Abstract
Global demand for biotechnological products has increased steadily over the years. Thus, need for optimized processes and reduced costs appear as a key factor in the success of this market. A process tool of high importance is the direct or indirect use of enzymes to catalyze the generation of various substances. Also, obtaining aromas and pigments from natural sources has becoming priority in cosmetic and food industries in order to supply the demand from consumers to substitute synthetic compounds, especially when by-products can be used as starting material for this purpose. Species from Fusarium genera are recognized as promising sources of several enzymes for industrial application as well as biocatalysts in the production of aromas, pigments and second generation biofuels, among others. In addition, secondary metabolites from these strains can present important biological activities for medical field. In this approach, this review brings focus on the use of Fusarium sp. strains in biotechnological production of compounds of industrial interest, showing the most recent researches in this area, results obtained and the best process conditions for each case.
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References
Aditiya HB, Mahila TMI, Chong WT, Nur H, Sebayang AH (2016) Second generation bioethanol production: a critical review. Renew Sust Energ Rev 66:631–653. doi:10.1016/j.rser.2016.07.015
Akilandeswari P, Pradeep BV (2016) Exploration of industrially important pigments from soil fungi. Appl Microbiol Biotechnol 100:1631–1643. doi:10.1007/s00253-015-7231-8
Alfenore S, Molina-Jouve C (2016) Current status and future prospects of conversion of lignocellulosic resources to biofuels using yeast and bacteria. Process Biochem (In Press). doi:10.1016/j.procbio.2016.07.028
Ali SS, Khan M, Fagan B, Mullins E, Doohan FM (2012) Exploiting the inter-strain divergence of Fusarium oxysporum for microbial bioprocessing of lignocellulose to bioethanol. AMB Expr 2:16. doi:10.1186/2191-0855-2-16
Ali SS, Nugent B, Mullins E, Doohan FM (2016) Fungal-mediated consolidated bioprocessing: the potential of Fusarium oxysporum for the lignocellulosic ethanol industry. AMB Expr 6:13. doi:10.1186/s13568-016-0185-0
Ali SS, Vidhale NN (2013) Protease production by Fusarium oxysporum in solid-state fermentation using rice bran. Am J Microbiol Res 1:45–47 doi: 10.12691/ajmr-1-3-2
Almeida MN (2013) Complexo celulolítico e hemicelulolítico do fungo endofítico Fusarium verticillioides e sua aplicação para sacarificação do bagaço de cana. Federal University of Viçosa, Dissertation
Almeida MN, Falkoski DL, Guimarães VM, Ramos HJO, Visser EM, Maitan-Alfenas GP, Rezende ST (2013) Characteristics of free endoglucanase and glycosidases multienzyme complex from Fusarium verticillioides. Bioresour Technol 143:413–422. doi:10.1016/j.biortech.2013.06.021
Almeida MN, Guimarães VM, Falkoski DL, Paes GBT, Ribeiro JI Jr, Visser EM, Alfenas RF, Pereira OL, Rezende ST (2014) Optimization of endoglucanase and xylanase activities from Fusarium verticillioides for simultaneous saccharification and fermentation of sugarcane bagasse. Appl Biochem Biotechnol 172:1332–1346. doi:10.1007/s12010-013-0572-9
Amoah J, Ho S, Hama S, Yoshida A, Nakanishi A, Hasunuma T, Ogino C, Kondo A (2016) Converting oils high in phospholipids to biodiesel using immobilized Aspergillus oryzae whole-cell biocatalysts expressing Fusarium heterosporum lipase. Biochem Eng J 105:10–15. doi:10.1016/j.bej.2015.08.007
Anasontzis GE, Christakopoulos P (2014) Challenges in ethanol production with Fusarium oxysporum through consolidated bioprocessing. Bioengineered 5:393–395. doi:10.4161/bioe.36328
Anasontzis GE, Zerva A, Stathopoulou PM, Haralampidis K, Diallinas GD, Karagouni AD, Hatzinikolaou (2011) Homologous overexpression of xylanase in Fusarium oxysporum increases ethanol productivity during consolidates bioprocessing (CBP) of lignocellulosics. J Biotechnol 152:16–23 doi: 10.1016/j.jbiotec.2011.01.002
Andre C, Charmoille L (1999) Fusarium isolate and lipases, cutinases and enzyme compositions derived therefrom. USA US5990069A
Ariyarathna IR, Karunarathne DN (2016) Microencapsulation stabilizes curcumin for efficient delivery in food applications. Food Packag Shelf Life 10:79–86. doi:10.1016/j.fpsl.2016.10.005
Arndt B, Studt L, Wiemann P, Osmanov H, Kleigrewe K, Kӧhler J, Krug I, Tudzynski B, Humpf HU (2015) Genetic engineering, high resolution mass spectrometry and nuclear magnetic resonance spectroscopy elucidate the bikaverin biosynthetic pathway in Fusarium fujikuroi. Fungal Genet Biol 84:26–36. doi:10.1016/j.fgb.2015.09.006
Arnstein HR, Cook AH, Lacey MS (1946) An antibacterial pigment from Fusarium javanicum. Nature 157:333. doi:10.1038/157333b0
Ashley JN, Hobbs BC, Raistrick H (1937) Studies in the biochemistry of microorganisms LIII. The crystalline colouring matters of Fusarium culmorum (W.G. Smith) Sacc. and related forms. Biochem J 31:385–397. doi:10.1042/bj0310385
Baeyens J, Kang Q, Appels L, Dewil R, Lv Y, Tan T (2015) Challenges and opportunities in improving the production of bio-ethanol. Prog Energy Combust Sci 47:60–88. doi:10.1016/j.pecs.2014.10.003
Baker RA, Tatum JH, Nemec S Jr (1990) Antimicrobial activity of naphthoquinones from fusaria. Mycopathologia 111:9–15. doi:10.1007/bf02277294
Barros DPC, Azevedo AM, Cabral JMS, Fonseca LP (2012) Optimization of flavor esters synthesis by Fusarium solani pisi cutinase. J Food Biochem 36:275–284. doi:10.1111/j.1745-4514.2010.00535.x
Behera SS, Ray RC (2016) Solid state fermentation for production of microbial cellulases: recent advances and improvement strategies. I J Biological Macromol 86:656–669. doi:10.1016/j.ijbiomac.2015.10.090
Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1-26 doi:10.10338/já.2005.1
Berger RG (2009) Biotechnology of flavours--the next generation. Biotechnol Lett 31:1651–1659. doi:10.1007/s10529-009-0083-5
Bicas J, Barros F, Wagner R (2008) Optimization of R-(+)-α-terpineol production by the biotransformation of R-(+)-limonene. J Ind Microbiol Biotechnol 35:1061–1070. doi:10.1007/s10295-008-0383-0
Bicas J, de Quadros C, Néri-Numa I, Pastore G (2010a) Integrated process for co-production of alkaline lipase and R-(+)-α-terpineol by Fusarium oxysporum. Food Chem 120:452–456. doi:10.1016/j.foodchem.2009.10.037
Bicas JL, Dionísio AP, Pastore GM (2009) Bio-oxidation of terpenes: an approach for the flavor industry. Chem Rev 109:4518–4531. doi:10.1021/cr800190y
Bicas JL, Silva C, Dionísio AP, Pastore M (2010b) Biotechnological production of bioflavors and functional sugars. Ciênc Tecnol Aliment 30:7–18
Bicas JL, Silva WS (2013a) Process of production and deriving pigment application of the fungus Fusarium oxysporum Brazil:BR102013015305
Bicas JL, Silva WS (2013b) Processes of dyeing of fabrics and plastics using fungous pigments Brazil:BR102013027036
Boonla O, Kukongviriyapan U, Pakdeechote P, Kukongviriyapan V, Pannangpetch P, Prachaney P, Greenwald SE (2014) Curcumin improves endothelial dysfunction and vascular remodelling in 2K-1C hypertensive rats by raising nitric oxide availability and reducing oxidative stress. Nitric Oxide 42:44–53. doi:10.1016/j.niox.2014.09.001
Boonyapranai K, Tungpradit R, Hieochaiphant S (2008) Optimization of submerged culture for the production of naphthoquinones pigment by Fusarium verticillioides. Chiang Mai J Sci 35:457–466
Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev 11:21–32. doi:10.3389/fmicb.2014.00656
Brakhage AA, Schroeckh V (2011) Fungal secondary metabolites—strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22. doi:10.1016/j.fgb.2010.04.004
Brown TR (2015) A techno-economic review of thermochemical cellulosic biofuel pathways. Bioresour Technol 178:166–176. doi:10.1016/j.biortech.2014.09.053
Burdock GA (2010) Fenaroli’s handbook of flavor ingredients, sixth. CRC Press, Boca Raton
Carocho M, Morales P, Ferreira ICFR (2015) Natural food aditives: quo vadis? Trends Food Sci Tech 45:284–295. doi:10.1016/j.tifs.2015.06.007
Chhaya U, Gupte A (2013) Effect of different cultivation conditions and inducers on the production of laccase by the litter-dwelling fungal isolate Fusarium incarnatum LD-3 under solid substrate fermentation. Ann Microbiol 63:215–223. doi:10.1007/s13213-012-0464-1
Christakopoulos P, Macris BJ, Kekos D (1989) Direct fermentation of cellulose to ethanol by Fusarium oxysporum. Enzym Microb Technol 11:236–239. doi:10.1016/0141-0229(89)90098-7
Christakopoulos P, Tzalas B, Mamma D, Stamatis H, Liadakis GN, Tzia C, Kekos D, Kolisis FN, Macris BJ (1998) Production of an esterase from Fusarium oxysporum catalysing transesterification reactions in organic solvents. Process Biochem 33:729–733. doi:10.1016/S0032-9592(98)00039-9
Cortinovis C, Pizzo F, Spicer LJ, Caloni F (2013) Fusarium mycotoxins: effects on reproductive function in domestic animals—a review. Theriogenology 80:557–564. doi:10.1016/j.theriogenology.2013.06.018
De Carvalho CCCR, da Fonseca MMR (2006) Biotransformation of terpenes. Biotechnol Adv 24:134–142. doi:10.1016/j.biotechadv.2005.08.004
De Castro RJS, Sato HH (2013) Synergistic effects of agroindustrial wastes on simultaneous production of protease and α-amylase under solid state fermentation using a simplex centroid mixture design. Ind Crop Prod 49:813–821. doi:10.1016/j.indcrop.2013.07.002
Deshmukh R, Mathew A, Purohit HJ (2014) Characterization of antibacterial activity of bikaverin from Fusarium sp. HKF15. J Biosci Bioeng 117:443–448. doi:10.1016/j.jbiosc.2013.09.017
Deshmukh RR, Vidhale NN (2015) Effect of pH on the production of protease by Fusarium oxysporum using agroindustrial waste. Biosci Biotech Res Comm 8:78–83
Dhake KP, Thakare DD, Bhanage BM (2013) Lipase: a potential biocatalyst for the synthesis of valuable flavour and fragrance ester compounds. Flavour Fragr J 28:71–83. doi:10.1002/ffj.3140
Ding L, Dahse HM, Hertweck (2012) Cytotoxic alkaloids from Fusarium incarnatum associated with the mangrove tree Aegiceras corniculatum. J Nat Prod 75:617–621 doi: 10.1021/np2008544
Ding TZ, Cai L, Dong JW (2016) Fusarium sp fermentation of Fusarium through a solid one creation of a new antimicrobials sambacide method China:CN106117293
Dong JW, Cai L, Li XJ, Duan RT, Shu Y, Chen FY, Wang JP, Zhou H, Ding ZT (2016) Production of a new tetracyclic triterpene sulfate metabolite sambacide by solid-state cultivated Fusarium sambucinum B10.2 using potato as substrate. Bioresour Technol 218:1266–1270. doi:10.1016/j.biortech.2016.07.014
Du L, Lou L (2009) PKS and NRPS release mechanisms. Nat Prod Rep 27:255–278. doi:10.1039/b912037h
Dufossé L, Galaup P, Yaron A, Arad SM, Blanc P, Murthy KNC, Ravishankar GA (2005) Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality? Trends Food Sci Tech 16:389–406. doi:10.1016/j.tifs.2005.02.006
Duran N, Teixeira MFS, De Conti R, Esposito E (2002) Ecological-friendly pigments from fungi. Crit Rev Food Sci Nutr 42:53–66. doi:10.1080/10408690290825457
Dvorska JE, Surai PF, Speake BK, Sparks NHC (2001) Effect of the mycotoxin aurofusarin on the antioxidant composition and fatty acid profile of quail eggs. Br Poult Sci 42:643–649. doi:10.1080/00071660120088470
Dvorska JE, Surai PF, Speake BK, Sparks NHC (2002) Antioxidant systems of the developing quail embryo are compromised by mycotoxin aurofusarin. Comp Biochem Physiol C Toxicol Pharmacol 131:197–205. doi:10.1016/s1532-0456(02)00006-6
Edel-Hermann V, Gautheron N, Mounier A, Steinberg C (2015) Fusarium diversity in soil using a specific molecular approach and a cultural approach. J Microbiol Methods 111:64–71. doi:10.1016/j.mimet.2015.01.026
Escrivá L, Font F, Manyes L (2015) In vivo toxicity studies of fusarium mycotoxins in the last decade: a review. Food Chem Toxicol 78:185–206. doi:10.1016/j.fct.2015.02.005
Farhangi B, Alizadeh AM, Khodayari H, Khodayari S, Dehghan MJ, Khori V, Heidarzadeh A, Khaniki M, Sadeghiezadeh M, Najafi F (2015) Protective effects of dendrosomal curcumin on an animal metastatic breast tumor. Eur J Pharmacol 758:188–196. doi:10.1016/j.ejphar.2015.03.076
Feron G, Bonnarme P, Durand A (1996) Prospects for the microbial production of food flavours. Trends Food Sci Technol 7:285–293. doi:10.1016/0924-2244(96)10032-7
Feron G, Waché Y (2006) Microbial biotechnology of food flavor production. In: Paliyath G, Pometto A, Levin R (eds) Shetty K. CRC Press Taylor & Franc, Food Biotechnology, pp 407–442
Fox EM, Howlett B (2008) Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol 11:481–487
Frandsen RJ, Nielsen NJ, Maolanon N, Sørensen JC, Olsson S, Nielsen J, Giese H (2006) The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a clone link between the naphthoquinones and naphthopyrones. Mol Microbiol 61:1069–1080. doi:10.1111/j.1365-2958.2006.05295.x
Frandsen RJN, Rasmussen SA, Knudsen PB, Uhlig S, Petersen D, Lysøe E, Gotfredsen CH, Giese H, Larsen TO (2016) Black perithecial pigmentation in Fusarium species is due to the accumulation of 5-deoxybostrycoidin-based melanin. Sci Rep 6:26206. doi:10.1038/srep26206
Fu Y, Gao R, Cao Y, Guo M, Wei Z, Zhou E, Li Y, Yao M, Yang Z, Zhang N (2014) Curcumin attenuates inflammatory responses by supressing TLR4-mediated NF-kB signaling pathway in lipopolysaccharide-induced mastitis in mice. Int Immunopharmacol 20:54–58. doi:10.1016/j.intimp.2014.01.024
Furusawa M, Hashimoto T, Noma Y, Asakawa Y (2005) Biotransformation of citrus aromatics nootkatone and valencene by microorganisms. Chem Pharm Bull 53:1423–1429. doi:10.1248/cpb.53.1423
Gessler NN, Egorova AS, Belozerskaya TA (2013) Fungal anthraquinones. Appl Biochem Microbiol 49:85–99. doi:10.1134/s000368381302004x
Grabarczyk M (2012) Fungal strains as catalysts for the biotransformation of halolactones by hydrolytic dehalogenation with the dimethylcyclohexane system. Molecules 17:9741–9753. doi:10.3390/molecules17089741
Gupta A, Verma JP (2015) Sustainable bio-ethanol production from agro-residues: a review. Renew Sust Energ Rev 41:550–567. doi:10.1016/j.rser.2014.08.032
Gupta VK, Kubicek CP, Berrin JG, Wilson DW, Couturier M, Berlin A, Filho EXF, Ezeji T (2016) Fungal enzymes for bio-products from sustainable and waste biomass. Trends Biochem Sci 41:633–645. doi:10.1016/j.tibs.2016.04.006
Hagedorn S, Kaphammer B (1994) Microbial biocatalysis in the generation of flavor and fragrance chemicals. Ann Rev Microbiol 48:773–780. doi:10.1146/annurev.mi.48.100194.004013
Hama S, Tamalampudi S, Suzuki Y, Yoshida A, Kufuda H, Kondo A (2008) Preparation and comparative characterization of immobilized Aspergillus oryzae expressing Fusarium heterosporum lipase for enzymatic biodiesel production. Appl Microbiol Biotechnol 81:637–645. doi:10.1007/s00253-008-1689-6
Hamilton MA, Knorr MS, Cajori FA (1953) Experimental studies of an antibiotic derived from Fusarium bostrycoides. Antibiot Chemother 3:853–860
Hanson JR (2008) The chemistry of fungi. The Royal Society of Chemistry, Cambrige, pp 1–114
Harish BS, Ramaiah MJ, Uppulur KB (2015) Bioengineering strategies on catalysis for the effective production of renewable and sustainable energy. Renew Sust Energ Rev 51:533–547. doi:10.1016/j.rser.2015.06.030
Huang Z, Yang R, Guo Z, She Z, Lin Y (2010) New anthraquinone derivative produced by cultivation of mangrove endophytic fungus Fusarium sp. ZZF60 from the South China Sea. Chin J Appl Chem 27:394–395
Husson F, Couturier A, Kermasha S, Belin JM (1998a) Induction and localization of a lipoxygenase from Fusarium proliferatum. J Mol Catal - B Enzym 5:159–163. doi:10.1016/S1381-1177(98)00026-5
Husson F, Pagot Y, Kermasha S, Belin JM (1998b) Fusarium proliferatum: induction and intracellular location of a lipoxygenase. Enzym Microb Technol 23:42–48. doi:10.1016/S0141-0229(98)00009-X
Ibrahim SRM, Abdallah HM, Mohamed GA, Ross SA (2016b) Integracides H-J: new tetracyclic triterpenoids from the endophytic fungus Fusarium sp. Fitoterapia 112:161–167. doi:10.1016/j.fitote.2016.06.002
Ibrahim SRM, Elkhayat ES, Mohamed GA, Fat’hi SM, Ross SA (2016a) Fusarithioamide A, a new antimicrobial and cytotoxic benzamide derivative from the endophytic fungus Fusarium chlamydosporium. Biochem Biophys Res Commun 479:211–216. doi:10.1016/j.bbrc.2016.09.041
Ibrahim SRM, Mohamed GA, Ross AS (2016c) Integracides F and G: new tetracyclic triterpenoids from the endophytic fungus Fusarium sp. Phytochem Lett 15:125–130. doi:10.1016/j.phytol.2015.12.010
Indira D, Sharmila D, Balasubramanian P, Thirugnanam A, Jayabalan R (2016) Utilization of sea water based media for the production and characterization of cellulase by Fusarium subglutinans MTCC 11891. Biocatal Agric Biotechnol 7:187–192. doi:10.1016/j.bcab.2016.06.006
Jackson M, Andersen C, Beier L, Friis EP, Toscano MDGP, Bjoernvad M, Rasmussen FW, Christiansen LS, Souter PF, Bewick LS, Kaasgaard S, Oebro J, Larsen SE, Svendsen A, Johansen AH, Skjoet M (2013) Cleaning compositions comprising amylase variants reference to a sequence listing. France EP2540825A2
Jadhav DD, Patil HS, Chaya PS, Thulasiram HV (2016) Fungal mediated kinetic resolution of racemic acetates to (R)-alcohols using Fusarium proliferatum. Tetrahedron Lett 57:4563–4567. doi:10.1016/j.tetlet.2016.08.084
Jun H, Kieselbach T, Jönsson LJ (2011) Enzyme production by filamentous fungi: analysis of the secretome of Trichoderma reesei grown on unconventional carbon source. Microbial Cell Fact 10:68. doi:10.1186/1475-2859-10-68
Kasprowicz MJ, Gorczyca A, Frandsen RJ (2013) The effect of nanosilver on pigments production by Fusarium culmorum (W.G.Sm) Sacc. Pol J Microbiol 62:365–372
Keller NP, Turner G, Bennett J (2005) Fungal secondary metabolism-from biochemistry to genomics. Nat Rev Microbiol 3:937–947. doi:10.1038/nrmicro1286
Kimura Y, Takashi H, Nakajima H (1981) Isolation, identification and biological activities of 8-O-methyl-javanicin produced by Fusarium solani. Agric Biol Chem 45:2653–2654. doi:10.1080/00021369.1981.10864943
Kirk O, Borchert TV, Fuglsang CC (2002) Industrial enzyme applications. Curr Opin Biotechnol 13:345–351. doi:10.1016/s0958-1669(02)00328-2
Koda R, Numata T, Hama S, Tamalampudi S, Nakashima K, Tanaka T, Ogino C, Fukuda H, Kondo A (2010) Ethanolysis of rapeseed oil to produce biodiesel fuel catalyzed by Fusarium heterosporum lipase-expressing fungus immobilized. J Mol Catal B Enzym 66:101–104. doi:10.1016/j.molcatb.2010.04.001
Krings U, Berger RG (1998) Biotechnological production of flavours and fragrances. Appl Microbiol Biotechnol 49:1–8. doi:10.1007/s002530051129
Kundu A, Saha S, Walia S, Dutta TK (2016) Anti-nemic secondary metabolites produced by Fusarium oxysporum f.sp.ciceris. J Asia Pac Entomol 19:631–636. doi:10.1016/j.aspen.2016.06.003
Kurobane I, Zaita N, Fukuda A (1986) New metabolites of Fusarium martii related to dihydrofusarubin. J Antibiot 39:205–214. doi:10.7164/antibiotics.39.205
Lale GJ, Gadre RV (2016) Production of bikaverin by a Fusarium fujikuroi mutant in submerged cultures. AMB Expr 6:34. doi:10.1186/s13568-016-0205-0
Lant NJ, Erlandsen L, Hansen CV, Vind J, Svendsen A, Sonksen CP (2013) Compositions and methods for surface treatment with lipases. France WO 2013116261A2
Lazzaro I, Busman M, Battilani P, Butchko RAE (2012) FUM and BIK gene expression contribute to describe fumonisin and bikaverin synthesis in Fusarium verticiloides. Int J Food Microbiol 160:94–98. doi:10.1016/j.ijfoodmicro.2012.10.004
Lennartsson PR, Erlandsson P, Taherzadeh MJ (2014) Integration of the first and second generation bioethanol processes and the importance of by-products. Bioresour Technol 165:3–8. doi:10.1016/j.biortech.2014.01.127
Leslie JF, Summerell BA (2006) The fusarium laboratory manual. Blackwell, London
Lopes FC, Tichota DM, Pereira JQ, Segalin J, Rios AO, Brandelli A (2013) Pigment production by filamentous fungi on agro-industrial byproducts: an eco-friendly alternative. Appl Biochem Biotechnol 171:616–625. doi:10.1007/s12010-013-0392-y
Maheshwari RK, Singh AK, Gaddipati J, Srimal RC (2006) Multiple biological activities of curcumin: a short review. Life Sci 78:2081–2087. doi:10.1016/j.lfs.2005.12.007
Maitan-Alfenas GP, Visser EM, Guimarães VM (2015) Enzymatic hydrolysis of lignocellulosic biomass: converting food waste in valuable products. Curr Opin Food Sci 1:44–49. doi:10.1016/j.cofs.2014.10.001
Mäkelä MR, Donofrio N, de Vries RP (2014) Plant biomass degradation by fungi. Fungal Genet Biol 72:2–9. doi:10.1016/j.fgb.2014.08.010
Manganyi MC, Regnier T, Olivier EI (2015) Antimicrobial activities of selected essential oils against Fusarium oxysporum isolates and their biofilms. S Afr J Bot 99:115–121. doi:10.1016/j.sajb.2015.03.192
Mapari SAS, Nielsen KF, Larsen TO, Frisvad JC, Meyer AS, Thrane U (2005) Exploring fungal biodiversity for the production of water-soluble pigments as potential natural food colorants. Curr Opin Biotechnol 16:231–238. doi:10.1016/j.copbio.2005.03.004
Mapari SAS, Thrane U, Meyer AS (2010) Fungal polyketide azaphilone pigments as future nature food colorants? Trends Biotechnol 28:300–307. doi:10.1016/j.tibtech.2010.03.004
Maróstica MR, Pastore GM (2007) Production of R-(+)-α-terpineol by the biotransformation of limonene from orange essential oil, using cassava waste water as medium. Food Chem 101:345–350. doi:10.1016/j.foodchem.2005.12.056
Martins N, Roriz CL, Morales P, Barros L, Ferreira ICFR (2016) Food colorants: challenges, opportunities and current desires of agro-industries to ensure consumer expectation and regulatory practices. Trends Food Sci Tech 52:1–15. doi:10.1016/j.tifs.2016.03.009
Medentsev AG, Arinbasarova AY, Akimenko VK (2005) Biosynthesis of naphtoquinone pigments by fungi of the genus Fusarium. Appl Biochem Microbiol 41:503–507. doi:10.1007/s10438-005-0091-8
Menon V, Rao M (2012) Trends in bioconversion of lignocellulose: biofuels, platform chemicals & biorefinery concept. Progr Energ Combust Sci 38:522–550. doi:10.1016/j.pecs.2012.02.002
Misiek M, Hoffmeister D (2007) Fungal genetics, genomics, and secondary metabolites in pharmaceutical sciences. Planta Med 73:103–115. doi:10.1016/j.fgb.2010.04.004
Molina G, Abrahão MRE, Pessôa MG, Bution ML, Paulino BN, Néri-Numa IA, Pastore GM (2016) Industrial additives obtained through microbial biotechnology: bioflavors and biocolorants. In: Gupta VK, Sharma GD, Tuohy MG, Gaur R (eds) The handbook of microbial bioresources, 1ed. CABI Publishing, Boston, pp 549–566. doi:10.1079/9781780645216.0549
Molina G, Bution ML, Bicas JL, Dolder MAH, Pastore GM (2015) Comparative study of the bioconversion process using R-(+)- and S-(-)-limonene as substrates for Fusarium oxysporum 152B. Food Chem 174:606–613. doi:10.1016/j.foodchem.2014.11.059
Molina G, Pessôa MG, Pimentel MR, Pelissari FM, Bicas JL, Pastore GM (2014) Production of natural flavor compounds using monoterpenes as substrates. In: Hu J (ed) New developments in terpene research, 1ed. Nova Publishers, New York, pp 1–24
Müller M, Dirlam K, Wenk HH, Berger RG, Krings U, Kaspera R (2005) Method for the production of flavor-active terpenes. Germany WO 2005078110:A1
Nagia FA, EL-Mohamedy RSR (2007) Dyeing of wool with natural anthraquinone dyes from Fusarium oxysporum. Dyes Pigments 75:550–555. doi:10.1016/j.dyepig.2006.07.002
Nelson PE, Desjardins AE, Plattner RD (1993) Fumonisins, mycotoxins produced by Fusarium species: biology, chemistry, and significance. Annu Rev Phytopathol 31:233–252. doi:10.1146/annurev.py.31.090193.001313
Néri-Numa IA, Paulino BN, Pessôa MG, Abrahão MRE, Bution ML, Molina G, Pastore GM (2016) Industrial additives obtained through microbial biotechnology: biosurfactants and prebiotic carbohydrates. In: Gupta VK, Sharma GD, Tuohy MG, Gaur R (eds) The handbook of microbial bioresources, 1ed. CABI Publishing, Boston, pp 528–548. doi:10.1079/9781780645216.0528
Nielsen RI, Aaslyng DA, Jensen GW, Schneider P (1994) Endoprotease from Fusarium oxysporum DSM 2672 for use in detergents. USA US5288627A
Nigam PS, Singh A (2011) Production of liquid biofuels from renewable resources. Progr Energy Combust Sci 37:52–68. doi:10.1016/j.pecs.2010.01.003
Nirmaladevi D, Venkataramana M, Chandranayaka S, Ramesha A, Jameel NM, Srinivas C (2014) Neuroprotective effects of bikaverin on H2O2-induced oxidative stress mediated neuronal damage in SH-SY5Y cell line. Cell Mol Neurobiol 34:973–985. doi:10.1007/s10571-014-0073-6
Olajuyigbe FM, Nlekerem CM, Ogunyewo OA (2016) Production and characterization of highly thermostable β-glucosidase during the biodegradation of methyl cellulose by Fusarium oxysporum. Biochem Res Int 2016:1–8. doi:10.1155/2016/3978124
Oliveira BH, Coradi GV, Attili-Angelis D, Scauri C, Luques AHPG, Barbosa AM, Dekker RFH, Neto PO, Lima VMG (2013) Comparison of lipase production on crambe oil and meal by Fusarium sp. (Gibberella fujikuroi complex). Eur J Lipid Sci Technol 115:1413–1425. doi:10.1002/ejlt.201300087
Panagiotou G, Christakopoulos P, Olsson L (2005) Simultaneous saccharification and fermentation of cellulose by Fusarium oxysporum F3-growth characteristics and metabolite profiling. Enzym Microb Technol 36:693–699. doi:10.1016/j.enzmictec.2004.12.029
Panagiotou G, Kekos D, Macris BJ, Christakopoulos P (2003) Production of cellulolytic and xylanolytic enzymes by Fusarium oxysporum grown on corn stover in solid state fermentation. Ind Crops Prod18:37–45 doi: 10.1016/S0926-6690(03)00018-9
Panagiotou G, Topakas E, Moukouli M, Christakopoulos P, Olsson L (2011) Studying the ability of Fusarium oxysporum and recombinant Saccharomyces cerevisiae to efficiently cooperate in decomposition and ethanolic fermentation of wheat straw. Biomass Bioenergy 35:3727–3732. doi:10.1016/j.biombioe.2011.05.005
Parisot D, Devys M, Barbier M (1990) Naphthoquinone pigments related to fusarubin from the fungus Fusarium solani ( Mart.) Sacc. Microbios 64:31–47
Paulova L, Patakova P, Branska B, Rychtera M, Melzoch K (2015) Lignocellulosic ethanol: technology design and its impact on process efficiency. Biotechnol Adv 33:1091–1107. doi:10.1016/j.biotechadv.2014.12.002
Petrova A, Dar’in D, Ivanov A, Moskin L, Ishimatsu R, Nakano K, Imato T, Bulatov A (2016) Determination of curcumin in biologically active supplements and food spices using a mesofluidic plataform with fluorescence detection. Talanta 159:300–306. doi:10.1016/j.talanta.2016.06.046
Phelps DC, Nemee S, Baker R, Mansell R (1990) Immunoassay for naphthazarin phytoxins produced by Fusarium solani. Phytopathology 80:298–302. doi:10.1094/phyto-80-298
Pollet A, Beliën T, Fierens K, Delcour JA, Courtin CM (2009) Fusarium graminearum xylanases show different functional stabilities, substrate specificities and inhibition sensitivities. Enzym Microb Technol 44:189–195. doi:10.1016/j.enzmictec.2008.12.005
Pradeep FS, Palaniswamy M, Ravi S, Thangamani A, Pradeep BV (2015) Larvicidal activity of a novel isoquinoline type pigment from Fusarium moniliforme KUMBF1201 against Aedes aegypti and Anopheles stephensi. Process Biochem 50:1479–1486. doi:10.1016/j.procbio.2015.05.022
Pradeep FS, Pradeep BV (2013) Optimization of pigment and biomass production from Fusarium moniliforme under submerged fermentation conditions. Int J Pharm Pharm Sci 5:526–535
Pradeep FS, Shakilabegan M, Palaniswamy M, Pradeep BV (2013) Influence of culture media on growth and pigment production by Fusarium moniliforme KUMBF1201 isolated from paddy field soil. World Appl Sci J 22:70–77
Prakash S, Singh G, Soni N, Sharma S (2010) Pathogenicity of Fusarium oxysporum against the larvae of Culex quinquefasciatus (Say) and Anopheles stephensi (Liston) in laboratory. Parasitol Res 107:651–655. doi:10.1007/s00436-010-1911-1
Prazeres JN (2006) Produção e caracterização da lipase alcalina de Fusarium oxysporum. State University of Campinas, Dissertation
Prazeres JN, Cruz JAB, Pastore GM (2006) Characterization of alkaline lipase from Fusarium oxysporum and the effect of different surfactants and detergents on the enzyme activity. Braz J Microbiol 37:505–509. doi:10.1590/S1517-83822006000400019
Quadros CP, Duarte MCT, Pastore GM (2011) Biological activities of a mixture of biosurfactants from Bacillus subtilis and alkaline lipase from Fusarium oxysporum. Braz J Microbiol 42:354–361. doi:10.1590/s1517-83822011000100045
Rodriguez-Amaya DB (2016) Natural food pigments and colorants. Curr Opin Food Sci 7:20–26. doi:10.1016/j.cofs.2015.08.004
Sagaram US, Kolomiets M, Shim W (2006) Regulation of fumonisin biosynthesis in Fusarium verticilloides-maize system. Plant Pathol J 22:203–210. doi:10.5423/ppj.2006.22.3.203
Sancho RAS, Pastore GM (2012) Evaluation of the effects of anthocyanins in type 2 diabetes. Food Res Int 46:378–386. doi:10.1016/j.foodres.2011.11.021
Sarris J, Latrasse A (1985) Production of odoriferous gamma lactones by Fusarium poae. Agric Biol Chem 49:3227–3230. doi:10.1271/bbb1961.49.3227
Sasanya JJ, Hall C, Wolf-Hall C (2008) Analysis of deoxynivalenol, masked deoxynivalenol, and Fusarium graminearum pigment in wheat samples, using liquid chromatography–UV–mass spectrometry. J Food Protect 71:1205–1213. doi:10.4315/0362-028x-71.6.1205
Shiono Y, Ariefa NR, Anwar C, Matsjeh S, Sappapan R, Murayama T, Koseki T, Kawamura T, Uesugi S, Kimura KI (2016) New metabolites produced by Fusarium solani T-13 isolated from a dead branch. Phytochem Lett 17:232–237. doi:10.1016/j.phytol.2016.08.003
Siddiqui KS (2015) Some like it hot, some like it cold: temperature dependent biotechnological applications and improvements in extremophilic enzymes. Biotechnol Adv 33:1912–1922. doi:10.1016/j.biotechadv.2015.11.001
Singh R, Kumar M, Mittal A, Mehta PK (2016) Microbial enzymes: industrial progress in 21st century. 3. Biotech 6:174. doi:10.1007/s13205-016-0485-8
Son SW, Kim HY, Choi GJ, Lim HK, Jang KS, Lee SO, Lee S, Sung ND, Kim JC (2008) Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against Phytophthora infestans. J Appl Microbiol 104:692–698. doi:10.1111/j.1365-2672.2007.03581.x
Sondergaard TE, Klitgaard LG, Purup S, Kobayashi H, Giese H, Sørensen JL (2012) Estrogenic effects of fusarielins in human breast cancer cell lines. Toxicol Lett 214:259–262. doi:10.1016/j.toxlet.2012.09.004
Soni H, Rawat HK, Ahirwar S, Kango N (2016) Screening, statistical optimized production and application of β-mannanase from some newly isolated fungi. Eng Life Sci doi. doi:10.1002/elsc.201600136
Sørensen JL, Sondergaard TE (2014) The effects of different yeast extracts on secondary metabolite production in Fusarium. Int J Food Microbiol 170:55–60. doi:10.1016/j.ijfoodmicro.2013.10.024
Souza PNC, Grigoletto TLB, Moraes LAB, Abreu LM, Guimarães LHS, Santos C, Glavão LR, Cardoso PG (2016) Production and chemical characterization of pigments in filamentous fungi. Microbiology 162:12–22. doi:10.1099/mic.0.000168
Stamatis H, Christakopoulos P, Kekos D, Macris BJ, Kolisis FN (1998) Studies on the synthesis of short-chain geranyl esters catalysed by Fusarium oxysporum esterase in organic solvents. J Mol Catal - B Enzym 4:229–236. doi:10.1016/S1381-1177(98)00003-4
Studt L, Wiemann P, Kleigrewe K, Humpf HU, Tudzynski B (2012) Biosynthesis of fusarubins accounts for pigmentation of Fusarium fujikuroi perithecia. Appl Environm Microbiol 78:4468–4480. doi:10.1128/aem.00823-12
Suresh PV, Sakhare PZ, Sachindra NM, Halami PM (2014) Extracellular chitin deacetylase production in solid state fermentation by native soil isolates of Penicillium monoverticillium and Fusarium oxysporum. J Food Sci Technol 51(8):1594–1599. doi:10.1007/s13197-012-0676-1
Takemoto K, Kamisuki S, Chia PT, Kuriyama I, Mizushina Y, Sugawara F (2014) Bioactive dihydronaphthoquinone derivatives from Fusarium solani. J Nat Prod 77:1992–1996. doi:10.1021/np500175j
Tatum JH, Baker RA, Berry RE (1985) Naphthoquinones produced by Fusarium oxysporum isolated from citrus. Phytochemistry 24:457–459. doi:10.1016/s0031-9422(00)80746-3
Tatum JH, Baker RA, Berry RE (1987) Naphthoquinones and derivatives from Fusarium. Phytochemistry 26:795–798. doi:10.1016/s0031-9422(00)84789-5
Tatum JH, Baker RA, Berry RE (1989) Metabolites of Fusarium solani. Phytochemistry 28:283–284. doi:10.1016/0031-9422(89)85062-9
Thadathil N, Kuttappan AKP, Vallabaipatel E, Kandasamy M, Velappan SP (2014) Statistical optimization of solid state fermentation conditions for the enhanced production of thermoactive chitinases by mesophilic soil fungi using response surface methodology and their application in the reclamation of shrimp processing by-products. Ann Microbiol 64:671–681. doi:10.1007/s13213-013-0702-1
Thrane U, Adler A, Clasen PE, Galvano F, Langseth W, Lew H, Logrieco A, Nielsen KF, Ritieni A (2004) Diversity in metabolite production by Fusarium langsethiae, Fusarium poae, and Fusarium sporotrichioides. Int J Fodd Microbiol 95:257–266. doi:10.1016/j.ijfoodmicro.2003.12.005
Trisuwan K, Khamthong N, Rukachaisirikul V, Phongpaichit S, Preedanon S, Sakayaroj J (2010) Antraquinone, cyclopentanone, and naphthoquinne derivatives from the sea fan-derived fungi Fusarium spp. PSU-F14 and PSU-F1135. J Nat Prod 73:1507–1511. doi:10.1021/np100282k
Trisuwan K, Rukachaisirikul V, Borwornwiriyapanc K, Phongpaichit S, Sakayaroj J (2013) Pyrone derivatives from the soil fungus Fusarium solani PSU-RSPG37. Phytochem Lett 6:495–497. doi:10.1016/j.phytol.2013.06.008
Tuli HS, Chaudhary P, Beniwal V, Sharma AK (2015) Microbial pigments as natural color sources: current trends and future perspectives. J Food Sci Technol 52:4669–4678. doi:10.1007/s13197-014-1601-6
van der Schaft PH, Burg N ter, van den Bosch S, Cohen AM (1992) Fed-batch production of 2-heptanone by Fusarium poae. Appl Microbiol Biotechnol 36:709–711 doi: 10.1007/bf00172179
Vandamme EJ (2003) Bioflavours and fragrances via fungi and their enzymes. Fungal Divers 13:153–166
Velmurugan P, Kamala-Kannan S, Balachandar V, Lakshmanaperumalsamy P, Chae JC, Oh BT (2010) Natural pigment extraction from five filamentous fungi for industrial applications and dyeing of leather. Carbohydr Polym 79:261–268. doi:10.1016/j.carbpol.2009.07.058
Venil CK, Zakaria ZA, Ahmad WA (2013) Bacterial pigments and their applications. Process Biochem 48:1065–1079. doi:10.1016/j.procbio.2013.06.006
Venugopalan A, Potunuru UR, Dixit M, Srivastava S (2016) Reprint of: effect of fermentation parameters, elicitors and precursors on camptothecin production from the endophyte Fusarium solani. Bioresour Tecnol 213:311–318. doi:10.1016/j.biortech.2016.05.023
Venugopalan A, Srivastava S (2015) Enhanced camptothecin production by ethanol addition in the suspension culture of the endophyte, Fusarium solani. Bioresour Technol 188:251–257. doi:10.1016/j.biortech.2014.12.106
Vohra M, Manwar J, Manmode R, Padgilwar S, Patil S (2014) Bioethanol production: feedstock and current technologies. J Environ Chem Eng 2:573–584. doi:10.1016/j.jece.2013.10.013
Waśkiewicz A, Stępień L (2012) Mycotoxins biosynthesized by plant-derived Fusarium isolates. Arh Hig Rada Toksikol 63:437–446. doi:10.2478/10004-1254-63-2012-2230
Wiemann P, Willmann A, Straeten M, Kleigrewe K, Beyer M, Humpf HU, Tudzynski B (2009) Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi: genes, their function and regulation. Mol Microbiol 72:931–946. doi:10.1111/j.1365-2958.2009.06695.x
Wu Y, Nian D (2014) Production optimization and molecular structure characterization of a newly isolated novel laccase from Fusarium solani MAS2, an anthracene-degrading fungus. Int Biodeterior Biodegrad 86:382–389. doi:10.1016/j.ibiod.2013.10.015
Xiros C, Christakopoulos P (2009) Enhanced ethanol production from brewer’s spent grain by a Fusarium oxysporum consolidated system. Biotechnol Biofuels 2009:2–4. doi:10.1186/1754-6834-2-4
Xiros C, Katapodis P, Christakopoulos P (2009) Evaluation of Fusarium oxysporum cellulolytic system for an efficient hydrolysis of hydrothermally treated wheat straw. Bioresour Technol 100:5362–5365. doi:10.1016/j.biortech.2009.05.065
Xiros C, Katapodis P, Christakopoulos P (2011) Factors affecting cellulose and hemicellulose hydrolysis of alkali treated brewers spent grain by Fusarium oxysporum enzyme extract. Bioresour Technol 102:1688–1696. doi:10.1016/j.biortech.2010.09.108
Xiros C, Topakas E, Katapodis P, Christakopoulos P (2008) Evaluation of Fusarium oxysporum as an enzyme factory for the hydrolysis of brewer’s spent grain with improved biodegradability for ethanol production. Ind Crop Prod 28:213–224. doi:10.1016/j.indcrop.2008.02.004
Xu J, Wang X, Hu L, Xia J, Wu Z, Xu N, Dai B, Wu B (2015) A novel ionic liquid-tolerant Fusarium oxysporum BN secreting ionic liquid-stable cellulase: consolidated bioprocessing of pretreated lignocellulose containing residual ionic liquid. Bioresour Technol 181:18–25. doi:10.1016/j.biortech.2014.12.080
Yang SX, Gao JM, Laatsch H, Tian JM, Pescitelli G (2012a) Absolute configuration of fusarone, a new azaphilone from the endophytic fungs Fusarium sp. isolated from Melia azedarach, and of related azaphilones. Chirality 24:621–627. doi:10.1002/chir.22044
Yang SX, Gao JM, Zhang Q, Laatsch H (2011) Toxic polyketides produced by Fusarium sp., an endophytic fungus isolated from Melia azedarach. Bioorg Med Chem Lett 21:1887–1889. doi:10.1016/j.bmcl.2010.12.043
Yang SX, Wang HP, Gao JM, Zhang Q, Laatsch H, Kuang Y (2012b) Fusaroside, a unique glycolipid from Fusarium sp., an endophytic fungus isolated from Melia azedarach. Org Biomol Chem 10:819–824. doi:10.1039/c1ob06426f
Yang X, Choi HS, Park C, Kim SW (2015) Current states and prospects of organic waste utilization for biorefineries. Renew Sust Energ Rev 49:335–349. doi:10.1016/j.rser.2015.04.114
Yusuf F, Chaubey A, Jamwal U, Parshad R (2013) A new isolate from Fusarium proliferatum (AUF-2) for efficient nitrilase production. Appl Biochem Biotechnol 171:1022–1031. doi:10.1007/s12010-013-0416-7
Zabed H, Sahu JN, Boyce AN, Faruq G (2016) Fuel ethanol production from lignocellulosic biomass: an overview on feedstocks and technological approaches. Renew Sust Energ Rev 66:751–774. doi:10.1016/j.rser.2016.08.038
Zaher AM, Makboul MA, Moharram AM, Tekwani BL, Calderón AI (2015) A new enniatin antibiotic from the endophyte Fusarium tricinctum Corda. J Antibiot 68:197–200. doi:10.1038/ja.2014.129
Zhong JJ, Xiao JH (2009) Secondary metabolites from higher fungi: discovery, bioactivity, and bioproduction. Adv Biochem Eng Biotechnol 113:79–150. doi:10.1007/10_2008_26
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The authors acknowledge the funding agencies Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP—process number 2013/18390-0), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—process number 460897/2014-4), Fundação de Amparo a Pesquisa do Estado de Minas Gerais and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes).
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Pessôa, M.G., Paulino, B.N., Mano, M.C.R. et al. Fusarium species—a promising tool box for industrial biotechnology. Appl Microbiol Biotechnol 101, 3493–3511 (2017). https://doi.org/10.1007/s00253-017-8255-z
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DOI: https://doi.org/10.1007/s00253-017-8255-z