potato protein liquor (PPL) in airlift bioreactor. Fermentation 3(1):12

    Article  Google Scholar 

  • Srinuanpan S, Cheirsilp B, Prasertsan P, Kato Y, Asano Y (2018) Photoautotrophic cultivation of oleaginous microalgae and co-pelletization with filamentous fungi for cost-effective harvesting process and improved lipid yield. Aquacult Int 26(6):1493–1509. https://doi.org/10.1007/s10499-018-0300-0

    Article  CAS  Google Scholar 

  • Struszczyk-Świta K, Stańczyk Ł, Szczęsna-Antczak M, Antczak T (2017) Scale-up of PUF-immobilized fungal chitosanase–lipase preparation production. Prep Biochem Biotechnol 47(9):909–917

    Article  PubMed  Google Scholar 

  • Subczynski WK, Markowska E, Sielewiesiuk J (1991) Effect of polar carotenoids on the oxygen diffusion-concentration product in lipid bilayers. An EPR spin label study. Biochimica et Biophysica Acta (BBA)-Biomembranes 1068(1):68–72

  • Sues A, Millati R, Edebo L, Taherzadeh MJ (2005) Ethanol production from hexoses, pentoses, and dilute-acid hydrolyzate by Mucor indicus. FEMS Yeast Res 5(6–7):669–676. https://doi.org/10.1016/j.femsyr.2004.10.013

    Article  PubMed  CAS  Google Scholar 

  • Svensson SE, Bucuricova L, Ferreira JA, Souza Filho PF, Taherzadeh MJ, Zamani A (2021) Valorization of bread waste to a fiber-and protein-rich fungal biomass. Fermentation 7(2):91

    Article  CAS  Google Scholar 

  • Sørensen A, Lübeck PS, Lübeck M, Teller PJ, Ahring BK (2011) β-Glucosidases from a new Aspergillus species can substitute commercial β-glucosidases for saccharification of lignocellulosic biomass. Can J Microbiol 57(8):638–650

    Article  PubMed  Google Scholar 

  • Takano M, Hoshino K (2012) Direct ethanol production from rice straw by coculture with two high-performing fungi. Front Chem Sci Eng 6(2):139–145. https://doi.org/10.1007/s11705-012-1281-6

    Article  CAS  Google Scholar 

  • Takano M, Hoshino K (2018) Bioethanol production from rice straw by simultaneous saccharification and fermentation with statistical optimized cellulase cocktail and fermenting fungus. Bioresour Bioproc 5(1):16. https://doi.org/10.1186/s40643-018-0203-y

    Article  Google Scholar 

  • Takó M, Farkas E, Lung S, Krisch J, Vágvölgyi C, Papp T (2010) Identification of acid-and thermotolerant extracellular β-glucosidase activities in Zygomycetes fungi. Acta Biol Hung 61(1):101–110

    Article  PubMed  Google Scholar 

  • Takó M, Kotogán A, Krisch J, Vágvölgyi C, Mondal KC, Papp T (2015) Enhanced production of industrial enzymes in Mucoromycotina fungi during solid-state fermentation of agricultural wastes/by-products. Acta Biol Hung 66(3):348–360

    Article  PubMed  Google Scholar 

  • Takó M, Kotogán A, Papp T, Kadaikunnan S, Alharbi NS, Vágvölgyi C (2017) Purification and properties of extracellular lipases with transesterification activity and 1, 3-regioselectivity from Rhizomucor miehei and Rhizopus oryzae. J Microbiol Biotechnol 27(2):277–288

    Article  PubMed  Google Scholar 

  • Tan SC, Tan TK, Wong SM, Khor E (1996) The chitosan yield of zygomycetes at their optimum harvesting time. Carbohyd Polym 30(4):239–242. https://doi.org/10.1016/s0144-8617(96)00052-5

    Article  CAS  Google Scholar 

  • Tang X, Chang L, Gu S, Zhang H, Chen YQ, Chen H, Zhao J, Chen W (2021) Role of beta-isopropylmalate dehydrogenase in lipid biosynthesis of the oleaginous fungus Mortierella alpina. Fungal Genet Biol 152:103572. https://doi.org/10.1016/j.fgb.2021.103572

    Article  PubMed  CAS  Google Scholar 

  • Tang X, Chen H, Gu Z, Zhang H, Chen YQ, Song Y, Chen W (2017) Comparative proteome analysis between high lipid-producing strain Mucor circinelloides WJ11 and low lipid-producing strain CBS 277.49. J Agricult Food Chem 65(24):5074–5082

    Article  CAS  Google Scholar 

  • Tang X, Chen H, Gu Z, Zhang H, Chen YQ, Song Y, Chen W (2020) Role of g 6 pdh and leuB on lipid accumulation in Mucor circinelloides. J Agric Food Chem 68(14):4245–4251

    Article  PubMed  CAS  Google Scholar 

  • Thongchul N, Navankasattusas S, Yang S-T (2010) Production of lactic acid and ethanol by Rhizopus oryzae integrated with cassava pulp hydrolysis. Bioprocess Biosyst Eng 33(3):407–416

    Article  PubMed  CAS  Google Scholar 

  • Tijssen J, Van Steveninck J, De Bruijn W (1985) Cytochemical staining of a yeast polyphosphate fraction, localized outside the plasma membrane. Protoplasma 125(1–2):124–128

    Article  CAS  Google Scholar 

  • Tzimorotas D, Afseth NK, Lindberg D, Kjørlaug O, Axelsson L, Shapaval V (2018) Pretreatment of different food rest materials for bioconversion into fungal lipid-rich biomass. Bioprocess Biosyst Eng 41(7):1039–1049

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ueng PP, Gong C-s (1982) Ethanol production from pentoses and sugar-cane bagasse hemicellulose hydrolysate by Mucor and Fusarium species. Enzyme Microb Technol 4(3):169–171

    Article  CAS  Google Scholar 

  • Vadivelan G, Rao PP, Venkateswaran G (2017) Influence of supplementation of vegetable oil blends on omega-3 fatty acid production in Mortierella alpina CFR-GV15. BioMed Res Int 2017

  • Wang H, Zhang C, Chen H, Gu Z, Zhao J, Zhang H, Chen YQ, Chen W (2020) Tetrahydrobiopterin plays a functionally significant role in lipogenesis in the oleaginous fungus Mortierella alpina. Front Microbiol 11:250

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Pang J, Zheng Y, Jiang P, Gong W, Chen X, Chen D (2017) Genetic manipulation of the bifunctional gene, carRA, to enhance lycopene content in Blakeslea trispora. Biochem Eng J 119:27–33

    Article  CAS  Google Scholar 

  • Wei H, Wang W, Yarbrough JM, Baker JO, Laurens L, Van Wychen S, Chen X, Taylor LE, Xu Q, Himmel ME (2013) Genomic, proteomic, and biochemical analyses of oleaginous Mucor circinelloides: evaluating its capability in utilizing cellulolytic substrates for lipid production. PloS one 8(9):e71068

  • Werner TP, Amrhein N, Freimoser FM (2007) Specific localization of inorganic polyphosphate (poly P) in fungal cell walls by selective extraction and immunohistochemistry. Fungal Genet Biol 44(9):845–852

    Article  PubMed  CAS  Google Scholar 

  • White SA, Farina PR, Fulton I (1979) Production and isolation of chitosan from Mucor rouxii. Appl Environ Microbiol 38(2):323–328. https://doi.org/10.1128/AEM.38.2.323-328.1979

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ye Y, Gan J, Hu B (2015) Screening of phosphorus-accumulating fungi and their potential for phosphorus removal from waste streams. Appl Biochem Biotechnol 177(5):1127–1136

    Article  PubMed  CAS  Google Scholar 

  • Yegin S, Fernandez-Lahore M, Jose Gama Salgado A, Guvenc U, Goksungur Y, Tari C (2011) Aspartic proteinases from Mucor spp. in cheese manufacturing. Appl Microbiol Biotechnol 89(4):949–960. https://doi.org/10.1007/s00253-010-3020-6

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Navarro E, Cánovas-Márquez JT, Almagro L, Chen H, Chen YQ, Zhang H, Torres-Martínez S, Chen W, Garre V (2016) 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 15(1):1–14

    Article  Google Scholar 

  • Zhang Y, Song Y (2021) Lipid accumulation by xylose metabolism engineered Mucor circinelloides strains on corn straw hydrolysate. Appl Biochem Biotechnol 193(3):856–868

    Article  PubMed  Google Scholar 

  • Zhao H, Lv M, Liu Z, Zhang M, Wang Y, Ju X, Song Z, Ren L, Jia B, Qiao M (2020) High-yield oleaginous fungi and high-value microbial lipid resources from Mucoromycota. BioEnergy Res 1–11

  • Zheng Y-x, Wang Y-l, Pan J, Zhang J-r, Dai Y, Chen K-y (2017) Semi-continuous production of high-activity pectinases by immobilized Rhizopus oryzae using tobacco wastewater as substrate and their utilization in the hydrolysis of pectin-containing lignocellulosic biomass at high solid content. Biores Technol 241:1138–1144

    Article  CAS  Google Scholar 

  • Zininga JT, Puri AK, Govender A, Singh S, Permaul K (2019) Concomitant production of chitosan and lipids from a newly isolated Mucor circinelloides ZSKP for biodiesel production. Biores Technol 272:545–551. https://doi.org/10.1016/j.biortech.2018.10.035

    Article  CAS  Google Scholar 

  • Zorn SMFE, Reis CER, Silva MB, Hu B, De Castro HF (2020) Consortium growth of filamentous fungi and microalgae: evaluation of different cultivation strategies to optimize cell harvesting and lipid accumulation. Energies 13(14):3648. https://doi.org/10.3390/en13143648

    Article  CAS  Google Scholar 

  • zu Berstenhorst SM, Hohmann HP, Stahmann KP (2009) Vitamins and vitamin-like compounds: microbial production. In: Schaechter M (ed) Encyclopedia of microbiology (third edition). Academic Press, Oxford, pp 549-561

Download references

Funding

Open Access funding provided by Norwegian University of Life Sciences. The study was funded by the Research Council of Norway-FMETEKN grant, project number 257622; BIONÆR grant, project number 305215; DAAD grant, project number 309220; HAVBRUK2 grant, project number 302543/E40; MATFONDAVTALE grant, project number 301834/E50.

Author information

Authors and Affiliations

Authors

Contributions

Conceived the research idea: SD, VS. Wrote the manuscript: SD, CB, BG, KF, VS. Discussed and revised the manuscript: SD, VS, CB, BG. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Volha Shapaval.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 179 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dzurendova, S., Losada, C.B., Dupuy-Galet, B.X. et al. Mucoromycota fungi as powerful cell factories for modern biorefinery. Appl Microbiol Biotechnol 106, 101–115 (2022). https://doi.org/10.1007/s00253-021-11720-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-021-11720-1

Keywords

Navigation