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.
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Notes
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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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Economou CN, Aggelis G, Pavlou S, Vayenas DV (2011) Single cell oil production from rice hulls hydrolysate. Biores Technol 102(20):9737–9742
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
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
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
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
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
Ghormade V, Pathan E, Deshpande M (2017) Can fungi compete with marine sources for chitosan production? Int J Biol Macromol 104:1415–1421
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Rajendran A, Hu B (2016) Mycoalgae biofilm: development of a novel platform technology using algae and fungal cultures. Biotechnol Biofuels 9(1):1–13
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
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
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
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
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
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
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
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
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
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
Sandmann G (1994) Carotenoid biosynthesis in microorganisms and plants. Eur J Biochem 223(1):7–24
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
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
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
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
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
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
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
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
Skory C (2004) Lactic acid production by Rhizopus oryzae transformants with modified lactate dehydrogenase activity. Appl Microbiol Biotechnol 64(2):237–242
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
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
Souza Filho PF, Zamani A, Taherzadeh MJ (2017) Production of edible fungi from potato protein liquor (PPL) in airlift bioreactor. Fermentation 3(1):12
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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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.
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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.
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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
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DOI: https://doi.org/10.1007/s00253-021-11720-1