Exopolysaccharides from Lactic Acid Bacteria: Functional Properties and Effects on Yogurt Texture

Abstract

Exopolysaccharides (EPS) are polysaccharides synthesized extracellularly by microorganisms and have positive effects on health. Exopolysaccharides produced even at low concentrations have the effect of improving the structure of food products. Thus, it is possible to meet the needs and demands of consumers by developing the textural feature of the final product as desired without using any additives, as well as positive benefits for human health. The number of studies on the use of EPS-producing microorganisms in the production of fermented milk products is increasing. However, there are not enough studies explaining the interaction between caseins and exopolysaccharides in fermented milk products. In this study, the effects of exopolysaccharides and their functional properties were investigated in order to prevent undesirable problems such as serum separation and loose structure caused by the interaction of caseins and exopolysaccharides, which are critical factors in the formation of yoghurt texture.

Keywords

• Exopolysaccharide
• gelation
• yogurt
• lactic acid bacteria
• biopolymer

Laktik Asit Bakterileri Tarafından Üretilen Ekzopolisakkaritler: Fonksiyonel Özellikleri ve Yoğurt Dokusu Üzerine Etkileri

Abstract

Ekzopolisakkaritler (EPS), mikroorganizmalar tarafından hücre dışı olarak sentezlenen ve sağlık üzerinde olumlu etkileri olan polisakkaritlerdir. Düşük konsantrasyonlarda bile sentezlenen ekzopolisakkaritler, gıda ürünlerinin yapısını iyileştirme etkisine sahiptir. Böylece nihai ürünün dokusal özelliğini herhangi bir katkı maddesi kullanmadan istenilen şekilde geliştirerek tüketicilerin ihtiyaç ve taleplerini karşılamak mümkün olduğu gibi insan sağlığına da olumlu faydalar sağlamaktadır. EPS üreten mikroorganizmaların fermente süt ürünleri üretiminde kullanımına yönelik çalışmaların sayısı giderek artmaktadır. Ancak fermente süt ürünlerinde kazeinler ile ekzopolisakkaritler arasındaki etkileşimi açıklayan yeterli çalışma bulunmamaktadır. Bu derlemede, ekzopolisakkaritler, fonksiyonel özellikleri ve yoğurt dokusunun oluşumunda kritik faktör olan kazein ile ekzopolisakkaritlerin etkileşimi ve buna bağlı olarak serum ayrılması, gevşek yapı gibi istenmeyen sorunlara karşı etkileri araştırılmıştır.

Keywords

• Ekzopolisakkarit
• jelleşme
• yoğurt
• laktik asit bakterileri
• biyopolimer

References

1. Abarquero D., Renes E., Fresno JM. Tornadijo, M. E. Study of exopolysaccharides from lactic acid bacteria and their industrial applications: a review. International Journal of Food Science & Technology 2021.
2. Abushelaibi A.., Al-Mahadin S., El-Tarabily K., Shah, NP., Ayyash M. Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT-Food Science and Technology 2017; 79, 316-325.
3. Ale EC., Bourin MJB., Peralta GH., Burns PG., Ávila OB., Contini L., Binetti AG. Functional properties of exopolysaccharide (EPS) extract from Lactobacillus fermentum Lf2 and its impact when combined with Bifidobacterium animalis INL1 in yoghurt. International Dairy Journal 2019; 96, 114-125.
4. Almalki MA. Exopolysaccharide production by a new Lactobacillus lactis isolated from the fermented milk and its antioxidant properties. Journal of King Saud University-Science 2020; 32(2): 1272-1277.
5. Amiri S., Rezazadeh-Bari M., Alizadeh-Khaledabad M., Rezaei-Mokarram R., Sowti-Khiabani M. Fermentation optimization for co-production of postbiotics by Bifidobacterium lactis BB12 in cheese whey. Waste and Biomass Valorization 2021; 12, 1-16.
6. Andhare P., Chauhan K., Dave M., Pathak H. Microbial exopolysaccharides: advances in applications and future prospects. Biotechnology 2014; 3, 25.
7. Angelin J., Kavitha M. Exopolysaccharides from probiotic bacteria and their health potential. International Journal of Biological Macromolecules 2020; 162, 853-865.
8. Ayyash M., Abu-Jdayil B., Itsaranuwat P., Galiwango E., Tamiello-Rosa C., Abdullah H., Hamed F. Characterization, bioactivities, and rheological properties of exopolysaccharide produced by novel probiotic Lactobacillus plantarum C70 isolated from camel milk. International Journal of Biological Macromolecules 2020; 144, 938-946.

9. Barros CP., Guimarães JT., Esmerino EA., Duarte MCK., Silva MC., Silva R., Cruz AG. Paraprobiotics and postbiotics: concepts and potential applications in dairy products. Current Opinion in Food Science 2020; 32, 1-8.
10. Bensmira M., Nsabimana C., Jiang B. Effects of fermentation conditions and homogenization pressure on the rheological properties of Kefir. LWT-Food Science and Technology 2010; 43(8): 1180-1184.
11. Bhat B., Bajaj BK. Hypocholesterolemic potential and bioactivity spectrum of an exopolysaccharide from a probiotic isolate Lactobacillus paracasei M7. Bioactive Carbohydrates and Dietary Fibre 2019; 19, 100191.
12. Birch J., Harðarson HK., Khan S., Van Calsteren MR., Ipsen R., Garrigues C., Svensson B. Effect of repeat unit structure and molecular mass of lactic acid bacteria hetero- exopolysaccharides on binding to milk proteins. Carbohydrate polymers 2017; 177, 406-414.
13. Das K., Choudhary R., Thompson-Witrick KA. Effects of new technology on the current manufacturing process of yogurt-to increase the overall marketability of yogurt. LWT 2019; 108, 69-80.
14. Di W., Zhang L., Wang S., Yi H., Han X., Fan R., Zhang, Y. Physicochemical characterization and antitumour activity of exopolysaccharides produced by Lactobacillus casei SB27 from yak milk. Carbohydrate polymers 2017; 171, 307-315.
15. Ergene E., Avcı A. Microbial exopolisaccharides. Sakarya University Journal of Science 2016; 20(2): 193-202.
16. Farnworth ERT. Handbook of Fermented Functional Foods. London: CRC press; 2008.
17. Freitas F., Alves VD., Reis MA. Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends in biotechnology 2011; 29(8): 388-398.
18. Gentès MC., St-Gelais D., Turgeon SL. Gel formation and rheological properties of fermented milk with in situ exopolysaccharide production by lactic acid bacteria. Dairy science & technology 2011; 91(5): 645.
19. Gientka I., Bzducha-Wróbel A., Stasiak-Różańska L., Bednarska AA., Błażejak S. The exopolysaccharides biosynthesis by Candida yeast depends on carbon sources. Electronic Journal of Biotechnology 2016; 22, 31-37.
20. Girard M., Schaffer-Lequart C. Attractive interactions between selected anionic exopolysaccharides and milk proteins. Food Hydrocolloids 2008; 22(8): 1425-1434.
21. Grosu-Tudor SS., Zamfir M. Exopolysaccharide production by selected lactic acid bacteria isolated from fermented vegetables, Scientific Bulletin Series F. Biotechnologies 2014; 18, 2285-1364.
22. Güler‐Akın MB., Serdar Akin M., Korkmaz A. Influence of different exopolysaccharide‐producing strains on the physicochemical, sensory and syneresis characteristics of reduced‐fat stirred yoghurt. International journal of dairy technology 2009; 62(3): 422-430.
23. Guo Y., Pan D., Li H., Sun Y., Zeng X., Yan B. Antioxidant and immunomodulatory activity of selenium exopolysaccharide produced by Lactococcus lactis subsp. Lactis. Food chemistry 2013; 138(1): 84-89.
24. Gupta P., Diwan B. Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnology Reports 2017; 13, 58-71.
25. Han X., Yang Z., Jing X., Yu P., Zhang Y., Yi H., Zhang, L. Improvement of the texture of yogurt by use of exopolysaccharide producing lactic acid bacteria. BioMed research international 2016.
26. Hassan AN., Corredig M., Frank JF. Viscoelastic properties of yogurt made with ropy and non-ropy exopolysaccharides producing cultures. Milchwissenschaft 2001; 56(12): 684-686.
27. Hassan AN., Frank JF., Farmer MA., Schmidt KA., Shalabi SI. Formation of yogurt microstructure and three-dimensional visualization as determined by confocal scanning laser microscopy. Journal of Dairy Science 1995; 78(12): 2629-2636.
28. Hundschell CS., Wagemans AM. Rheology of common uncharged exopolysaccharides for food applications. Current Opinion in Food Science 2019; 27, 1-7.
29. Kavitake D., Devi PB., Shetty PH. Overview of an exopolysaccharides produced by Weissella genus–A review. International Journal of Biological Macromolecules 2020.
30. Korcz E., Varga L. Exopolysaccharides from lactic acid bacteria: Techno-functional application in the food industry. Trends in Food Science & Technology 2021
31. Kumar M., Kumar R., Singh D., Bhatt S., Gupta M. Physiological and genomic characterization of an exopolysaccharide-producing Weissella cibaria CH2 from cheese of the western Himalayas. Food Bioscience 2020; 100570.
32. Lee WJ., Lucey JA. Rheological properties, whey separation, and microstructure in set‐style yogurt: Effects of heating temperature and incubation temperature. Journal of Texture Studies 2003; 34(5‐6): 515-536.
33. Lee WJ., Lucey JA. Formation and physical properties of yogurt. Asian-Australasian Journal of Animal Sciences 2010; 23(9): 1127-1136.
34. Li XW., Lv S., Shi TT., Liu K., Li QM., Pan LH., Luo JP. Exopolysaccharides from yoghurt fermented by Lactobacillus paracasei: Production, purification and its binding to sodium caseinate. Food Hydrocolloids 2020; 102, 105635.
35. Luang-In V., Deeseenthum S. Exopolysaccharide-producing isolates from Thai milk kefir and their antioxidant activities. LWT 2016; 73, 592-601.
36. Madhubasani GBL., Prasanna PHP., Chandrasekara A., Gunasekara DCS., Senadeera P., Chandramali DVP., Vidanarachchi JK. Exopolysaccharide producing starter cultures positively influence on microbiological, physicochemical, and sensory properties of probiotic goats' milk set‐yoghurt. Journal of Food Processing and Preservation 2020; 44(3): e14361.
37. Mende S., Rohm H., Jaros D. Influence of exopolysaccharides on the structure, texture, stability and sensory properties of yoghurt and related products. International Dairy Journal 2016; 52, 57-71.
38. Minervini F., De Angelis M., Surico RF., Di Cagno R., Gänzle M., Gobbetti M. Highly efficient synthesis of exopolysaccharides by Lactobacillus curvatus DPPMA10 during growth in hydrolyzed wheat flour agar. International journal of food microbiology 2010, 141(1-2): 130-135.
39. Moradi M., Guimarães JT., Sahin S. Current applications of exopolysaccharides from lactic acid bacteria in the development of food active edible packaging. Current Opinion in Food Science 2021; 40, 33-39.
40. Patel M., Prasad W., Naithani H., Nataraj BH., Arora S., Behare PV. Comparative evaluation of in situ and ex-situ iron-complexing ability of exopolysaccharides producing lactic acid bacteria in whey medium. LWT 2021; 147, 111598.
41. Rajoka MSR., Wu Y., Mehwish HM., Bansal M., Zhao L. Lactobacillus exopolysaccharides: New perspectives on engineering strategies, physiochemical functions, and immunomodulatory effects on host health. Trends in Food Science & Technology 2020.
42. Ramirez-Santiago C., Ramos-Solis L., Lobato-Calleros C., Peña-Valdivia C., Vernon-Carter EJ., Alvarez-Ramírez J. Enrichment of stirred yogurt with soluble dietary fiber from Pachyrhizus erosus L. Urban: Effect on syneresis, microstructure and rheological properties. Journal of Food Engineering 2010, 101(3): 229-235.
43. Rana S., Upadhyay LSB. Microbial exopolysaccharides: Synthesis pathways, types and their commercial applications. International journal of biological macromolecules 2020; 157, 577-583.
44. Ruas-Madiedo P., De Los Reyes-Gavilán CG. Invited review: methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. Journal of dairy science 2005; 88(3): 843-856.
45. Ruas-Madiedo P., Hugenholtz J., Zoon P. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. International Dairy Journal 2002, 12(2-3): 163-171.
46. Saadat YR., Khosroushahi AY., Gargari BP. A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides. Carbohydrate polymers 2019; 217, 79-89.
47. Şanli T., Gursel A., Şanli E., Acar E., Benli M. The effect of using an exopolysaccharide‐producing culture on the physicochemical properties of low‐fat and reduced‐fat Kasar cheeses. International Journal of Dairy Technology 2013; 66(4): 535-542.
48. Suresh Kumar A., Mody K., Jha B. Bacterial exopolysaccharides–a perception. Journal of basic microbiology 2007; 47(2): 103-117.
49. Tan KX., Chamundeswari VN., Loo SCJ. Prospects of kefiran as a food-derived biopolymer for agri-food and biomedical applications. RSC Advances 2020; 10(42): 25339-25351.
50. Tiwari S., Kavitake D., Devi PB., Halad PS. Bacterial exopolysaccharides for improvement of technological, functional and rheological properties of yoghurt. International Journal of Biological Macromolecules 2021.
51. Tomasik P., Tomasik P. Probiotics, non-dairy prebiotics and postbiotics in nutrition. Applied Sciences 2020; 10(4): 1470.
52. Werning ML., Notararigo S., Nácher M., Fernández de Palencia P., Aznar R., López P. Biosynthesis, purification and biotechnological use of exopolysaccharides produced by lactic acid bacteria. Food additives 2012; 83-114.
53. Wu X., Xu R., Ren Q., Bai J., Zhao J. Factors affecting extracellular and intracellular polysaccharide production in submerged cultivation of Tricholoma Mongolicum. African Journal of Microbiology Research 2012; 6(5): 909-916.
54. Xiao Y., Liu Y., Wang Y., Jin Y., Guo X, Liu Y., Xu H. Heat-induced whey protein isolate gels improved by cellulose nanocrystals: Gelling properties and microstructure. Carbohydrate polymers 2020; 231, 115749.
55. Xu R., Shang N., Li P. In vitro and in vivo antioxidant activity of exopolysaccharide fractions from Bifidobacterium animalis RH. Anaerobe 2011; 17(5): 226-231.
56. Yang T., Wu K., Wang F., Liang X., Liu Q., Li G., Li Q. Effect of exopolysaccharides from lactic acid bacteria on the texture and microstructure of buffalo yoghurt. International Dairy Journal 2014; 34(2): 252-256.
57. Yilmaz MT., Dertli E., Toker OS., Tatlisu NB., Sagdic O., Arici M. Effect of in situ exopolysaccharide production on physicochemical, rheological, sensory, and microstructural properties of the yogurt drink ayran: an optimization study based on fermentation kinetics. Journal of Dairy Science 2015, 98(3): 1604-1624.
58. Younes E. Structural properties of casein micelles in milk; the effect of salt, temperature, and pH. Int J biotech & bioeng 2017; 3, 202-215.
59. Zhang L., Folkenberg DM., Amigo JM., Ipsen R. Effect of exopolysaccharide- producing starter cultures and post-fermentation mechanical treatment on textural properties and microstructure of low fat yoghurt. International Dairy Journal 2016; 53, 10-19.
60. Zhang M., Lai T., Yao M., Zhang M., Yang Z. Interaction of the Exopolysaccharide from Lactobacillus plantarum YW11 with Casein and Bioactivities of the Polymer Complex. Foods 2021; 10(6): 1153.
61. Zhang M., Fan S., Hao M., Hou H., Zheng H., Darwesh OM. Improving the production of fungal exopolysaccharides with application of repeated batch fermentation technology coupling with foam separation in the presence of surfactant. Process Biochemistry 2021; 100, 82-89.
62. Zhou Q., Feng F., Yang Y., Zhao F., Du R,, Zhou Z., Han Y. Characterization of a dextran produced by Leuconostoc pseudomesenteroides XG5 from homemade wine. International journal of biological macromolecules 2018; 107, 2234-2241.
63. Zhu Y., Zhou JM., Liu W., Pi X., Zhou Q., Li P., Gu Q. Effects of exopolysaccharide from Lactobacillus rhamnosus on human gut microbiota in in vitro fermentation model. LWT 2020; 110524.