Production of biodegradable microbial polymers from whey

Abstract

Current research in industrial microbiology and biotechnology focuses on the production of biodegradable microbial polymers as an environmentally friendly alternative to still dominant fossil-based plastics. Microbial polymers have an extensive biotechnological potential and are already widely used in a variety of fields ranging from medicine to technology. However, their increase in production and wider use is hampered by the high cost of raw materials and therefore requires a focus on cheaper inputs, including dairy by-products and waste such as cheese whey (CW). This is an environmentally unfriendly by-product of milk processing and reducing it would also reduce the risk of environmental pollution. This review summarises current knowledge on the use of CW and derived products to obtain commercially important microbial polymers, including information about producer cultures, fermentation techniques and methods used, composition of culture medium, cultivation conditions and productivity of bioprocesses. The main methods and applications of cheese whey pre-treatment are also summarised.

Keywords

Biopolymers / Bacterial exopolysaccharides / Polyhydroxyalkanoates / Whey

References

[1] Abd El-Gawad IA, Murad HA, El-Sayed EM, Salah SH. Optimum conditions for the production of xanthan gum from hydrolysed UF-milk permeate by locally isolated Xanthomonas campestris. Egypt J Dairy Sci, 2001, 29: 37-51.

[2] Abdel Hafez AM, Abdelhady HM, Sharaf MS, El-Tayeb TS. Bioconversion of various industrial by-products and agricultural wastes into pullulan. J Appl Sci Res, 2007, 3(11): 1416-1425.

[3] Abdelhady HM, Enas AH, Sohir SA, Sara MA. Bacterial cellulose production as affected by bacterial strains and some fermentation conditions. Nat Sci, 2015, 13(3): 30-40.

[4] Ahn WS, Park SJ, Lee SY. Production of poly (3-hydroxybutyrate) by fed-batch culture of recombinant Escherichia coli with a highly concentrated whey solution. Appl Environ Microbiol, 2000, 66: 3624-3627.

[5] Ahn WS, Park SJ, Lee SY. Production of poly (3-hydroxybutyrate) from whey by cell recycle fed-batch culture of recombinant Escherichia coli. Biotechnol Lett, 2001, 23: 235-240.

[6] Alborch M (2014) LIFE+ WHEYPACK - Reduction of CO2 emissions by the PHB use obtained from whey : demonstration in dairy products packaging. LIFE 13 ENV/ES/000608. https://ec.europa.eu/environment/life/project/Projects/index.cfm?fuseaction=search.dspPage&n proj id=5084#PD

[7] Amado IR, Vázquez JA, Pastrana L, Teixeira JA. Cheese whey: a cost-effective alternative for hyaluronic acid production by Streptococcus zooepidemicus. Food Chem, 2016, 198: 54-61.

[8] Amaro TMMM, Rosa F, Comi G, Iacumin L. Prospects for the use of whey for polyhydroxyalkanoate (PHA) production. Front Microbiol, 2019, 10: 992.

[9] Arancon RAD, Lin CSK, Chan KM, Kwan TH, Luque R. Advances on waste valorization: new horizons for a more sustainable society. Ener Sci Engin, 2013, 1(2): 53-71.

[10] Babu RP, O’Connor K, Seeram R. Current progress on bio-based polymers and their future trends. Prog Biomat, 2013, 2(8): 1-16.

[11] Bajaj IB, Saudagar PS, Singhal RS, Pandey A. Statistical approach to optimization of fermentative production of gellan gum from Sphingomonas paucimobilis ATCC 31461. J Biosci Bioeng, 2006, 102(3): 150-156.

[12] Battad-Bernardo E, McCrindle SL, Couperwhite I, Neilan BA. Insertion of an E. coli lacZ gene in Acetobacter xylinus for the production of cellulose in whey. FEMS Microbiol Lett., 2004, 231(2): 253-260.

[13] Becker A. (2015). Challenges and perspectives in combinatorial assembly of novel exopolysaccharide biosynthesis pathways. Front Microbiol. 6:687. doi: 10.3389/fmicb.2015.00687

[14] Bekatorou A, Plioni I, Sparou K, Tsafrakidou RMP, Petsi T, Kordouli E. Bacterial cellulose production using the corinthian currant finishing side-stream and cheese whey: process optimization and textural characterization. Foods, 2019, 8: 193-207.

[15] Berwig KH, Baldasso C, Dettmer A. Production and characterization of poly(3-hydroxybutyrate) generated by Alcaligenes latus using lactose and whey after acid protein precipitation process. Bioresour Technol, 2016, 218: 31-37.

[16] Brown S, Pummill P. Recombinant production of hyaluronic acid. Cur Pharmac Biotechnol, 2008, 9(4): 239-241.

[17] Bustamante D, Segarra S, Tortajada M, Ramón D, del Cerro C, Prieto A, Rojas A. In silico prospection of microorganisms to produce polyhydroxyalkanoate from whey: Caulobacter segnis DSM 29236 as a suitable industrial strain. Microbial Biotechnol, 2019

[18] Carreira P, Mendes JAS, Trovatti E, Serafim LS, Freire CSR, Silvestre AJD, Neto CP. Utilization of residues from agro-forest industries in the production of high value bacterial cellulose. Biores Techn, 2011, 102(15): 7354-7360.

[19] Chanfrau JMP, Pérez JN, Fiallos MVL, Rivera L, Abril VH, Guerrero MJC, Toledo LET. Milk whey—from a problematic byproduct to a source of valuable products for health and industry: an overview from biotechnology. Prensa Med Argent, 2017, 103(4): 1-11.

[20] Chegini G, Taheri M. Whey powder: process technology and physical properties: a review. J Middle East Sci Res, 2013, 13: 1377-1387.

[21] Chen X, Gao H, Ploehn HJ. Montmorillonite-levan nanocomposites with improved thermal and mechanical properties. Carbohyd Polym, 2014, 101: 565-573.

[22] Cheng KC, Demirci A, Catchmark JM. Pullulan: biosynthesis, production, and applications. Appl Microbiol and Biotechnol, 2011, 92(1): 29-44.

[23] Chong BF, Blank LM, Mclaughlin R, Nielsen LK. Microbial hyaluronic acid production. Appl Microbiol and Biotechnol, 2004, 66(4): 341-351.

[24] Cinti G (2015) Method for the production of dextran. International Patent WO 2015/117624 AI, 13 Aug 2015

[25] Colombo B, Pepè Sciarria T, Reis M, Scaglia B, Adani F. Polyhydroxyalkanoates (PHAs) production from fermented cheese whey by using a mixed microbial culture. Biores Technol, 2016, 218(692): 699.

[26] Donot F, Fontana A, Baccou JC, Schorr-Galindo S. Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohyd Polym, 2012, 87(2): 951-962.

[27] Duque AF, Oliveira CSS, Carmo ITD, Gouveia AR, Pardelha F, Ramos AM, Reis MAM. Response of a three-stage process for PHA production by mixed microbial cultures to feedstock shift: impact on polymer composition. New Biotechnol, 2014, 31(4): 276-288.

[28] El-Sawah MMA, Ashour EH. Xanthan production from whey treated with lactase. Pakistan J Biol Sci, 1999, 2(4): 1240-1244.

[29] Esmaeilnejad-Moghadam B, Mokarram RR, Hejazi MA, Khiyabani MS, Keivaninahr F. Low molecular weight dextran production by Leuconostoc mesenteroides strains: optimization of a new culture medium and the rheological assessments. Bioact Carbohydr Diet Fibre, 2019

[30] Eweda WE, Sharaf MS, El Sayed AM. Production of curdlan by some bacteria isolated from Egyptian soils. Middle East J App. Sci, 2015, 1: 102-118.

[31] Fialho AM, Martins LO, Donval ML, Leitao JH, Ridout MJ, Jay AJ, Morris VJ, Sá-Correia I. Structures and properties of gellan polymers produced by Sphingomonas paucimobilis ATCC 31461 from lactose compared with those produced from glucose and from cheese whey. Appl Environ Microbiol, 1999, 65: 2485-2491.

[32] Fialho AM, Moreira LM, Granja AT, Popescu AO, Hoffmann K, Sá-Correia I. Occurrence, production, and applications of gellan: current state and perspectives. Appl Microbiol Biotechnol, 2008, 79(6): 889-900.

[33] Freitas F, Alves VD, Reis MAM. Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol, 2011, 29(8): 388-398.

[34] Gahlawat G, Srivastava AK. Model-based nutrient feeding strategies for the increased production of polyhydroxybutyrate (PHB) by Alcaligenes latus. Appl Biochem Biotechnol, 2017, 183(2): 530-542.

[35] Gamal FG, Abdel-hady HM, Amin SA, Ali SK. Production of gellan gum by Sphingomonas paucimobilis on crude sweet whey using different bioreactor feeding strategies. South Asian J Res in Microbiol, 2018, 1(4): 1-12.

[36] Ghazal SMA, Elsayed WS, Badr UM, Gebreel HM, Khalil KMA. Genetically modified strains of Xanthomonas campestris higher xanthan producer and capable to utilize whey. Cur Res in Bacteriol, 2011, 4: 44-62.

[37] Gopi S, Anitha A, Thomas S (2016) Biodegradable Green Composites (ed) Biodegradable Green Composites, 1E. Wiley & Sons Inc, USA pp 1-17

[38] Gorgieva S, Trček J. Bacterial cellulose: production, modification and perspectives in biomedical applications. Nanomaterials, 2019, 9(10): 1352.

[39] Güven G, Perendeci A, Tanyolaç A. Electrochemical treatment of deproteinated whey wastewater and optimization of treatment conditions with response surface methodology. J of Haz Mater, 2008, 157(1): 69-78.

[40] Hendawy WS, El Kanani YM, El Batawy OI, El Mongy TM. Optimization the alginate production conditions in sweet whey medium by Azotobacter chrococcum. AUJAS Egypt Spec Issue, 2019, 27(4): 479-489.

[41] Kang HK, Seo MY, Seo ES, Kim D, Chung SY, Kimura A, Robyt JF. Cloning and expression of levansucrase from Leuconostoc mesenteroides B-512 FMC in Escherichia coli. Biochem Biophys Acta, 2005, 1727(1): 5-15.

[42] Katzen F, Ferreiro DU, Oddo CG. Xanthomonas campestris pv. campestris gum mutants: effects on xanthan biosynthesis and plant virulence. J Bacteriol, 1998, 180(7): 1607-1617.

[43] Khanafari A, Sepahei A. Alginate biopolymer production by Azotobacter chroococcum from whey degradation. Int J Environ Sci Tech, 2007, 4(4): 427-432.

[44] Koller M, Braunegg G. Advanced approaches to produce polyhydroxyalkanoate (PHA) biopolyesters in a sustainable and economic fashion. EuroBiotech J, 2018

[45] Koller M, Hesse PJ, Bona R, Kutschera C, Atlic A, Braunegg G. Biosynthesis of high quality polyhydroxyalkanoate co- and terpolyesters for potential medical application by the archaeon Haloferax mediterranei. Macromol Symp, 2007, 253: 33-39.

[46] Koller M, Salerno A, Muhr A, . Polyhydroxyalkanoates: biodgradable polymers and plastics from renewable resources. Mater Technol, 2012, 46: 23-30.

[47] Kreyenschulte D, Krull R, Margariti A. Recent advances in microbial biopolymer production and purification. Crit Rev Biotechnol, 2012

[48] Kucera D, Pernicová I, Kovalcik A, Koller M, Mullerova L, Sedlacek P. Characterization of the promising poly(3-hydroxybutyrate) producing halophilic bacterium Halomonas halophila. Bioresour Technol, 2018, 256: 552-556.

[49] Lappa IK, Papadaki A, Kachrimanidou V, Terpou A, Koulougliotis D, Eriotou E, Kopsahelis N. Cheese whey processing: integrated biorefinery concepts and emerging food applications. Foods, 2019, 8(8): 347.

[50] Lin AY, Nickerson TA. Acid hydrolysis of lactose in whey versus aqueous solutions. J Dair Sci, 1977, 60(1): 34-39.

[51] Liu Y, Gu Q, Ofosu FK, Yu X. Isolation and characterization of curdlan produced by Agrobacterium HX1126 using α-lactose as substrate. Inter J Biol Macromol, 2015, 81: 498-503.

[52] Lo YM, Sanem AS, Hsu CH. Yang ST. Bioconversion of whey lactose into microbial exopolysaccharides. Bioprocessing for Value-Added Products from Renewable Resources, 2007, Netherlands: Elsevier Science.

[53] Luckachan GE, Pillai CKS. Biodegradable Polymers—a review on recent trends and emerging perspectives. J Polym Environ, 2011, 19: 637-676.

[54] Lule V, Singh R, Behare P, Tomar SK. Comparison of exopolysaccharide production by indigenous Leuconostoc mesenteroides strains in whey medium. Asian J Dairy Food Res, 2015

[55] Lule VK, Singh R, Pophaly SD, Poonam SK, Tomar SK. Production and structural characterisation of dextran from an indigenous strain of Leuconostoc mesenteroides BA08 in whey. Inter J Dairy Tech, 2016, 69(4): 520-531.

[56] Marangoni C, Furigo A, De Aragão GMF. Production of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) by Ralstonia eutropha in whey and inverted sugar with propionic acid feeding. Proc Biochem, 2002, 38: 137-141.

[57] Mesomo M, Silva MF, Boni G, Padilha FF, Mazutti M, Mossi A, Treichel H. Xanthan gum produced by Xanthomonas campestrisfrom cheese whey: production optimisation and rheological characterisation. J Scien Food Agricult, 2009, 89(14): 2440-2445.

[58] Mikkelsen D, Flanagan BM, Dykes GA, Gidley MJ. Influence of different carbon sources on bacterial cellulose production by Gluconacetobacter xylinusstrain ATCC 53524. J Appl Microbiol, 2009, 107(2): 576-583.

[59] Mohan N, Balakrishnan R, Sivaprakasam S. Optimization and effect of dairy industrial waste as media components in the production of hyaluronic acid by Streptococcus thermophilus. Prepar Biochem Biotechnol, 2016, 46(6): 628-638.

[60] Mollea C, Marmo L, Bosco F. Valorisation of cheese whey, a by-product from the dairy industry. Food Ind, 2013

[61] Narancic T, O’Connor KE. Plastic waste as a global challenge: are biodegradable plastics the answer to the plastic waste problem?. Microbiol, 2019, 165: 129-137.

[62] Nath A, Dixit M, Bandiya A, Chavda S, Desai AJ. Enhanced PHB production and scale up studies using cheese whey in fed batch cultures of Methylobacterium sp ZP24. Biores Techn., 2008, 99(13): 5749-5755.

[63] Niknezhad SV, Asadollahi MA, Zamani A, Biria D, Doostmohammadi M. Optimization of xanthan gum production using cheese whey and response surface methodology. Food Sci Biotech, 2015, 24(2): 453-460.

[64] Nitschke M, Rodrigues V, Schinatto LF. Formulacao de meios de cultivo a base de soro de leite para a producao de goma xantana por X. campestris C7L. Cienc Tecnol Alim, 2001, 21: 82-85.

[65] Özcan E, Öner ET. Microbial Production of Extracellular Polysaccharides from Biomass Sources. Polysacch, 2015

[66] Pais J, Serafim LS, Freitas F, Reis MAM. Conversion of cheese whey into poly(3-hydroxybutyrate-co-3-hydroxyvalerate) by Haloferax mediterranei. N Biotechnol, 2016, 33(1): 224-230.

[67] Pantazaki AA, Papaneophytou CP, Pritsa AG, Liakopoulou-Kyriakides M, Kyriakidis DA. Production of polyhydroxyalkanoates from whey by Thermus thermophilus HB8. Proc Biochem, 2009, 44(8): 847-853.

[68] Park SJ, Park JP, Lee SY. Production of poly(3-hydroxybutyrate) from whey by fed-batch culture of recombinant Escherichia coli in a pilot-scale fermenter. Appl Environ Microbiol, 2002, 63: 4795-4796.

[69] Pescuma M, de Valdez GF, Mozzi F. Whey-derived valuable products obtained by microbial fermentation. Appl Microbiol Biotechnol, 2015, 99(15): 6183-6196.

[70] Poli A, Di Donato P, Abbamondi GR, Nicolaus B. Synthesis, production, and biotechnological applications of exopolysaccharides and polyhydroxyalkanoates by archaea. Archaea, 2011

[71] Pollock and Thorne (1994) Xanthomonas campestris strain for production of xanthan gum. US Patent 5,279,961 18 Jan 1994

[72] Popović SZ, Lazić VL, Hromiš NM, Šuput DZ, Bulu SN. Biopolymer packaging materials for food shelf-life prolongation. Biopolymers Food Design, 2018

[73] Povolo S, Toffano P, Basaglia M, Casella S. Polyhydroxyalkanoates production by engineered Cupriavidus necator from waste material containing lactose. Bioresour Technol, 2010, 101: 7902-7907.

[74] Prazeres AR, Carvalho F, Rivas J. Cheese whey management: a review. J Environ Manag, 2012, 110: 48-68.

[75] RamKumar Pandian S, Deepak V, Kalishwaralal K, Rameshkumar N, Jeyaraj M, Gurunathan S. Optimization and fed-batch production of PHB utilizing dairy waste and sea water as nutrient sources by Bacillus megaterium SRKP-3. Biores Techn, 2010, 101(2): 705-711.

[76] Rehm BHA. Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol, 2010, 8: 578-592.

[77] Revin VV, Novokuptsev NV, Red’kin NA. Optimization of cultivation conditions for Azotobacter vinelandii D-08, producer of the polysaccharide levan, for obtaining biocomposite materials. BioRes, 2016

[78] Revin V, Liyaskina E, Nazarkina M, Bogatyreva A, Shchankin M. Cost-effective production of bacterial cellulose using acidic food industry by-products. Braz J Microb, 2018

[79] Rosalam S, England R. Review of xanthan gum production from unmodified starches by Xanthomonas campestris sp. Enz Microbial Technol, 2006, 39: 197-207.

[80] Rottava I, Batesini G, Silva MF, Lerin L, de Oliveira D, Padilha FF, Treichel H. Xanthan gum production and rheological behavior using different strains of Xanthomonas sp. Carbohyd Polym, 2009, 77(1): 65-71.

[81] Roukas T. Pullulan production from deproteinized whey by Aureobasidium pullulans. J Industr Microbiol Biotechnol, 1999, 22: 617-621.

[82] Sadh PK, Duhan S, Duhan JS. Agro-industrial wastes and their utilization using solid state fermentation: a review. Bioresour Bioprocess, 2018, 5: 1-15.

[83] Salari M, Khiabani MS, Mokarram RR, Ghanbarzadeh B, Kafil HS. Preparation and characterization of cellulose nanocrystals from bacterial cellulose produced in sugar beet molasses and cheese whey media. Intern J Bio Macromol, 2018

[84] San Bias F (1991) Xanthomonas campestris mutant that produces xanthan gum upon cultivation on lactose or unhydrolyzed whey. European Patent 0 481 785 A2, 17 Oct 1991

[85] Santos M, Rodrigues A, Teixeira JA. Production of dextran and fructose from carob pod extract and cheese whey by Leuconostoc mesenteroides NRRL B512(f). Biochem Engin J, 2005, 25(1): 1-6.

[86] Savvides AL, Katsifas EA, Hatzinikolaou DG, Karagouni AD. Xanthan production by Xanthomonas campestris using whey permeate medium. W J Microbiol Biotechnol, 2012, 28(8): 2759-2764.

[87] Schwartz RD, Bodie EM. Production of viscous dextran-containing whey–sucrose broths by Leuconostoc mesenteroides ATCC 14935. Appl Environ Microbiol, 1984, 48: 678-679.

[88] Semjonovs P, Shakirova L, Treimane R, Shvirksts K, Auzina L, Cleenwerck I, Zikmanis P. Production of extracellular fructans by Gluconobacter nephelii P1464. Lett Appl Microbiol, 2015, 62: 145-152.

[89] Semjonovs P, Ruklisha M, Paegle L, Saka M, Treimane R, Skute M, Rozenberga L, Vikele L, Sabovics M, Cleenwerck I. Cellulose synthesis by Komagataeibacter rhaeticus strain P 1463 isolated from Kombucha. Appl Microbiol Biotechnol, 2017, 101: 1003-1012.

[90] Shanmugam M, Abirami RG. Microbial Polysaccharides—Chemistry and Applications. J Bio Active Prod Nat, 2019, 9: 73-78.

[91] Siddiqui NN, Aman A, Silipo A, Qader SAU, Molinaro A. Structural analysis and characterization of dextran produced by wild and mutant strains of Leuconostoc mesenteroides. Carbohyd Polym, 2014, 99: 331338.

[92] Siracusa V, Rocculi P, Romani S, Dalla Rosa M. Biodegradable polymers for food packaging: a review. Trends Food Sci Techn, 2008, 19: 634-643.

[93] Sirviö JA, Visanko M, Ukkola J, Liimatainen H. Effect of plasticizers on the mechanical and thermomechanical properties of cellulose-based biocomposite films. Industr Crops Prod, 2018, 122: 513-521.

[94] Sobenes J, Alegre R. Producão de goma xantana por X Campestris ATCC 13951 utilizando soro de queijo desproteinado. Rev Ion Invest Optim y Nuev Proce En Ingen, 2015, 28(2): 69-77.

[95] Thompson DN, Hamilton MA. Production of bacterial cellulose from alternate feedstocks. Appl Biochem Biotech, 2001, 91–93(1–9): 503-514.

[96] Torres DPM, Gonçalves MPF, Teixeira JA, Rodrigues LR. Galacto-oligosaccharides: production, properties, applications, and significance as prebiotics. Compreh Rev Food Sci Food Saf, 2010, 9(5): 438-454.

[97] Trujillo-Roldán MA, John FMG, Angélica MCA, Norma AVC. The production, molecular weight and viscosifying power of alginate produced by Azotobacter vinelandii is affected by the carbon source insubmerged cultures. DYNA, 2015, 82(194): 21-26.

[98] Tsang YF, Kumar V, Samadar P, Yang Y, Lee J, Ok YS, Song H, Ki-Hyun Kim K-H, Kwon EE, Jae Jeon YJ. Production of bioplastic through food waste valorization. Environ Int, 2019, 127: 625-644.

[99] Tsouko E, Kourmentza C, Ladakis D, Kopsahelis N, Mandala I, Papanikolaou S, Koutinas A. Bacterial cellulose production from industrial waste and by-product streams. Inter J Molec Sci, 2015, 16(12): 14832-14849.

[100] Ul-Islam M, Khan S, Ullah MW, Park JK. Bacterial cellulose composites: synthetic strategies and multiple applications in bio-medical and electro-conductive fields. Biotechnol J, 2015, 10: 847-1861.

[101] Urtuvia V, Maturana N, Acevedo F, Peña C, Díaz-Barrera A. Bacterial alginate production: an overview of its biosynthesis and potential industrial production. W J Microbio Biotech, 2017

[102] Van de Velde K, Kiekens P. Biopolymers: overview of several properties and consequences on their applications. Polym Test, 2002, 21(4): 433-442.

[103] Wang D, Kim H, Lee S, Kim DH, Joe MH. Improved gellangum production by a newly-isolated Sphingomonas azotifigens GL-1 in a cheese whey and molasses based medium. Proc Biochem, 2020

[104] Yellore V, Desai A. Production of poly-3-hydroxybutyrate from lactose and whey by Methylobacterium sp. ZP24. Lett Appl Microbiol, 1998, 26: 391-394.

[105] Young FK, Kastner JR, May SW. Microbial production of poly-betahydroxybutyric acid from d-xylose and lactose by Pseudomonas cepacia. Appl Environ Microbiol, 1994, 60(11): 4195-4198.

Funding

Ministry of Agriculture and Rural Support Service of the Republic of Latvia(19-00-A01612-000004)