Abstract
Cheese whey (CW), the liquid resulting from the precipitation and removal of milk casein during cheese-making, and the second cheese whey (SCW) derived from the production of cottage and ricotta cheeses are the main byproducts of dairy industry. The major constituent of CW and SCW is lactose, contributing to the high BOD and COD content. Because of this, CW and SCW are high-polluting agents and their disposal is still a problem for the dairy sector. CW and SCW, however, also consist of lipids, proteins, and minerals, making them useful for production of various compounds. In this paper, microbial processes useful to promote the bioremediation of CW and SCW are discussed, and an overview on the main whey-derived products is provided. Special focus was paid to the production of health-promoting whey drinks, vinegar, and biopolymers, which may be exploited as value-added products in different segments of food and pharmaceutical industries.
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AbdulAlim TS, Zayan AF, Campelo PH, Bakry AM (2019) Development of new functional fermented product: mulberry-whey beverage. J Nutr Food Res Technol 1:64–69. https://doi.org/10.30881/jnfrt.00013
Ahmadi N, Khosravi-Darani K, Mortazavian AM (2017) An overview of biotechnological production of propionic acid: from upstream to downstream processes. Electronic. J Biotechnol 28:67–75. https://doi.org/10.1016/j.ejbt.2017.04.004
Almeida KE, Tamime AY, Oliveira MN (2009) Influence of total solids contents of milk whey on the acidifying profile and viability of various lactic acid bacteria. LWT - Food Sci Technol 42:672–678. https://doi.org/10.1016/j.lwt.2008.03.013
Amaro TMMM, Rosa D, Comi G, Iacumin L (2019) Prospects for the use of whey for polyhydroxyalcanoate (PHA) production. Front Microbiol 10:992. https://doi.org/10.3389/fmicb.2019.00992
Anjum A, Zuber M, Zia KM, Noreen A, Anjum MN, Tabasum S (2016) Microbial production of polyhydroxyalkanoates (PHAs) and its copolymers: a review of recent advancements. Int J Biol Macromol 89:161–174. https://doi.org/10.1016/j.ijbiomac.2016.04.069
Becerra M, Cerdán ME, González-Siso MI (2015) Biobutanol from cheese whey. Microb Cell Factories 14:27–41. https://doi.org/10.1186/s12934-015-0200-1
Bekatorou A, Plioni I, Sparou K, Maroutsiou R, Tsafrakidou P, Petsi T, Kordouli E (2019) Bacterial cellulose production using the corinthian currant finishing side-stream and cheese whey: process optimization and textural characterization. Foods 4:8. E193. https://doi.org/10.3390/foods8060193
Bertrand N, Fliss I, Lacroix C (2001) High nisin-Z production during repeated-cycle batch cultures in supplemented whey permeate using immobilized Lactococcus lactis UL719. Int Dairy J 11:953–960. https://doi.org/10.1016/S0958-6946(01)00129-7
Brady D, Nigam P, Marchant R, McHale AP (1997) Ethanol production at 45°C by alginate-immobilized Kluyveromyces marxianus IMB3 during growth on lactose-containing media. Bioprocess Eng 16:103–104. https://doi.org/10.1007/s004490050295
Bugnicourt E, Cinelli P, Lazzeri A, Alvarez V (2014) Polyhydroxyalkanoate (PHA): review of synthesis, characteristics, processing and potential applications in packaging. Express Polym Lett 8:791–808. https://doi.org/10.3144/expresspolymlett.2014.82
Bulatović ML, Krunić T, Vukašinović-Sekulić MS, Zarić DB, Rakin MB (2014) Quality attributes of a fermented whey-based beverage enriched with milk and a probiotic strain. RSC Adv 4:55503–55510. https://doi.org/10.1039/C4RA08905G
Cardoso T, Marques C, Dagostin JLA, Masson ML (2019) Lactobionic acid as a potential food ingredient: recent studies and applications. J Food Sci 84:1672–1681. https://doi.org/10.1111/1750-3841.14686
Carvalho F, Prazeres AR, Rivas J (2013) Cheese whey wastewater: characterization and treatment. Sci Total Environ 445–446:385–396. https://doi.org/10.1016/j.scitotenv.2012.12.038
Castro WF, Cruz AG, Bisinotto MS, Guerreiro LMR, Faria JAF, Bolini HMA, Cunha RL, Deliza R (2013a) Development of probiotic dairy beverages: rheological properties and application of mathematical models in sensory evaluation. J Dairy Sci 96:16–25. https://doi.org/10.3168/jds.2012-5590
Castro WF, Cruz AG, Rodrigues D, Ghiselli G, Oliveira CAF, Faria JAF, Godoy HT (2013b) Short communication: effects of different whey concentrations on physicochemical characteristics and viable counts of starter bacteria in dairy beverage supplemented with probiotics. J Dairy Sci 96:96–100. https://doi.org/10.3168/jds.2012-5576
Chatzipaschali AA, Stamatis AG (2012) Biotechnological utilization with a focus on anaerobic treatment of cheese whey: current status and prospects. Energies 5:3492–3525. https://doi.org/10.3390/en5093492
Chavan RS, Shradda R, Kumar A, Nalawade T (2015) Whey based beverage: its functionality, formulations, health benefits and applications. J Food Process Technol 6:10. https://doi.org/10.4172/2157-7110.1000495
Chawla PR, Bajaj IB, Survase S, Singhal RS (2009) Microbial cellulose: fermentative production and applications. Food Technol Biotechnol 47:107–124
Christensen AD, Kádár Z, Oleskowicz-Popiel P, Thomsen MH (2011) Production of bioethanol from organic whey using Kluyveromyces marxianus. J Ind Microbiol Biotechnol 38:283–289. https://doi.org/10.1007/s10295-010-0771-0
Chwialkowska J, Duber A, Zagrodnik R, Walkiewicz F, Łężyk M, Oleskowicz-Popiel P (2019) Caproic acid production from acid whey via open culture fermentation – Evaluation of the role of electron donors and downstream processing. Biores Technol 279:74-83. https://doi.org/10.1016/j.biortech.2019.01.086
Coenen TMM, Bertens AMC, De Hoog SCM, Verspeek-Rip CM (2000) Safety evaluation of a lactase enzyme preparation derived from Kluyveromyces lactis. Food Chem Toxicol 38:671–677. https://doi.org/10.1016/S0278-6915(00)00053-3
Colombo B, Sciarria TP, Reis M, Scaglia B, Adani F (2016) Polyhydroxyalkanoates (PHAs) production from fermented cheese whey by using a mixed microbial culture. Bioresour Technol 218:692–699. https://doi.org/10.1016/j.biortech.2016.07.024
da Silva AN, Perez R, Minim VPR, Martins DDSA, Minim LA (2015) Integrated production of whey protein concentrate and lactose derivatives: what is the best combination? Food Res Int 73:62–74. https://doi.org/10.1016/j.foodres.2015.03.009
da Silveira EOD, Lopes Neto JH, da Silva LA, AES R, Magnani M, Cardarelli HR (2015) The effects of inulin combined with oligofructose and goat cheese whey on the physicochemical properties and sensory acceptance of a probiotic chocolate goat dairy beverage. LWT - Food Sci Technol 62:445–451. https://doi.org/10.1016/j.lwt.2014.09.056
Das B, Sarkar S, Maiti S, Bhattacharjee S (2016) Studies on production of ethanol from cheese whey using Kluyveromyces marxianus. In: Materials Today: Proceedings. Elsevier Ltd, pp 3253–3257
de Castro FP, Cunha TM, Ogliari PJ, Teófilo RF, Ferreira MMC, Prudêncio ES (2009) Influence of different content of cheese whey and oligofructose on the properties of fermented lactic beverages: study using response surface methodology. LWT - Food Sci Technol 42:993–997. https://doi.org/10.1016/j.lwt.2008.12.010
Domingues L, Guimarães PMR, Oliveira C (2010) Metabolic engineering of Saccharomyces cerevisiae for lactose/whey fermentation. Bioeng Bugs 1:164–171. https://doi.org/10.4161/bbug.1.3.10619
Donot F, Fontana A, Baccou JC, Schorr-Galindo S (2012) Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohydr Polym 87:951–962. https://doi.org/10.1016/j.carbpol.2011.08.083
Enan G, Aziz A, Amri A (2006) Novel plantaricin UG1 production by Lactobacillus plantarum UG1 in enriched whey permeate in batch fermentation processes. J Food Agric Environ 4:85–88
European Commission (2013) Analysis of the public consultation on the green paper “European strategy on plastic waste in the environment”. EU DG ENV
Faisal S, Chakraborty S, Devi WE, Hazarika MK, Puranik V (2017) Sensory evaluation of probiotic whey beverages formulated from orange powder and flavor using fuzzy logic. Int Food Res J 24:703–710
Fernández-Gutiérrez D, Veillette M, Giroir-Fendler A, Avalos Ramirez A, Faucheux N, Heitz M (2017) Biovalorization of saccharides derived from industrial wastes such as whey: a review. Rev Environ Sci Biotechnol 16:147–174. https://doi.org/10.1007/s11157-016-9417-7
Ferreira PG, da Silveira FA, dos Santos RCV, Genier HLA, Diniz RHS, Ribeiro JI, Fietto LG, Passos FML, da Silveira WB (2015) Optimizing ethanol production by thermotolerant Kluyveromyces marxianus CCT 7735 in a mixture of sugarcane bagasse and ricotta whey. Food Sci Biotechnol 24:1421–1427. https://doi.org/10.1007/s10068-015-0182-0
Fonseca GG, Heinzle E, Wittmann C, Gombert AK (2008) The yeast Kluyveromyces marxianus and its biotechnological potential. Appl Microbiol Biotechnol 79:339–354. https://doi.org/10.1007/s00253-008-1458-6
Food and Drug Administration (2017) FDA/ORA Compliance Policy Guides Sec. 525.825 Vinegar, Definitions - Adulteration with Vinegar Eels (CPG 7109.22)
Furrer P, Panke S, Zinn M (2007) Efficient recovery of low endotoxin medium-chain-length poly ([R]-3-hydroxyalkanoate) from bacterial biomass. J Microbiol Meth 69:206–213. https://doi.org/10.1016/j.mimet.2007.01.002
Gabardo S, Rech R, Rosa CA, Ayub MAÔZ (2014) Dynamics of ethanol production from whey and whey permeate byimmobilized strains of Kluyveromyces marxianus in batch andcontinuous bioreactors. Renew Energy 69:89–96. https://doi.org/10.1016/j.renene.2014.03.023
Gallardo-Escamilla FJ, Kelly AL, Delahunty CM (2007) Mouthfeel and flavour of fermented whey with added hydrocolloids. Int Dairy J 17:308–315. https://doi.org/10.1016/j.idairyj.2006.04.009
Guerra NP, Rus ML, Pastrana L (2001) Nutritional factors affecting the production of two bacteriocins from lactic acid bacteria on whey. Int J Food Microbiol 70:267–281. https://doi.org/10.1016/S0168-1605(01)00551-7
Guimarães PMR, Teixeira JA, Domingues L (2010) Fermentation of lactose to bio-ethanol by yeasts as part of integrated solutions for the valorisation of cheese whey. Biotechnol Adv 28:375–384. https://doi.org/10.1016/j.biotechadv.2010.02.002
Gullo M, Verzelloni E, Canonico M (2014) Aerobic submerged fermentation by acetic acid bacteria for vinegar production: process and biotechnological aspects. Process Biochem 49:1571–1579. https://doi.org/10.1016/j.procbio.2014.07.003
Gullo M, Sola A, Zanichelli G, Montorsi M, Messori M, Giudici P (2017) Increased production of bacterial cellulose as starting point for scaled-up applications. Appl Microbiol Biotechnol 101:8115–8127. https://doi.org/10.1007/s00253-017-8539-3
Gullo M, La China S, Falcone PM, Giudici P (2018) Biotechnological production of cellulose by acetic acid bacteria: current state and perspectives. Appl Microbiol Biotech 102:6885–6898. https://doi.org/10.1007/s00253-018-9164-5
Gullo M, La China S, Petroni G, Di Gregorio S, Giudici P (2019) Exploring K2G30 genome: a high bacterial cellulose producing strain in glucose and mannitol based media. Front Microbiol 10:6885–6898. https://doi.org/10.3389/fmicb.2019.00058
Gutierrez NA, Debarr AD, Maddox IS (1996) Production of diacetyl from whey permeate using Lactoccoccus lactis subsp. lactis. J Ferment Bioeng 81:183–184. https://doi.org/10.1007/s10295-009-0617-9
Hadiyanto, Ariyanti D, Aini AP, Pinundi DS (2014) Optimization of ethanol production from whey through fed-batch fermentation using Kluyveromyces marxianus. In: Energy Procedia. Elsevier Ltd, pp 108–112. doi: https://doi.org/10.1016/j.egypro.2014.01.203
Hassan AN, Nelson BK (2012) Invited review: anaerobic fermentation of dairy food wastewater. J Dairy Sci 95:756–774. https://doi.org/10.3168/jds.2012-5732
Hernandez-Mendoza A, Robles VJ, Angulo JO, De La Cruz J, Garcia HS (2007) Preparation of a whey-based probiotic product with Lactobacillus reuteri and Bifidobacterium bifidum. Food Technol Biotechnol 45:27–31
Hughes P, Risner D, Meunier Goddik L (2018) Whey to vodka chapter in whey - biological properties and alternative uses. In: Gigli (ed) . IntechOpen. https://doi.org/10.5772/intechopen.81679
Jakob F, Pfaff A, Novoa-Carballal R, Rübsam H, Becker T, Vogel RF (2013) Structural analysis of fructans produced by acetic acid bacteria reveals a relation to hydrocolloid function. Carbohydr Polym 92:1234–1242. https://doi.org/10.1016/j.carbpol.2012.10.054
Jipa IM, Stoica-Guzun A, Stroescu M (2012) Controlled release of sorbic acid from bacterial cellulose based mono and multilayer antimicrobial films. LWT-Food Sci Technol 47:400–406. https://doi.org/10.1016/j.lwt.2012.01.039
Joint FAO/WHO Food Standards Programme (1998) Conversion of European regional standard for vinegar into world-wide standard. Report No: FAO-ESN–CX/PFV-98/8. Codex committee on processed fruits and vegetables. Sess 19. Washington, DC, 16–18 March 1998. FAO, Rome
Jozala AF, Silva DP, Vincente AA, Teixeira JA, Pessoa AJ, Penna CV (2011) Processing of byproducts to improve nisin production by Lactococcus lactis. J Biotechnol 10:14920–14925. https://doi.org/10.5897/AJB11.979
Koller M (2014) Poly(hydroxyalkanoates) for food packaging: application and attempts towards implementation. Appl Food Biotechnol 1(1):1–13. https://doi.org/10.22037/afb.v1i1.7127
Koller M, Salerno A, Muhr A, Reiterer A, Braunegg G (2013) Polyhydroxyalkanoates: Biodegrad-able polymers and plastics from renewable resources. Mater Technol 47:5–12 eid: 2-s2.0-84875258409
Koller M, Maršálek L, de Sousa Dias MM, Braunegg G (2017) Producing microbial polyhydroxyalkanoate (PHA) biopolyesters in a sustainable manner. New Biotechnol 37:24–38. https://doi.org/10.1016/j.nbt.2016.05.001
Kourkoutas Y, Dimitropoulou S, Kanellaki M, Marchant R, Nigam P, Banat IM, Koutinas AA (2002) High-temperature alcoholic fermentation of whey using Kluyveromyces marxianus IMB3 yeast immobilized on delignified cellulosic material. Bioresour Technol 82:177–181. https://doi.org/10.1016/S0960-8524(01)00159-6
Koutinas AA, Athanasiadis I, Bekatorou A, Psarianos C, Kanellaki M, Agouridis N, Blekas G (2007) Kefir-yeast technology: industrial scale-up of alcoholic fermentation of whey, promoted by raisin extracts, using kefir-yeast granular biomass. Enzym Microb Technol 41:576–582. https://doi.org/10.1016/j.enzmictec.2007.05.013
Kumar RS (2015) Development, quality evaluation and shelf life studies of probiotic beverages using whey and Aloe vera juice. J Food Process Technol 6:9. https://doi.org/10.4172/2157-7110.1000486
Kuo CH, Lin PJ, Lee CK (2010) Enzymatic saccharification of dissolution pretreated waste cellulosic fabrics for bacterial cellulose production by Gluconacetobacter xylinus. J Chem Technol Biotechnol 85:1346–1352. https://doi.org/10.1002/jctb.2439
La China S, Zanichelli G, De Vero L, Gullo M (2018) Oxidative fermentations and exopolysaccharides production by acetic acid bacteria: a mini review. Biotechnol Lett 40:1289–1302. https://doi.org/10.1007/s10529-018-2591-7
La China S, Bezzecchi A, Moya F, Petroni G, Di Gregorio S, Gullo M (2020) Genome sequencing and phylogenetic analysis of K1G4: a new Komagataeibacter strain producing bacterial cellulose from different carbon sources. https://doi.org/10.1007/s10529-020-02811-6
Lappa IK, Papadaki A, Kachrimanidou V (2019) Cheese whey processing : integrated biorefinery. Foods 8:347. https://doi.org/10.3390/foods8080347
Lemoigne M (1927) Microbial autolysis and autolytic origin of β-hydroxybutyric acid. Ann Inst Pasteur 41:148–165
Liao C, Yousef AE, Richter ER, Chism GW (1993) Pediococcus acidilactici PO2 bacteriocin production in whey permeate and inhibition of Listeria monocytogenes in foods. J Food Sci 58:430–434. https://doi.org/10.1111/j.1365-2621/1993.tb042291.x
Liu X, Chung YK, Yang ST, Yousef AE (2005) Continuous nisin production in laboratory media and whey permeate by immobilized Lactococcus lactis. Process Biochem 40:13–24. https://doi.org/10.1016/j.procbio.2003.11.032
Liu L, Zhu Y, Li J, Wang M, Lee P, Du G, Chen J (2012) Microbial production of propionic acid from propionibacteria: current state, challenges and perspectives. Crit Rev Biotechnol 32:374–381. https://doi.org/10.3109/07388551.2011.651428
Longanesi L, Frascari D, Spagni C, DeWever H, Pinelli D (2018) Succinic acid production from cheese whey by biofilms of Actinobacillus succinogenes: packe d bed bioreactor tests. J Chem Technol Biotechnol 93:246–256. https://doi.org/10.1002/jctb.5347
Lule VK, Singh R, Pophaly S, Poonam, Tomar SK (2016) Production and structural characterisation of dextran from an indigenous strain of Leuconostoc mesenteroides BA08 in whey. Int J Dairy Technol 69:520–531. https://doi.org/10.1111/1471-0307.12271
Lustrato G, Salimei E, Alfano G, Belli C, Fantuz F, Grazia L, Ranalli G (2013) Cheese whey recycling in traditional dairy food chain: effects of vinegar from whey in dairy cow nutrition. Acetic Acid Bact 2:47. https://doi.org/10.4081/aab.2013.s1.e8
Macedo MG, Lacroix C, Gardner N, Champagne CP (2002) Effect of medium supplementation on exopolysaccharide production by Lactobacillus rhamnosus RW-9595M in a whey permeate. Int Dairy J 12:419–426. https://doi.org/10.1016/S0958-6946(01)00173-X
Magalhães KT, Pereira MA, Nicolau A, Dragone G, Domingues L, Teixeira JA, Batista De Almeida Silva J, Schwan RF (2010) Production of fermented cheese whey-based beverage using kefir grains as starter culture: evaluation of morphological and microbial variations. Bioresour Technol 101:8843–8850. https://doi.org/10.1016/j.biortech.2010.06.083
Mauriello G, Moio L, Moschetti G, Piombino P, Addeo F, Coppola S (2001) Characterization of lactic acid bacteria strains on the basis of neutral volatile compounds produced in whey. J Appl Microbiol 90:928–942. https://doi.org/10.1046/j.1365-2672.2001.01327.x
Méndez-Lorenzo L, Porras-Domínguez JR, Raga-Carbajal E, Olvera C, Rodríguez-Alegría ME, Carrillo-Nava E, Costas M, Munguía AL (2015) Intrinsic levanase activity of Bacillus subtilis 168 levansucrase (SacB). PLoS One 10. https://doi.org/10.1371/journal.pone.0143394
Mills O (1986) Sheep dairying in Britain — a future industry. Int J Dairy Technol 39:88–90. https://doi.org/10.1111/j.1471-0307.1986.tb02378.x
Mollea C, Marmo L, Bosco F (2013) Valorisation of cheese whey, a by-product from the dairy industry. 549-588. https://doi.org/10.5772/53159
Morgan-Sagastume F (2016) Characterisation of open, mixed microbial cultures for polyhydroxyalkanoate (PHA) production. Rev Environ Sci Bio 15:593–625. https://doi.org/10.1007/s11157-016-9411
Nadal I, Rico J, Pérez-Martínez G, Yebra MJ, Monedero V (2009) Diacetyl and acetoin production from whey permeate using engineered Lactobacillus casei. J Ind Microbiol Biotechnol 36:1233–1237. https://doi.org/10.1007/s10295-009-0617-9
Nath A, Verasztó B, Basak S, Koris A, Kovács Z, Vatai G (2016) Synthesis of lactose-derived nutraceuticals from dairy waste whey-a review. Food Bioprocess Technol 9:16–48. https://doi.org/10.1007/s11947-015-1572-2
Niaounakis M (2015) Medical, dental, and pharmaceutical applications. Biopolymers: applications and trends, (1st). Elsevier, pp. 291-405. ISBN: 9780323353991
Niknezhad SV, Asadollahi MA, Zamani A, Biria D, Doostmohammadi M (2015) Optimization of xanthan gum production using cheese whey and response surface methodology. Food Sci Biotechnol 24:453–460. https://doi.org/10.1007/s10068-015-0060-9
O’Brien DJ, Panzer C, Eisele W (1990) Biological production of acrylic acid from cheese whey by resting cells of Clostridium propionicum. Biotechnol Prog 6(4):237–242. https://doi.org/10.1012/bp00004a001
Pagliano G, Ventorino V, Panico A, Romano I, Pirozzi F, Pepe O (2019) Anaerobic process for bioenergy recovery from dairy waste: meta-analysis and enumeration of microbial community related to intermediates production. Front Microbiol 9:3229. https://doi.org/10.3389/fmicb.2018.03229
Pandey A, Srivastava S, Rai P, Duke M (2019) Cheese whey to biohydrogen and useful organic acids: a non-pathogenic microbial treatment by L. acidophilus. Sci Rep 9:8320. https://doi.org/10.1038/s41598-019-42752-3
Panesar PS, Panesar R, Singh RS, Kennedy JF, Kumar H (2006) Microbial production, immobilization and applications of β-D-galactosidase. J Chem Technol Biotechnol 81:530–543. https://doi.org/10.1002/jctb.1453
Parrondo J, Herrero M, García LA, Díaz M (2003) A note – production of vinegar from whey. J Inst Brew 109:356–358. https://doi.org/10.1002/j.2050-0416.2003.tb00610.x
Parrondo J, Garcia LA, Diaz M (2009) Whey vinegar. In: Vinegars of the World. Springer Milan, pp 273–288
Patel S (2015) Emerging trends in nutraceutical applications of whey protein and its derivatives. J Food Sci Technol 52:6847–6858. https://doi.org/10.1007/s13197-015-1894-0
Pescuma M, Hébert EM, Mozzi F, Font De Valdez G, Heert EM, Mozzi F, Font De Valdez G (2008) Whey fermentation by thermophilic lactic acid bacteria: evolution of carbohydrates and protein content. Food Microbiol 25:442–451. https://doi.org/10.1016/j.fm.2008.01.007
Pescuma M, Hébert EM, Bru E, de Valdez GF, Mozzi F (2012) Diversity in growth and protein degradation by dairy relevant lactic acid bacteria species in reconstituted whey. J Dairy Res 79:201–208. https://doi.org/10.1017/S0022029912000040
Pescuma M, Font de Valdez G, Mozzi F (2015) Whey-derived valuable products obtained by microbial fermentation. Appl Microbiol Biotechnol 99:6183–6196. https://doi.org/10.1007/s00253-015-6766-z
Petersen N, Gatenholm P (2011) Bacterial cellulose-based materials and medical devices: current state and perspectives. Appl Microbiol Biotechnol 91:1277–1286. https://doi.org/10.1007/s00253-011-3432-y
Prazeres AR, Carvalho F, Rivas J (2012) Cheese whey management: a review. J Environ Manag 110:48–68. https://doi.org/10.1016/j.jenvman.2012.05.018
Ricciardi A, Zotta T, Ianniello RG, Boscaino F, Matera A, Parente E (2019) Effect of respiratory growth on the metabolite production and stress robustness of Lactobacillus casei N87 cultivated in cheese whey permeate medium. Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.00851
Risner D, Shayevitz A, Haapala K, Meunier-Goddik L, Hughes P (2018) Fermentation and distillation of cheese whey: carbon-dioxide equivalent emissions and water use in the production of whey spirits and white whiskey. J Dairy Sci 101:2963–2973. https://doi.org/10.3168/jds.2017-13774
Risner D, Tomasino E, Hughes P, Meunier-Goddik L (2019) Volatile aroma composition of distillates produced from fermented sweet and acid whey. J Dairy Sci 102:202–210. https://doi.org/10.3168/jds.2018-14737
Roberfroid MB, Van Loo JAE, Gibson GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. J Nutr 128:11–19. https://doi.org/10.1093/jn/128.1.11
Roohina F, Mohammadi M, Najafpour GD (2016) Immobilized Kluyveromyces marxianus cells in carboxymethyl cellulose for production of ethanol from cheese whey: experimental and kinetic studies. Bioprocess Biosyst Eng 39:1341–1349. https://doi.org/10.1007/s00449-016-1610-0
Sabokbar N, Khodaiyan F (2016) Total phenolic content and antioxidant activities of pomegranate juice and whey based novel beverage fermented by kefir grains. J Food Sci Technol 53:739–747. https://doi.org/10.1007/s13197-015-2029-3
Saeed M, Anjum FM, Khan MR, Khan MI, Nadeem M (2013) Isolation, characterization and utilization of starter cultures for the development of wheyghurt drink. Br Food J 115:1169–1186. https://doi.org/10.1108/BFJ-10-2011-0274
Sansonetti S, Curcio S, Calabrò V, Iorio G (2009) Bio-ethanol production by fermentation of ricotta cheese whey as an effective alternative non-vegetable source. Biomass Bioenergy 33:1687–1692. https://doi.org/10.1016/j.biombioe.2009.09.002
Sansonetti S, Curcio S, Calabrò V, Iorio G (2010) Optimization of ricotta cheese whey (RCW) fermentation by response surface methodology. Bioresour Technol 101:9156–9162. https://doi.org/10.1016/j.biortech.2010.07.030
Sansonetti S, Hobley TJ, Calabrò V, Villadsen J, Sin G (2011) A biochemically structured model for ethanol fermentation by Kluyveromyces marxianus: a batch fermentation and kinetic study. Bioresour Technol 102:7513–7520. https://doi.org/10.1016/j.biortech.2011.05.014
Savvides AL, Katsifas EA, Hatzinikolaou DG, Karagouni AD (2012) Xanthan production by Xanthomonas campestris using whey permeate medium. World J Microbiol Biotechnol 28:2759–2764. https://doi.org/10.1007/s11274-012-1087-1
Shukla M (2012) Development of probiotic beverage from whey and pineapple juice. J Food Process Technol 04:4–7. https://doi.org/10.4172/2157-7110.1000206
Silva e Alves A, Spadoti L, Zacarchenco P, Trento F (2018) Probiotic functional carbonated whey beverages: development and quality evaluation. Beverages 4:49. https://doi.org/10.3390/beverages4030049
Siso MIG (1996) The biotechnological utilization of cheese whey: a review. Bioresour Technol 57:1–11
Skryplonek K (2018) The use of acid whey for the production of yogurt-type fermented beverages. Mljekarstvo 68:139–149. https://doi.org/10.15567/mljekarstvo.2018.0207
Skryplonek K, Jasińska M (2017) Whey-based beverages. Electr J Polish Agr Univ 20(4). https://doi.org/10.30825/5.EJPAU.36.2017.20.4
Sohrabi Z, Eftekhari MH, Eskandari MH, Rezaeianzadeh A, Sagheb MM (2016) Development and characterization of fermented and unfermented whey beverages fortified with vitamin E. J Agric Sci Technol 18:1511–1521
Tamura Y (2000) Manufacture of the vinegar from cheese whey. Milk Sci 49:15–20. https://doi.org/10.11465/milk.49.15
Thakkar P, Vaghela B, Patel A, Modi HA, Prajapati JB (2018) Formulation and shelf life study of a whey-based functional beverage containing orange juice and probiotic organisms. Int Food Res J 25:1675–1681
Thompson DN, Hamilton MA (2001) Production of bacterial cellulose from alternate feedstocks. Appl Biochem Biotechnol 91-93:503–513. https://doi.org/10.1385/ABAB:91-93:1-9:503
Tomaszewska M, Białończyk L (2016) Ethanol production from whey in a bioreactor coupled with direct contact membrane distillation. Catalysis Today. Elsevier, pp 156–163. https://doi.org/10.1016/j.cattod.2016.01.059
Tripathi V, Jha YK (2004) Development of whey beverage with antagonistic characteristics and probiotics. Int J Food Prop 7:261–272. https://doi.org/10.1081/JFP-120030037
Turkmen N, Akal C, Özer B (2019) Probiotic dairy-based beverages: a review. J Funct Foods 53:62–75. https://doi.org/10.1016/j.jff.2018.12.004
Ulerly BD, Nair LS, Laurencin CT (2011) Biomedical applications of biodegradable polymers. J Polym Sci B Polym Phys 49(12):832–864. https://doi.org/10.1002/polb.22259
Umaraw P, Verma A (2015) Comprehensive review on application of edible film on meat and meat products: an eco-friendly approach. Crit Rev Food Sci 57(6):1549–7852. https://doi.org/10.1080/10408398.2014.986563
Utama GL, Kurnani TBA, Sunardi S, Cahyandito MF, Balia RL (2017) Joint cost allocation of cheese-making wastes bioconversions into ethanol and organic liquid fertilizer. Bulg J Agric Sci 23:1016–1020
van Dijken JP, Weusthuis RA, Pronk JT (1993) Kinetics of growth and sugar consumption in yeasts. Antonie Van Leeuwenhoek 63:343–352. https://doi.org/10.1007/BF00871229
Vaningelgem F, Zamfir M, Adriany T, De Vuyst L (2004) Fermentation conditions affecting the bacterial growth and exopolysaccharide production by Streptococcus thermophilus ST 111 in milk-based medium. J Appl Microbiol 97:1257–1273. https://doi.org/10.1111/j.1365-2672.2004.02418.x
Varela JA, Montini N, Scully D, Van der Ploeg R, Oreb M, Boles E, Hirota J, Akada R, Hoshida H, Morrissey JP (2017) Polymorphisms in the LAC12 gene explain lactose utilisation variability in Kluyveromyces marxianus strains. FEMS Yeast Res 17. https://doi.org/10.1093/femsyr/fox021
Vazquez A, Foresti ML, Cerrutti P, Galvagno M (2013) Bacterial cellulose from simple and low cost production media by Gluconacetobacter xylinus. J Polym Environ 21:545–554. https://doi.org/10.1007/s10924-012-0541-3
Ventkiteshwaran K, Bocher B, Maki J, Zitomer D (2015) Relating anaerobic digestion microbial community and process function. Microbiol Insights 8:37–44. https://doi.org/10.4137/MBI.S33593
Verlinden RA, Hill DJ, Kenward MA, Williams CD, Radecka I (2007) Bacterial synthesis of biodegradable polyhydroxyalkanoates. J Appl Microbiol 102:1437–1449. https://doi.org/10.1111/j.1365-2672.2007.03335.x
Virtanen T, Pihlanto A, Akkanen S, Korhonen H (2007) Development of antioxidant activity in milk whey during fermentation with lactic acid bacteria. J Appl Microbiol 102:106–115. https://doi.org/10.1111/j.1365-2672.2006.03072.x
Wan C, Li Y, Shahbazi A, Xiu S (2008) Succinic acid production from cheese whey using Actinobacillus succinogenes 130 Z. Appl Biochem Biotechnol 145:111–119. https://doi.org/10.1007/s12010-007-8031-0
Xie YY, Hu XH, Zhang YW, Wahid F, Chu LQ, Jia SR, Zhong C (2020) Development and antibacterial activities of bacterial cellulose/graphene oxide-CuO nanocomposite films. Carbohydr Polym 229:115456. https://doi.org/10.1016/j.carbpol.2019.115456
Yadav JSS, Yan S, Pilli S, Kumar L, Tyagi RD, Surampalli RY (2015) Cheese whey: a potential resource to transform into bioprotein, functional/nutritional proteins and bioactive peptides. Biotechnol Adv 33:756–774. https://doi.org/10.1016/j.biotechadv.2015.07.002
Yerlikaya O, Akpinar A, Torunoglu FA, Kinik O, Akbulut N, Uysal H (2012) Effect of some prebiotic combination on viability of probiotic bacteria in reconstituted whey and milk beverages. Agro Food Ind Hi Tech 23:XXVII–XXIX
Zisu B, Shah NP (2003) Effects of pH, temperature, supplementation with whey protein concentrate, and adjunct cultures on the production of exopolysaccharides by Streptococcus thermophilus 1275. J Dairy Sci 86:3405–3415. https://doi.org/10.3168/jds.S0022-0302(03)73944-7
Zoellner SS, Cruz AG, Faria JAF, Bolini HMA, Moura MRL, Carvalho LMJ, Sant’ana AS (2009) Whey beverage with acai pulp as a food carrier of probiotic bacteria. Aust J Dairy Technol 64:177–181
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Zotta, T., Solieri, L., Iacumin, L. et al. Valorization of cheese whey using microbial fermentations. Appl Microbiol Biotechnol 104, 2749–2764 (2020). https://doi.org/10.1007/s00253-020-10408-2
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DOI: https://doi.org/10.1007/s00253-020-10408-2