Abstract
This study evaluates the capability of Komagataeibacter hansenii ATCC 23769 to synthesize bacterial nanocellulose (BNC) under strict limitation of nutrients with different carbon and nitrogen sources in a defined minimal culture medium in static culture. Five carbon sources were prepared based on the C-molar basis concentration: glycerol, glucose, fructose, mannitol and saccharose, combined with three different nitrogen sources: NH4Cl, NH4NO3 and (NH4)2SO4. BNC production yields were determined based on the dry weight of the produced BNC-Minimal membranes and the carbon consumption for each condition. The combination of 25 mM of glucose and 10 mM of NH4Cl showed the best concentration of C and N sources regarding BNC yield and membrane stability. This is a new proposal of defined minimal culture medium that supports growth of BNC membranes production, without the addition of complex elements such as yeast extract and peptone. BNC membranes produced under these conditions exhibited great optical transparency compared to the membranes produced in complex media (Mannitol and Hestrin–Schramm), therefore increasing a wide range of technological applications.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Azeredo J, Oliveira R (1996) A new method for precipitating bacterial exopolysaccharides. Biotechnol Tech 10:341–344. https://doi.org/10.1007/BF00173251
Berti FV, Rambo CR, Dias PF, Porto LM (2013) Nanofiber density determines endothelial cell behavior on hydrogel matrix. Mater Sci Eng C 33:4684–4691
Brown AJ (1886) XIX.-The chemical action of pure cultivations of bacterium aceti. J Chem Soc Trans 49:172–187. https://doi.org/10.1039/CT8864900172
Caiut JMA, Barud H da S, Messaddeq Y et al (2011) Optically transparent composites based on bacterial cellulose and boehmite, siloxane and/or a boehmite- siloxane system. BR Patent, WO/2012/100315, 2 Aug 2012
Castro C, Zuluaga R, Putaux J-L et al (2011) Structural characterization of bacterial cellulose produced by Gluconacetobacter swingsii sp. from Colombian agroindustrial wastes. Carbohydr Polym 84:96–102. https://doi.org/10.1016/j.carbpol.2010.10.072
Chawla PR, Bajaj IB, Survase SA, Singhal RS (2009) Microbial cellulose: fermentative production and applications. Food Technol Biotechnol 47:107–124
Chernoviz PLN (1996) Farmacopéia Brasileira. Editora Itatiaia Ltda, Rio de Janeiro
Czaja W, Romanovicz D, Brown RM (2004) Structural investigations of microbial cellulose produced in stationary and agitated culture. Cellulose 11:403–411. https://doi.org/10.1023/B:CELL.0000046412.11983.61
Dagang L, Qiaoyun D, Yan L (2013) Bacterial cellulose nanometer optical transparent film preparation method. CN Patent, CN103396569A, 20 Nov 2013
Dahman Y, Jayasuriya KE, Kalis M (2010) Potential of biocellulose nanofibers production from agricultural renewable resources: preliminary study. Appl Biochem Biotechnol 162:1647–1659. https://doi.org/10.1007/s12010-010-8946-8
Feng H, Xue ZY, Guang Y, Xia YX (2011) Wheat straw acid hydrolysate as a potential cost-effective feedstock for production of bacterial cellulose. J Chem Technol Biotechnol 86:675–680. https://doi.org/10.1002/jctb.2567
Forng ER, Anderson SM, Cannon RE (1989) Synthetic medium for Acetobacter xylinum that can be used for isolation of auxotrophic mutants and study of cellulose biosynthesis. Appl Environ Microbiol 55:1317–1319
Fu L, Zhang J, Yang G (2013) Present status and applications of bacterial cellulose-based materials for skin tissue repair. Carbohydr Polym 92:1432–1442. https://doi.org/10.1016/j.carbpol.2012.10.071
Gomes FP, Silva NHCS, Trovatti E et al (2013) Production of bacterial cellulose by Gluconacetobacter sacchari using dry olive mill residue. Biomass Bioenerg 55:205–211. https://doi.org/10.1016/j.biombioe.2013.02.004
Hong F, Wei B, Chen L (2015) Preliminary study on biosynthesis of bacterial nanocellulose tubes in a novel double-silicone-tube bioreactor for potential vascular prosthesis. Biomed Res Int. https://doi.org/10.1155/2015/560365
Hwang JW, Yang YK, Hwang JK et al (1999) Effects of pH and dissolved oxygen on cellulose production by Acetobacter xylinum BRC5 in agitated culture. J Biosci Bioeng 88:183–188. https://doi.org/10.1016/S1389-1723(99)80199-6
Iguchi M, Yamanaka S, Budhiono A (2000) Bacterial cellulose—a masterpiece of nature’s arts. J Mater Sci 35:261–270
Jonas R, Farah LF (1998) Production and application of microbial cellulose. Polym Degrad Stab 59:101–106. https://doi.org/10.1016/S0141-3910(97)00197-3
Jozala AF, de Lencastre-Novaes LC, Lopes AM et al (2016) Bacterial nanocellulose production and application: a 10-year overview. Appl Microbiol Biotechnol 100:2063–2072
Jung H-I, Lee O-M, Jeong J-H et al (2010) Production and characterization of cellulose by Acetobacter sp. V6 using a cost-effective molasses-corn steep liquor medium. Appl Biochem Biotechnol 162:486–497. https://doi.org/10.1007/s12010-009-8759-9
Keshk SMAS (2014) Bacterial cellulose production and its industrial applications. J Bioprocess Biotech 04:1–10. https://doi.org/10.4172/2155-9821.1000150
Keshk SMAS, Sameshima K (2005) Evaluation of different carbon sources for bacterial cellulose production. Afr J Biotechnol 4:478–482
Khoda AKMB, Koc B (2013) Functionally heterogeneous porous scaffold design for tissue engineering. Comput Des 45:1276–1293. https://doi.org/10.1016/j.cad.2013.05.005
Klemm D, Heublein B, Fink H-P, Bohn A (2005) Cellulose: fascinating biopolymer and sustainable raw material. Angew Chemie Int Ed 44:3358–3393. https://doi.org/10.1002/anie.200460587
Kongruang S (2008) Bacterial cellulose production by Acetobacter xylinum strains from agricultural waste products. Appl Biochem Biotechnol 148:245. https://doi.org/10.1007/s12010-007-8119-6
Kumar RR, Prasad S (2011) Metabolic engineering of bacteria. Indian J Microbiol 51:403–409. https://doi.org/10.1007/s12088-011-0172-8
Kurosumi A, Sasaki C, Yamashita Y, Nakamura Y (2009) Utilization of various fruit juices as carbon source for production of bacterial cellulose by Acetobacter xylinum NBRC 13693. Carbohydr Polym 76:333–335. https://doi.org/10.1016/j.carbpol.2008.11.009
Legnani C, Vilani C, Calil VL et al (2008) Bacterial cellulose membrane as flexible substrate for organic light emitting devices. Thin Solid Films 517:1016–1020. https://doi.org/10.1016/j.tsf.2008.06.011
Li Y, Wang S, Huang R et al (2015) Evaluation of the effect of the structure of bacterial cellulose on full thickness skin wound repair on a microfluidic chip. Biomacromol 16:780–789. https://doi.org/10.1021/bm501680s
Liu M, Zhong C, Zhang YM et al (2016) Metabolic investigation in Gluconacetobacter xylinus and its bacterial cellulose production under a direct current electric field. Front Microbiol 7:331. https://doi.org/10.3389/fmicb.2016.00331
Luo H, Zhang J, Xiong G, Wan Y (2014) Evolution of morphology of bacterial cellulose scaffolds during early culture. Carbohydr Polym 111:722–728
Masaoka S, Ohe T, Sakota N (1993) Production of cellulose from glucose by Acetobacter xylinum. J Ferment Bioeng 75:18–22. https://doi.org/10.1016/0922-338X(93)90171-4
Matsuoka M, Tsuchida T, Matsushita K et al (1996) A synthetic medium for bacterial cellulose production by Acetobacter xylinum subsp. sucrofermentans. Biosci Biotechnol Biochem 60:575–579. https://doi.org/10.1271/bbb.60.575
Metcalfe AD, Ferguson MWJ (2007) Tissue engineering of replacement skin: the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration. J R Soc Interface 4:413–437. https://doi.org/10.1098/rsif.2006.0179
Mikkelsen D, Flanagan BM, Dykes GA, Gidley MJ (2009) Influence of different carbon sources on bacterial cellulose production by Gluconacetobacter xylinus strain ATCC 53524. J Appl Microbiol 107:576–583. https://doi.org/10.1111/j.1365-2672.2009.04226.x
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor, New York
Muller D, Rambo CR, Porto LM et al (2013) Structure and properties of polypyrrole/bacterial cellulose nanocomposites. Carbohydr Polym 94:655–662. https://doi.org/10.1016/j.carbpol.2013.01.041
Niaounakis M (2015a) Medical, dental, and pharmaceutical applications. In: Jackson D (eds) Biopolymers: applications and trends, 1st edn. William Andrew Publishing, Oxford, pp 291–405
Niaounakis M (2015b) Electronics. In: Jackson D (eds) Biopolymers: applications and trends, 1st edn. William Andrew Publishing, Oxford, pp 233–255
O’Neill H, Pingali SV, Petridis L et al (2017) Dynamics of water bound to crystalline cellulose. Sci Rep 7:11840. https://doi.org/10.1038/s41598-017-12035-w
Oikawa T, Ohtori T, Ameyama M (1995) Production of cellulose from D-Mannitol by Acetobacter xylinum KU-1. Biosci Biotechnol Biochem 59:331–332. https://doi.org/10.1271/bbb.59.331
Pickens LB, Tang Y, Chooi Y-H (2011) Metabolic engineering for the production of natural products. Annu Rev Chem Biomol Eng 2:211–236. https://doi.org/10.1146/annurev-chembioeng-061010-114209
Ramana K, Tomar A, Singh L (2000) Effect of various carbon and nitrogen sources on cellulose synthesis by Acetobacter xylinum. World J Microbiol Biotechnol 16:245–248
Ross P, Mayer R, Benziman M (1991) Cellulose biosynthesis and function in bacteria. Microbiol Rev 55:35–58. https://doi.org/10.1016/j.bbalip.2012.08.009
Ruka DR, Simon GP, Dean KM (2012) Altering the growth conditions of Gluconacetobacter xylinus to maximize the yield of bacterial cellulose. Carbohydr Polym 89:613–622
Santos SM, Carbajo JM, Villar J (2013) The effect of carbon and nitrogen sources on bacterial cellulose production and properties from Gluconacetobacter sucrofermentans CECT 7291 focused on its use in degraded paper restoration. BioResources 8:3630–3645
Saska S, Teixeira LN, Tambasco de Oliveira P et al (2012) Bacterial cellulose-collagen nanocomposite for bone tissue engineering. J Mater Chem 22:22102–22112. https://doi.org/10.1039/C2JM33762B
Saxena IM, Brown RM (2012) Biosynthesis of bacterial cellulose. In: Gama M, Gatenholm P, Klemm D (eds) Bacterial nanocellulose: a sophisticated multifunctional material. CRC, Boca Raton, pp 1–18
Schramm M, Hestrin S (1954) Factors affecting production of cellulose at the air/ liquid interface of a culture of Acetobacter xylinum. J Gen Microbiol 11:123–129. https://doi.org/10.1099/00221287-11-1-123
Shoda M, Sugano Y (2005) Recent advances in bacterial cellulose production. Biotechnol Bioprocess Eng 10:1. https://doi.org/10.1007/BF02931175
Son H-J, Kim H-G, Kim K-K et al (2003) Increased production of bacterial cellulose by Acetobacter sp. V6 in synthetic media under shaking culture conditions. Bioresour Technol 86:215–219. https://doi.org/10.1016/S0960-8524(02)00176-1
Souza SS, Castro JV, Porto LM (2018) Modeling the core metabolism of Komagataeibacter hansenii ATCC 23769 to evaluate nanocellulose biosynthesis. Braz J Chem Eng 35(3) (in press)
Suwanposri A, Yukphan P, Yamada Y, Ochaikul D (2013) Identification and biocellulose production of Gluconacetobacter strains isolated from tropical fruits in thailand. Maejo Int J Sci Technol 7:70–82
Svensson A, Nicklasson E, Harrah T et al (2005) Bacterial cellulose as a potential scaffold for tissue engineering of cartilage. Biomaterials 26:419–431
Tabaii MJ, Emtiazi G (2016) Comparison of bacterial cellulose production among different strains and fermented media. Appl Food Biotechnol 3:35–41
Tam RY, Fisher SA, Baker AEG, Shoichet MS (2016) Transparent porous polysaccharide cryogels provide biochemically defined, biomimetic matrices for tunable 3D cell culture. Chem Mater 28:3762–3770. https://doi.org/10.1021/acs.chemmater.6b00627
Tazi N, Zhang Z, Messaddeq Y et al (2012) Hydroxyapatite bioactivated bacterial cellulose promotes osteoblast growth and the formation of bone nodules. AMB Express 2:61. https://doi.org/10.1186/2191-0855-2-61
Torres FG, Commeaux S, Troncoso OP (2012) Biocompatibility of bacterial cellulose based biomaterials. J Funct Biomater 3:864–878
Tyagi N, Suresh S (2016) Production of cellulose from sugarcane molasses using Gluconacetobacter intermedius SNT-1: optimization & characterization. J Clean Prod 112, Part 1:71–80. https://doi.org/10.1016/j.jclepro.2015.07.054
Ummartyotin S, Juntaro J, Sain M, Manuspiya H (2012) Development of transparent bacterial cellulose nanocomposite film as substrate for flexible organic light emitting diode (OLED) display. Ind Crops Prod 35:92–97. https://doi.org/10.1016/j.indcrop.2011.06.025
Valepyn E, Berezina N, Paquot M (2012) Optimization of Production and preliminary characterization of new exopolysaccharides from Gluconacetobacter hansenii LMG1524. Adv Microbiol 02:488–496
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
Velasco-Bedrán H, López-Isunza F (2007) The unified metabolism of Gluconacetobacter entanii in continuous and batch processes. Process Biochem 42:1180–1190
Xinsheng L, Wankei W, Chandrakant JP (2009) Transparent bacterial cellulose nanocomposite biofilms. US Patent, 929US20130011385, 10 Jan 2013
Wilson SA, Roberts SC (2014) Metabolic engineering approaches for production of biochemicals in food and medicinal plants. Curr Opin Biotechnol 26:174–182. https://doi.org/10.1016/j.copbio.2014.01.006
Yim SM, Song JE, Kim HR (2016) Production and characterization of bacterial cellulose fabrics by nitrogen sources of tea and carbon sources of sugar. Process Biochem 59, Part A:26–36. https://doi.org/10.1016/j.procbio.2016.07.001
Yodsuwan N, Owatworakit A, Ngaokla A et al (2012) Effect of carbon and nitrogen sources on bacterial cellulose production for bionanocomposite materials. In: 1st MFUIC 2012. Mae Fah Luang University, Chiang Rai, Thailand. https://www.researchgate.net/publication/280730054. Accessed 02 April 2018
Yongjun Z, Yang H, Xin Z et al (2015) Transparent reproductive bacterial cellulose reproductive membrane as well as preparation method and application thereof. CN Patent, CN104587516, 06 May 2014
Zeng X, Small DP, Wan W (2011) Statistical optimization of culture conditions for bacterial cellulose production by Acetobacter xylinum BPR 2001 from maple syrup. Carbohydr Polym 85:506–513. https://doi.org/10.1016/j.carbpol.2011.02.034
Zhang J, Greasham R (1999) Chemically defined media for commercial fermentations. Appl Microbiol Biotechnol 51:407–421. https://doi.org/10.1007/s002530051411
Zhu J, Marchant RE (2011) Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Devices 8:607–626. https://doi.org/10.1586/erd.11.27
Acknowledgments
The authors thank the National Council for the Improvement of Higher Education (CAPES), for the financial support. The authors also thank the Central Laboratory of Electronic Microscopy at Federal University of Santa Catarina (LCME/UFSC) and the Analytical Center of the Chemical and Food Engineering Department (EQA/UFSC).
Funding
Funding was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Grant No. 1407463/2014-1) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant No. 402901/2013-4).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors have agreed to submit the manuscript to the Cellulose. The authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
de Souza, S.S., Berti, F.V., de Oliveira, K.P.V. et al. Nanocellulose biosynthesis by Komagataeibacter hansenii in a defined minimal culture medium. Cellulose 26, 1641–1655 (2019). https://doi.org/10.1007/s10570-018-2178-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10570-018-2178-4