Improving the Viability of Probiotics under Harsh Conditions by the Formation of Biofilm on Electrospun Nanofiber Mat
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Preparation of Nanofiber Mat
2.3. Characterization of Nanofiber Mats
2.4. Biofilm Formation and Characterization
2.5. Quantitation of Sessile Cells in Biofilms
2.6. Impact of Growth Conditions on the Formation of Biofilms
2.7. In Vitro Gastrointestinal Tolerance of Biofilm
2.8. Thermal Tolerance of Biofilm
2.9. RT-qPCR Assay
2.10. Statistical Analysis
3. Results and Discussion
3.1. Biofilm Formation on the EC Nanofiber Mat
3.2. Effects of Media on Biofilm Formation
3.3. Impact of Culture Conditions on the Formation of Biofilms
3.4. Sessile Cells’ Survival against Environmental Stresses
3.5. luxS Expression
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Gareau, M.G.; Sherman, P.M.; Walker, W.A. Probiotics and the gut microbiota in intestinal health and disease. Nat. Rev. Gastroenterol. Hepatol. 2010, 7, 503–514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duongthingoc, D.; George, P.; Katopo, L.; Gorczyca, E.; Kasapis, S. Effect of whey protein agglomeration on spray dried microcapsules containing Saccharomyces boulardii. Food Chem. 2013, 141, 1782–1788. [Google Scholar] [CrossRef] [PubMed]
- Feng, K.; Huang, R.M.; Wu, R.Q.; Wei, Y.S.; Zong, M.H.; Linhardt, R.J.; Wu, H. A novel route for double-layered encapsulation of probiotics with improved viability under adverse conditions. Food Chem. 2020, 310, 125977. [Google Scholar] [CrossRef] [PubMed]
- Sousa, S.; Gomes, A.M.; Pintado, M.M.; Silva, J.P.; Costa, P.; Amaral, M.H.; Duarte, A.C.; Rodrigues, D.; Rocha-Santos, T.A.P.; Freitas, A.C. Characterization of freezing effect upon stability of, probiotic loaded, calcium-alginate microparticles. Food Bioprod. Process. 2015, 93, 90–97. [Google Scholar] [CrossRef]
- Terpou, A.; Papadaki, A.; Lappa, I.K.; Kachrimanidou, V.; Bosnea, L.A.; Kopsahelis, N.J.N. Probiotics in Food Systems: Significance and Emerging Strategies Towards Improved Viability and Delivery of Enhanced Beneficial Value. Nutrients 2019, 11, 1591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, L.; Zhang, Y.; Guo, X.; Zhang, L.; Zhang, W.; Man, C.; Jiang, Y. Characterization and transcriptomic basis of biofilm formation by Lactobacillus plantarum J26 isolated from traditional fermented dairy products. LWT Food Sci. Technol. 2020, 125, 109333. [Google Scholar] [CrossRef]
- Hu, M.X.; Li, J.N.; Guo, Q.; Zhu, Y.Q.; Niu, H.M. Probiotics Biofilm-Integrated Electrospun Nanofiber Membranes: A New Starter Culture for Fermented Milk Production. J. Agric. Food Chem. 2019, 67, 3198–3208. [Google Scholar] [CrossRef]
- Cheow, W.S.; Kiew, T.Y.; Hadinoto, K. Controlled release of Lactobacillus rhamnosus biofilm probiotics from alginate-locust bean gum microcapsules. Carbohydr. Polym. 2014, 103, 587–595. [Google Scholar] [CrossRef]
- He, C.; Sampers, I.; Van De Walle, D.; Dewettinck, K.; Raes, K. Encapsulation of Lactobacillus in Low-Methoxyl Pectin-Based Microcapsules Stimulates Biofilm Formation: Enhanced Resistances to Heat Shock and Simulated Gastrointestinal Digestion. J. Agric. Food Chem. 2021, 69, 6281–6290. [Google Scholar] [CrossRef]
- Jingjing, E.; Rongze, M.; Zichao, C.; Caiqing, Y.; Ruixue, W.; Qiaoling, Z.; Zongbai, H.; Ruiyin, S.; Junguo, W. Improving the freeze-drying survival rate of Lactobacillus plantarum LIP-1 by increasing biofilm formation based on adjusting the composition of buffer salts in medium. Food Chem. 2021, 338, 128134. [Google Scholar] [CrossRef]
- Muffler, K.; Lakatos, M.; Schlegel, C.; Strieth, D.; Kuhne, S.; Ulber, R. Application of biofilm bioreactors in white biotechnology. Adv. Biochem. Eng. Biotechnol. 2014, 146, 123–161. [Google Scholar] [PubMed]
- Liu, W.; Lipner, J.; Xie, J.; Manning, C.N.; Thomopoulos, S.; Xia, Y. Nanofiber scaffolds with gradients in mineral content for spatial control of osteogenesis. ACS Appl. Mater. Interfaces 2014, 6, 2842–2849. [Google Scholar] [CrossRef] [PubMed]
- Speranza, B.; Corbo, M.R.; Campaniello, D.; Altieri, C.; Sinigaglia, M.; Bevilacqua, A. Biofilm formation by potentially probiotic Saccharomyces cerevisiae strains. Food Microbiol. 2020, 87, 103393. [Google Scholar] [CrossRef] [PubMed]
- Speranza, B.; Corbo, M.R.; Sinigaglia, M. Effects of nutritional and environmental conditions on Salmonella sp. biofilm formation. J. Food Sci. 2011, 76, 12–16. [Google Scholar] [CrossRef] [PubMed]
- Feng, K.; Zhai, M.Y.; Zhang, Y.; Linhardt, R.J.; Zong, M.H.; Li, L.; Wu, H. Improved Viability and Thermal Stability of the Probiotics Encapsulated in a Novel Electrospun Fiber Mat. J. Agric. Food Chem. 2018, 66, 10890–10897. [Google Scholar] [CrossRef] [PubMed]
- Valamehr, B.; Jonas, S.J.; Polleux, J.; Qiao, R.; Guo, S.; Gschweng, E.H.; Stiles, B.; Kam, K.; Luo, T.J.; Witte, O.N.; et al. Hydrophobic surfaces for enhanced differentiation of embryonic stem cell-derived embryoid bodies. Proc. Natl. Acad. Sci. USA 2008, 105, 14459–14464. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ong, Y.L.; Razatos, A.; Georgiou, G.; Sharma, M.M. Adhesion forces between E-coli bacteria and biomaterial surfaces. Langmuir 1999, 15, 2719–2725. [Google Scholar] [CrossRef]
- Anselme, K.; Davidson, P.; Popa, A.M.; Giazzon, M.; Liley, M.; Ploux, L. The interaction of cells and bacteria with surfaces structured at the nanometre scale. Acta Biomater. 2010, 6, 3824–3846. [Google Scholar] [CrossRef]
- Quirynen, M.; Bollen, C.M.; Papaioannou, W.; Van Eldere, J.; Van Steenberghe, D. The influence of titanium abutment surface roughness on plaque accumulation and gingivitis: Short-term observations. Int. J. Oral Maxillofac. Implants 1996, 11, 169–178. [Google Scholar]
- Terraf, M.C.; Juarez Tomas, M.S.; Nader-Macias, M.E.; Silva, C. Screening of biofilm formation by beneficial vaginal lactobacilli and influence of culture media components. J. Appl. Microbiol. 2012, 113, 1517–1529. [Google Scholar] [CrossRef]
- Perez Ibarreche, M.; Castellano, P.; Vignolo, G. Evaluation of anti-Listeria meat borne Lactobacillus for biofilm formation on selected abiotic surfaces. Meat Sci. 2014, 96, 295–303. [Google Scholar] [CrossRef] [PubMed]
- Emanuel, V.; Adrian, V.; Diana, P. Microbial Biofilm Formation under the Influence of Various Physical-Chemical Factors. Biotechnol. Biotechnol. Equip. 2010, 24, 1993–1996. [Google Scholar] [CrossRef]
- Rode, T.M.; Langsrud, S.; Holck, A.; Moretro, T. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int. J. Food Microbiol. 2007, 116, 372–383. [Google Scholar] [CrossRef] [PubMed]
- Muruzovic, M.Z.; Mladenovic, K.G.; Comic, L.R. In vitro evaluation of resistance to environmental stress by planktonic and biofilm form of lactic acid bacteria isolated from traditionally made cheese from Serbia. Food Biosci. 2018, 23, 54–59. [Google Scholar] [CrossRef]
- Huang, R.M.; Feng, K.; Li, S.F.; Zong, M.H.; Wu, H.; Han, S.Y. Enhanced survival of probiotics in the electrosprayed microcapsule by addition of fish oil. J. Food Eng. 2021, 307, 110650. [Google Scholar] [CrossRef]
- Cheow, W.S.; Hadinoto, K. Biofilm-like Lactobacillus rhamnosus probiotics encapsulated in alginate and carrageenan microcapsules exhibiting enhanced thermotolerance and freeze-drying resistance. Biomacromolecules 2013, 14, 3214–3222. [Google Scholar] [CrossRef]
- Lebeer, S.; De Keersmaecker, S.C.; Verhoeven, T.L.; Fadda, A.A.; Marchal, K.; Vanderleyden, J. Functional analysis of luxS in the probiotic strain Lactobacillus rhamnosus GG reveals a central metabolic role important for growth and biofilm formation. J. Bacteriol. 2007, 189, 860–871. [Google Scholar] [CrossRef] [Green Version]
- Lebeer, S.; Claes, I.J.; Verhoeven, T.L.; Shen, C.; Lambrichts, I.; Ceuppens, J.L.; Vanderleyden, J.; De Keersmaecker, S.C. Impact of luxS and suppressor mutations on the gastrointestinal transit of Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 2008, 74, 4711–4718. [Google Scholar] [CrossRef] [Green Version]
- Sun, Z.; He, X.; Brancaccio, V.F.; Yuan, J.; Riedel, C.U. Bifidobacteria exhibit LuxS-dependent autoinducer 2 activity and biofilm formation. PLoS ONE 2014, 9, e88260. [Google Scholar] [CrossRef] [Green Version]
- Olszewska, M.A.; Nynca, A.; Bialobrzewski, I. Biofilm formation by lactobacilli and resistance to stress treatments. Int. J. Food Sci. Technol. 2019, 54, 3058–3065. [Google Scholar] [CrossRef]
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Shi, J.; Li, S.-F.; Feng, K.; Han, S.-Y.; Hu, T.-G.; Wu, H. Improving the Viability of Probiotics under Harsh Conditions by the Formation of Biofilm on Electrospun Nanofiber Mat. Foods 2022, 11, 1203. https://0-doi-org.brum.beds.ac.uk/10.3390/foods11091203
Shi J, Li S-F, Feng K, Han S-Y, Hu T-G, Wu H. Improving the Viability of Probiotics under Harsh Conditions by the Formation of Biofilm on Electrospun Nanofiber Mat. Foods. 2022; 11(9):1203. https://0-doi-org.brum.beds.ac.uk/10.3390/foods11091203
Chicago/Turabian StyleShi, Jiao, Shu-Fang Li, Kun Feng, Shuang-Yan Han, Teng-Gen Hu, and Hong Wu. 2022. "Improving the Viability of Probiotics under Harsh Conditions by the Formation of Biofilm on Electrospun Nanofiber Mat" Foods 11, no. 9: 1203. https://0-doi-org.brum.beds.ac.uk/10.3390/foods11091203