Abstract
Bacterial cellulose (BC) was functionalized applying the Laccase/TEMPO oxidative treatment, leading to a five-fold increase of the concentration of carboxyl groups. Paper produced with this cellulose showed improved mechanical properties while maintaining barrier function against water and greases as compared to paper produced with non-oxidized BC. Also, the negative charge provided by the carboxyl groups on functionalized BC was used to generate silver nanoparticles (AgNPs), obtaining a BC paper and Ag composite. The presence of AgNPs in the composites was validated by SEM, EDS and ICP analysis, showing spherical, uniformly sized particles stabilized in the BC nanofibers matrix. Additionally, antimicrobial property of composites containing AgNPs was tested. The results showed the strong antimicrobial activity of the composites against Gram-positive and Gram-negative bacteria and fungi. The generation of Ag nanoparticles in a matrix that combine the physical characteristics of the BC nanofibers with the stiffness and the mechanical properties of paper produced composites that may have applicability in technological and biomedical uses.
Graphic abstract
This is a preview of subscription content, log in via an institution to check access.
References
Abdel-Mohsen AM, Abdel-Rahman RM, Fouda MMG, Vojtova L, Uhrova L, Hassan AF, Al-Deyab SS, El-Shamy IE, Jancar J (2014) Preparation, characterization and cytotoxicity of schizophyllan/silver nanoparticle composite. Carbohydr Polym 102(1):238–245. https://doi.org/10.1016/j.carbpol.2013.11.040
Aracri E, Vidal T (2012) Enhancing the effectiveness of a laccase–TEMPO treatment has a biorefining effect on sisal cellulose fibres. Cellulose 19(3):867–877. https://doi.org/10.1007/s10570-012-9686-4
Aracri E, Vidal T, Ragauskas AJ (2011) Wet strength development in sisal cellulose fibers by effect of a laccase–TEMPO treatment. Carbohydr Polym 84(4):1384–1390. https://doi.org/10.1016/j.carbpol.2011.01.046
Aracri E, Valls C, Vidal T (2012) Paper strength improvement by oxidative modification of sisal cellulose fibers with laccase–TEMPO system: influence of the process variables. Carbohydr Polym 88(3):830–837. https://doi.org/10.1016/j.carbpol.2012.01.011
Barud HS, Regiani T, Marques RFC, Lustri WR, Messaddeq Y, Ribeiro SJL (2011) Antimicrobial bacterial cellulose-silver nanoparticles composite membranes. J Nanomater 2011:1–8. https://doi.org/10.1155/2011/721631
Bielecki S, Kalinowska H, Krystynowicz A, Kubiak K, Kołodziejczyk M, de Groeve M (2012) Wound dressings and cosmetic materials from bacterial nanocellulose. In: Gama M, Gatenholm P, Klemm D (ed) Perspectives in nanotechnology series. Bacterial nanocellulose, 1st edn. CRC Press, Boca Raton, pp 157–174
Chawla PR, Bajaj IB, Survase SA, Singhal RS (2009) Microbial cellulose: fermentative production and applications. Food Technol Biotechnol 47:107–124
Chen Y, Geng B, Ru J, Tong C, Liu H, Chen J (2017) Comparative characteristics of TEMPO-oxidized cellulose nanofibers and resulting nanopapers from bamboo, softwood, and hardwood pulps. Cellulose 24(11):4831–4844. https://doi.org/10.1007/s10570-017-1478-4
Davidson GF (1948) The acidic properties of cotton cellulose and derived oxycelluloses. Part II. The absorption of methylene blue. J Text Inst Trans 39(3):T65–T86. https://doi.org/10.1080/19447024808659403
de Santa Maria LC, Santos ALC, Oliveira PC, Barud HS, Messaddeq Y, Ribeiro SJL (2009) Synthesis and characterization of silver nanoparticles impregnated into bacterial cellulose. Mater Lett 63(9–10):797–799. https://doi.org/10.1016/j.matlet.2009.01.007
Feng QL, Wu J, Chen GQ, Cui FZ, Kim TN, Kim JO (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52(4):662–668. https://doi.org/10.1002/1097-4636(20001215)52:4%3c662:AID-JBM10%3e3.0.CO;2-3
Feng J, Shi Q, Li W, Shu X, Chen A, Xie X, Huang X (2014) Antimicrobial activity of silver nanoparticles in situ growth on TEMPO-mediated oxidized bacterial cellulose. Cellulose 21(6):4557–4567. https://doi.org/10.1007/s10570-014-0449-2
Fillat A, Martínez J, Valls C, Cusola O, Roncero MB, Vidal T, Valenzuela SV, Diaz P, Pastor FIJ (2018) Bacterial cellulose for increasing barrier properties of paper products. Cellulose 25(10):6093–6105. https://doi.org/10.1007/s10570-018-1967-0
Gao C, Wan Y, Yang C, Dai K, Tang T, Luo H, Wang J (2011) Preparation and characterization of bacterial cellulose sponge with hierarchical pore structure as tissue engineering scaffold. J Porous Mater 18(2):139–145. https://doi.org/10.1007/s10934-010-9364-6
Gehmayr V, Potthast A, Sixta H (2012) Reactivity of dissolving pulps modified by TEMPO-mediated oxidation. Cellulose 19(4):1125–1134. https://doi.org/10.1007/s10570-012-9729-x
Gert EV, Torgashov VI, Zubets OV, Kaputskii FN (2005) Preparation and properties of enterosorbents based on carboxylated microcrystalline cellulose. Cellulose 12(5):517–526. https://doi.org/10.1007/s10570-005-7134-4
Hasan N, Biak DRA, Kamarudin S (2012) Application of bacterial cellulose (BC) in natural facial scrub. Int J Adv Sci Eng Inf Technol 2(4):272. https://doi.org/10.18517/ijaseit.2.4.201
Ifuku S, Tsuji M, Morimoto M, Saimoto H, Yano H (2009) Synthesis of silver nanoparticles templated by TEMPO-mediated oxidized bacterial cellulose nanofibers. Biomacromolecules 10(9):2714–2717. https://doi.org/10.1021/bm9006979
Inoue Y, Kiyono Y, Asai H, Ochiai Y, Qi J, Olioso A, Shiraiwa T, Horie T, Saito K, Dounagsavanh L (2010) Assessing land-use and carbon stock in slash-and-burn ecosystems in tropical mountain of Laos based on time-series satellite images. Int J Appl Earth Obs Geoinf 12(4):287–297. https://doi.org/10.1016/j.carbpol.2017.02.093
Isogai A, Saito T, Fukuzumi H (2011) TEMPO-oxidized cellulose nanofibers. Nanoscale 3(1):71–85. https://doi.org/10.1039/C0NR00583E
Jalili Tabaii M, Emtiazi G (2018) Transparent nontoxic antibacterial wound dressing based on silver nano particle/bacterial cellulose nano composite synthesized in the presence of tripolyphosphate. J Drug Deliv Sci Technol 44:244–253. https://doi.org/10.1016/j.jddst.2017.12.019
Jaušovec D, Vogrinčič R, Kokol V (2015) Introduction of aldehyde vs. carboxylic groups to cellulose nanofibers using laccase/TEMPO mediated oxidation. Carbohydr Polym 116:74–85. https://doi.org/10.1016/j.carbpol.2014.03.014
Jiang J, Ye W, Liu L, Wang Z, Fan Y, Saito T, Isogai A (2017) Cellulose nanofibers prepared using the TEMPO/laccase/O2 system. Biomacromolecules 18(1):288–294. https://doi.org/10.1021/acs.biomac.6b01682
Johnson RK, Zink-Sharp A, Glasser WG (2011) Preparation and characterization of hydrophobic derivatives of TEMPO-oxidized nanocelluloses. Cellulose 18(6):1599–1609. https://doi.org/10.1007/s10570-011-9579-y
Jun YW, Choi JS, Cheon J (2007) Heterostructured magnetic nanoparticles: their versatility and high performance capabilities. Chem Commun. https://doi.org/10.1039/b614735f
Kitaoka T, Isogai A, Onabe F (1999) Chemical modification of pulp fibers by TEMPO-mediated oxidation. Nord Pulp Pap Res J 14(04):279–284. https://doi.org/10.3183/NPPRJ-1999-14-04-p279-284
Kong H, Jang J (2008) Antibacterial properties of novel poly(methyl methacrylate) nanofiber containing silver nanoparticles. Langmuir 24(5):2051–2056. https://doi.org/10.1021/la703085e
Lai C, Sheng L, Liao S, Xi T, Zhang Z (2013) Surface characterization of TEMPO-oxidized bacterial cellulose. Surf Interface Anal 45(11–12):1673–1679. https://doi.org/10.1002/sia.5306
Lansdown ABG (2006) Silver in health care: antimicrobial effects and safety in use. Curr Probl Dermatol 33:17–34. https://doi.org/10.1159/000093928
Lee KY, Buldum G, Mantalaris A, Bismarck A (2014) More than meets the eye in bacterial cellulose: biosynthesis, bioprocessing, and applications in advanced fiber composites. Macromol Biosci 14(1):10–32. https://doi.org/10.1002/mabi.201300298
Liau SY, Read DC, Pugh WJ, Furr JR, Russell AD (1997) Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett Appl Microbiol 25(4):279–283. https://doi.org/10.1046/j.1472-765X.1997.00219.x
Maneerung T, Tokura S, Rujiravanit R (2008) Impregnation of silver nanoparticles into bacterial cellulose for antimicrobial wound dressing. Carbohydr Polym 72(1):43–51. https://doi.org/10.1016/j.carbpol.2007.07.025
Maria LCS, Santos ALC, Oliveira PC, Valle ASS, Barud HS, Messaddeq Y, Ribeiro SJL (2010) Preparation and antibacterial activity of silver nanoparticles impregnated in bacterial cellulose. Polímeros 20(1):72–77. https://doi.org/10.1590/S0104-14282010005000001
Marini M, De Niederhausern S, Iseppi R, Bondi M, Sabia C, Toselli M, Pilati F (2007) Antibacterial activity of plastics coated with silver-doped organic–inorganic hybrid coatings prepared by sol–gel processes. Biomacromolecules 8(4):1246–1254. https://doi.org/10.1021/bm060721b
Matsumoto A, Ishikawa T, Odani T, Oikawa H, Okada S, Nakanishi H (2006) An organic/inorganic nanocomposite consisting of polymuconate and silver nanoparticles. Macromol Chem Phys 207(4):361–369. https://doi.org/10.1002/macp.200500430
Miao C, Hamad WY (2013) Cellulose reinforced polymer composites and nanocomposites: a critical review. Cellulose 20(5):2221–2262. https://doi.org/10.1007/s10570-013-0007-3
Milanović J, Mihajlovski K, Nikolić T, Kostić M (2016) Antimicrobial cotton fibers prepared by tempo-mediated oxidation and subsequent silver deposition. Cellul Chem Technol 50(910):905–914
Nimeskern L, Martínez Ávila H, Sundberg J, Gatenholm P, Müller R, Stok KS (2013) Mechanical evaluation of bacterial nanocellulose as an implant material for ear cartilage replacement. J Mech Behav Biomed Mater 22:12–21. https://doi.org/10.1016/j.jmbbm.2013.03.005
Pahlevan M, Toivakka M, Alam P (2018) Mechanical properties of TEMPO-oxidised bacterial cellulose-amino acid biomaterials. Eur Polym J 101:29–36. https://doi.org/10.1016/j.eurpolymj.2018.02.013
Patel I, Ludwig R, Haltrich D, Rosenau T, Potthast A (2011) Studies of the chemoenzymatic modification of cellulosic pulps by the laccase–TEMPO system. Holzforschung 65(4):475–481. https://doi.org/10.1515/HF.2011.035
Perala SRK, Kumar S (2013) On the mechanism of metal nanoparticle synthesis in the Brust–Schiffrin method. Langmuir 29(31):9863–9873. https://doi.org/10.1021/la401604q
Pinto RJB, Marques PAAP, Neto CP, Trindade T, Daina S, Sadocco P (2009) Antibacterial activity of nanocomposites of silver and bacterial or vegetable cellulosic fibers. Acta Biomater 5(6):2279–2289. https://doi.org/10.1016/j.actbio.2009.02.003
Quintana E, Roncero MB, Vidal T, Valls C (2017) Cellulose oxidation by laccase–TEMPO treatments. Carbohydr Polym 157:1488–1495. https://doi.org/10.1016/j.carbpol.2016.11.033
Rol F, Belgacem MN, Gandini A, Bras J (2019) Recent advances in surface-modified cellulose nanofibrils. Prog Polym Sci 88:241–264. https://doi.org/10.1016/j.progpolymsci.2018.09.002
Saito T, Isogai A (2004) TEMPO-mediated oxidation of native cellulose. The effect of oxidation conditions on chemical and crystal structures of the water-insoluble fractions. Biomacromolecules 5(5):1983–1989. https://doi.org/10.1021/bm0497769
Saito T, Isogai A (2005) A novel method to improve wet strength of paper. Tappi J 4(3):3–8
Saito T, Isogai A (2006) Introduction of aldehyde groups on surfaces of native cellulose fibers by TEMPO-mediated oxidation. Colloids Surf A 289(1–3):219–225. https://doi.org/10.1016/j.colsurfa.2006.04.038
Saito T, Shibata I, Isogai A, Suguri N, Sumikawa N (2005) Distribution of carboxylate groups introduced into cotton linters by the TEMPO-mediated oxidation. Carbohydr Polym 61(4):414–419. https://doi.org/10.1016/j.carbpol.2005.05.014
Scott WE (1996) Wet strength additives. In: Principles of wet end chemistry, pp 61–68. Retrieved from http://www.tappi.org/content/pdf/member_groups/paper/0101r241.pdf. Accessed 7 Jan 2019
Shao W, Liu H, Liu X, Sun H, Wang S, Zhang R (2015) pH-responsive release behavior and anti-bacterial activity of bacterial cellulose–silver nanocomposites. Int J Biol Macromol 76:209–217. https://doi.org/10.1016/j.ijbiomac.2015.02.048
Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for gram-negative bacteria. J Colloid Interface Sci 275(1):177–182. https://doi.org/10.1016/j.jcis.2004.02.012
Spence KL, Venditti RA, Habibi Y, Rojas OJ, Pawlak JJ (2010) The effect of chemical composition on microfibrillar cellulose films from wood pulps: mechanical processing and physical properties. Biores Technol 101(15):5961–5968. https://doi.org/10.1016/j.biortech.2010.02.104
Stumpf TR, Yang X, Zhang J, Cao X (2018) In situ and ex situ modifications of bacterial cellulose for applications in tissue engineering. Mater Sci Eng C 82:372–383. https://doi.org/10.1016/j.msec.2016.11.121
Tolvaj L, Faix O (1995) Artificial ageing of wood monitored by DRIFT spectroscopy and CIE L*a*b* color measurements 1. Effect of UV light. Holzforschung 49(5):397–404. https://doi.org/10.1515/hfsg.1995.49.5.397
Uddin KMA, Lokanathan AR, Liljeström A, Chen X, Rojas OJ, Laine J (2014) Silver nanoparticle synthesis mediated by carboxylated cellulose nanocrystals. Green Mater 2(4):183–192. https://doi.org/10.1680/gmat.14.00010
Ul-Islam M, Khan S, Ullah MW, Park JK (2015) Bacterial cellulose composites: synthetic strategies and multiple applications in bio-medical and electro-conductive fields. Biotechnol J 10(12):1847–1861. https://doi.org/10.1002/biot.201500106
Ullah H, Santos HA, Khan T (2016a) Applications of bacterial cellulose in food, cosmetics and drug delivery. Cellulose 23(4):2291–2314. https://doi.org/10.1007/s10570-016-0986-y
Ullah H, Wahid F, Santos HA, Khan T (2016b) Advances in biomedical and pharmaceutical applications of functional bacterial cellulose-based nanocomposites. Carbohydr Polym 150:330–352. https://doi.org/10.1016/j.carbpol.2016.05.029
Wu Q, Cao H, Luan Q, Zhang J, Wang Z, Warner JH, Watt AAR (2008) Biomolecule-assisted synthesis of water-soluble silver nanoparticles and their biomedical applications. Inorg Chem 47(13):5882–5888. https://doi.org/10.1021/ic8002228
Wu C-N, Fuh S-C, Lin S-P, Lin Y-Y, Chen H-Y, Liu J-M, Cheng K-C (2018a) TEMPO-oxidized bacterial cellulose pellicle with silver nanoparticles for wound dressing. Biomacromolecules 19(2):544–554. https://doi.org/10.1021/acs.biomac.7b01660
Wu Y, Wang F, Huang Y (2018b) Facile and simple fabrication of strong, transparent and flexible aramid nanofibers/bacterial cellulose nanocomposite membranes. Compos Sci Technol 159:70–76. https://doi.org/10.1016/j.compscitech.2018.02.036
Yang G, Xie J, Deng Y, Bian Y, Hong F (2012) Hydrothermal synthesis of bacterial cellulose/AgNPs composite: a “green” route for antibacterial application. Carbohydr Polym 87(4):2482–2487. https://doi.org/10.1016/j.carbpol.2011.11.017
Yano H, Sugiyama J, Nakagaito AN, Nogi M, Matsuura T, Hikita M, Handa K (2005) Optically transparent composites reinforced with networks of bacterial nanofibers. Adv Mater 17(2):153–155. https://doi.org/10.1002/adma.200400597
Zhou Y, Yu SH, Thomas A, Han BH (2003) In situ cyclodextrin-based homogeneous incorporation of metal (M = Pd, Pt, Ru) nanoparticles into silica with bimodal pore structure. Chem Commun 9(2):262–263. https://doi.org/10.1039/b210590j
Zhou Q, Zhang Q, Wang P, Deng C, Wang Q, Fan X (2017) Enhancement biocompatibility of bacterial cellulose membrane via laccase/TEMPO mediated grafting of silk fibroins. Fibers Polym 18(8):1478–1485. https://doi.org/10.1007/s12221-017-7306-5
Acknowledgments
This work was financed by the Spanish Ministry of Economy, Industry and Competitiveness, Grant ref. MICROBIOCEL: CTQ2017-84966-C2-1-R and CTQ2017-84966-C2-2-R Projects, FILMBIOCEL CTQ2016-77936-R (funding also from the “Fondo Europeo de Desarrollo Regional FEDER”), by the Pla de Recerca de Catalunya, Grant 2017SGR-30, and by the Generalitat de Catalunya, “Xarxa de Referència en Biotecnologia” (XRB). Special thanks are also due to the Serra Húnter Fellow to C. Valls.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Morena, A.G., Roncero, M.B., Valenzuela, S.V. et al. Laccase/TEMPO-mediated bacterial cellulose functionalization: production of paper-silver nanoparticles composite with antimicrobial activity. Cellulose 26, 8655–8668 (2019). https://doi.org/10.1007/s10570-019-02678-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10570-019-02678-5