Abstract
The aim of this study was to assess the immobilization pattern of microorganisms characterized by varying cell shapes and sizes (rod-shaped bacteria Lactobacillus delbruecki, spherical-shaped yeast Saccharomyces cerevisiae and hyphae forms of Yarrowia lipolytica) on bacterial cellulose of various material properties. The ‘adsorption-incubation’ method was used for the purposes of immobilization. The immobilization pattern included adsorption efficiency, ability of the immobilized cells to multiply within the carrier expressed as incubation efficiency and the degree of release of the immobilized cells from the carrier. The efficiency of adsorption and incubation was affected by the morphology of the immobilized cells and increased together with cellulose surface area. For smaller bacterial cells a higher level of loading was obtained on the same surface as compared to larger yeast cells. During incubation, the number of immobilized bacterial and yeast cells increased significantly in comparison to the number of cells adsorbed on the carrier during the adsorption step. Despite the morphological differences between the S. cerevisiae and Y. lipolytica cells, there were no statistically significant differences in the efficiency of adsorption and incubation. It was also revealed that the release ratio values obtained for L. delbruecki and S. cerevisiae increased along with cellulose surface area. Interestingly, Y. lipolytica cells in the pseudohyphae and hyphae forms penetrated deeply into the three-dimensional network of BC nanofibrils which prevented subsequent cell release. It was confirmed that carrier selection must be individually matched to the type of immobilized cells based especially on its porosity-related parameters.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barth G, Gaillardin C (1997) Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol Rev 19:219–237. https://doi.org/10.1111/j.1574-6976.1997.tb00299.x
Braga A, Belo I (2013) Immobilization of Yarrowia lipolytica for aroma production from castor oil. Appl Biochem Biotechnol 169:2202–2211. https://doi.org/10.1007/s12010-013-0131-4
Chandel AK, Narasu ML, Chandrasekhar G, Manikyam A, Rao LV (2009) Use of Saccharum spontaneum (wild sugarcane) as biomaterial for cell immobilization and modulated ethanol production by thermotolerant Saccharomyces cerevisiae. Bioresour Technol 100:2404–2410. https://doi.org/10.1016/j.biortech.2008.11.014
Chavarri M, Maranon I, Villaran MC (2012) Encapsulation technology to protect probiotic bacteria. In: Rigobelo EC (ed) Probiotics, UNESP, Brazil, pp 501–540
Drozd R, Rakoczy R, Wasak A, Junka A, Fijałkowski K (2018) The application of magnetically modified bacterial cellulose for immobilization of laccase. Int J Biol Macromol 108:462–470. https://doi.org/10.1016/j.ijbiomac.2017.12.031
Fijałkowski K, Peitler D, Rakoczy R, Żywicka A (2016a) Survival of probiotic lactic acid bacteria immobilized in different forms of bacterial cellulose in simulated gastric juices and bile salt solution. LWT Food Sci Technol 68:322–328. https://doi.org/10.1016/j.lwt.2015.12.038
Fijałkowski K, Żywicka A, Drozd R, Kordas M, Rakoczy R (2016b) Effect of Gluconacetobacter xylinus cultivation conditions on the selected properties of bacterial cellulose. Pol J Chem Technol 18:116–122. https://doi.org/10.1515/pjct-2016-0080
Fijałkowski K, Żywicka A, Drozd R, Junka AF, Peitler D, Kordas M, Konopacki M, Szymczyk P, Rakoczy R (2017) Increased water content in bacterial cellulose synthesized under rotating magnetic fields. Electromagn Biol Med 36:192–201. https://doi.org/10.1080/15368378.2016.1243554
Förster M, Mansfield J, Schellenberger A, Dautzenberg H (1994) Immobilization of citrate-producing Yarrowia lipolytica cells in polyelectrolyte complex capsules. Enzyme Microb Technol 16:777–784
Górecka E, Jastrzębska M (2011) Immobilization techniques and biopolymer carriers. Biotechnol Food Sci 75:65–86
Hornung M, Ludwig M, Gerrard AM, Schmauder HP (2006) Optimizing the production of bacterial cellulose in surface culture: Evaluation of substrate mass transfer influences on the bioreaction (Part 1). Eng Life Sci 6:537–545. https://doi.org/10.1002/elsc.200620162
Johnson EA, Echavarri-Erasun C (2011) Yeast biotechnology. In: Kurtzman C, Fell JW, Boekhout T (ed) The yeasts, 5. Elsevier, New York, pp 21–44
Junka A, Fijałkowski K, Ząbek A, Mikołajewicz K, Chodaczek G, Szymczyk P, Smutnicka D, Żywicka A, Sedghizadeh PP, Dziadas M, Młynarz P, Bartoszewicz M (2017) Correlation between type of alkali rinsing, cytotoxicity of bio-nanocellulose and presence of metabolites within cellulose membranes. Carbohydr Polym 157:371–379. https://doi.org/10.1016/j.carbpol.2016.10.007
Keshk S (2014) Bacterial cellulose production and its industrial applications. J Bioprocess Biotech 4:1360–1401. https://doi.org/10.4172/2155-9821.1000150
Kim J, Cai ZJ, Lee HS, Choi GS, Lee DH, Jo C (2010) Preparation and characterization of a bacterial cellulose/chitosan composite for potential biomedical application. J Polym Res 18:739–744. https://doi.org/10.1002/app.38396
Klein J, Ziehr H (1990) Immobilization of microbial cells by adsorption. J Biotechnol 16:1–16. https://doi.org/10.1016/0168-1656(90)90061-F
Kourkoutas Y, Bekatorou A, Banat IM, Marchant R, Koutinas AA (2004) Immobilization technologies and support materials suitable in alcohol beverages production: a review. Food Microbiol 21:377–397. https://doi.org/10.1016/j.fm.2003.10.005
Krystynowicz A, Czaja W, Wiktorowska-Jezierska A, Goncalves-Miskiewicz M, Turkiewicz M, Bielecki S (2002) Factors affecting the yield and properties of bacterial cellulose. J Ind Microbiol Biotechnol 29:189–195. https://doi.org/10.1038/sj.jim.7000303
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
Nguyen DN, Ton NMN, Le VVM (2009) Optimization of Saccharomyces cerevisiae immobilization in bacterial cellulose by ‘adsorption-incubation’ method. Int Food Res J 16:59–64
Rezaee A, Godini H, Bakhtou H (2008) Microbial cellulose as support material for the immobilization of denitrifying bacteria. Environ Eng Manag J 7:589–594
Spencer JFT, Ragout de Spencer AL, Laluce C (2002) Non-conventional yeasts. Appl Microbiol Biotechnol 58:147–156. https://doi.org/10.1007/s00253-001-0834-2
Strehaiano P, Ramon-Portugal F, Taillandier P (2006) Yeasts as biocatalysts. In: Querol A, Fleet G (ed) Yeasts in food and beverages. Springer, New York, pp. 243–284
Tam TTM, Huong NT (2014) Optimization of Corynebacterium glutamicum immobilization process on bacterial cellulose carrier and its application for lysine fermentation. IOSR J Eng 4:33–38
Tang W, Jia S, Jia Y, Yang H (2010) The influence of fermentation conditions and post-treatment methods on porosity of bacterial cellulose membrane. World J Microbiol Biotechnol 26:125–131. https://doi.org/10.1007/s11274-009-0151-y
Ton NMN, Le VVM (2011) Application of immobilized yeast in bacterial cellulose to the repeated batch fermentation in wine-making. Int Food Res J 18:983–987
Vega R, Domínguez A (1986) Cell wall composition of the yeast and mycelial forms of Yarrowia lipolytica. Arch Microbiol 144:124–130
Volkov V (2015) Quantitative description of ion transport via plasma membrane of yeast and small cells. Front Plant Sci 6:425–428. https://doi.org/10.3389/fpls.2015.00425
Wu S-C, Lia J-K (2008) Application of bacterial cellulose pellets in enzyme immobilization. J Mol Catal B 54:103–108. https://doi.org/10.1016/j.molcatb.2007.12.021
Yao W, Wu X, Zhu J, Sun B, Zhang YY, Miller C (2011) Bacterial cellulose membrane—a new support carrier for yeast immobilization for ethanol fermentation. Process Biochem 46:2054–2058. https://doi.org/10.1016/j.procbio.2011.07.006
Żur J, Wojcieszyńska D, Guzik U (2016) Metabolic responses of bacterial cells to immobilization. Molecules 21:958. https://doi.org/10.3390/molecules21070958
Żywicka A, Peitler D, Rakoczy R, Junka AF, Fijałkowski K (2016) Wet and dry forms of bacterial cellulose synthetized by different strains of Gluconacetobacter xylinus as carriers for yeast immobilization. Appl Biochem Biotechnol 180:805–881. https://doi.org/10.1007/s12010-016-2134-4
Żywicka A, Fijałkowski K, Junka A, Grzesiak J, El Fray M (2018) Modification of bacterial cellulose with quaternary ammonium compounds based on fatty acids and amino acids and the effect on antimicrobial activity. Biomacromolecules 19:1528–1538. https://doi.org/10.1021/acs.biomac.8b00183
Acknowledgements
The authors would like to thank the Dean of the Faculty of Biotechnology and Animal Husbandry (Grant No. 517-01-027-3323/17) and the National Centre for Research and Development in Poland (Grant No. LIDER/011/221/L-5/13/NCBR/2014) for providing financial support to this work.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Żywicka, A., Wenelska, K., Junka, A. et al. Immobilization pattern of morphologically different microorganisms on bacterial cellulose membranes. World J Microbiol Biotechnol 35, 11 (2019). https://doi.org/10.1007/s11274-018-2584-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-018-2584-7