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Exploring encapsulation strategies as a protective mechanism to avoid amensalism in mixed populations of Pseudomonas taetrolens and Lactobacillus casei

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Abstract

Pseudomonas taetrolens constitutes an efficient platform for the biosynthesis of lactobionic acid, a potentially prebiotic compound. Unfortunately, an amensalistic interaction has been demonstrated between P. taetrolens and probiotic lactic acid bacteria (LAB), characterized by the competitive exclusion of P. taetrolens, hindering the in situ production of fermented dairy products with synbiotic properties. In the present research, encapsulation was explored as a barrier to the diffusion of the antimicrobial metabolites generated by LAB. Mixed fermentations involving P. taetrolens LMG 2336 and Lactobacillus casei CECT 475 were cultivated, entrapping both microorganisms alternately. Alginate, alginate/starch and carboxymethyl cellulose/k-carrageenan were tested as encapsulating agents. The immobilization of L. casei in 2% alginate/2% starch beads was found to be the best strategy, improving the production of lactobionic acid by 182% with respect to co-cultures with free cells. This study proves the potential of LAB encapsulation for the protection of sensitive strains in mixed food fermentations.

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References

  1. Alonso S, Rendueles M, Díaz M (2015) A novel approach to monitor stress-induced physiological responses in immobilized microorganisms. Appl Microbiol Biotechnol 99:3573–3583

    CAS  PubMed  Google Scholar 

  2. Champagne CP, Fustier P (2007) Microencapsulation for the improved delivery of bioactive compounds into foods. Curr Opin Biotechnol 18:184–190

    CAS  PubMed  Google Scholar 

  3. Sathyabama S, Ranjith Kumar M, Bruntha Devi P, Vijayabharathi R, Brindha Priyadharisini V (2014) Co-encapsulation of probiotics with prebiotics on alginate matrix and its effect on viability in simulated gastric environment. LWT Food Sci Technol 57:419–425

    CAS  Google Scholar 

  4. Chávarri M, Marañón I, Ares R, Ibáñez FC, Marzo F, Villarán MC (2010) Microencapsulation of a probiotic and prebiotic in alginate-chitosan capsules improves survival in simulated gastro-intestinal conditions. Int J Food Microbiol 142:185–189

    PubMed  Google Scholar 

  5. Divyashri G, Prapulla SG (2015) Mass transfer characterization of gamma-aminobutyric acid production by Enterococcus faecium CFR 3003: encapsulation improves its survival under simulated gastro-intestinal conditions. Bioprocess Biosyst Eng 38:569–574

    CAS  PubMed  Google Scholar 

  6. Martin MJ, Lara-Villoslada F, Ruiz MA, Morales ME (2013) Effect of unmodified starch on viability of alginate-encapsulated Lactobacillus fermentum CECT5716. LWT Food Sci Technol 53:480–486

    CAS  Google Scholar 

  7. Lozano-Vazquez G, Lobato-Calleros C, Escalona-Buendia H, Chavez G, Alvarez-Ramirez J, Vernon-Carter EJ (2015) Effect of the weight ratio of alginate-modified tapioca starch on the physicochemical properties and release kinetics of chlorogenic acid containing beads. Food Hydrocoll 48:301–311

    CAS  Google Scholar 

  8. Dafe A, Etemadi H, Zarredar H, Mahdavinia GR (2017) Development of novel carboxymethyl cellulose/k-carrageenan blends as an enteric delivery vehicle for probiotic bacteria. Int J Biol Macromol 97:299–307

    CAS  PubMed  Google Scholar 

  9. Hambleton A, Fabra MJ, Debeaufort F, Dury-Brun C, Voilley A (2009) Interface and aroma barrier properties of iota-carrageenan emulsion-based films used for encapsulation of active food compounds. J Food Eng 93:80–88

    CAS  Google Scholar 

  10. Cheirsilp B, Shoji H, Shimizu H, Shioya S (2003) Interactions between Lactobacillus kefiranofaciens and Saccharomyces cerevisiae in mixed culture for kefiran production. J Biosci Bioeng 96:279–284

    CAS  PubMed  Google Scholar 

  11. Doleyres Y, Fliss I, Lacroix C (2004) Increased stress tolerance of Bifidobacterium longum and Lactococcus lactis produced during continuous mixed-strain immobilized-cell fermentation. J Appl Microbiol 97:527–539

    CAS  PubMed  Google Scholar 

  12. Grattepanche F, Audet P, Lacroix C (2007) Enhancement of functional characteristics of mixed lactic culture producing nisin Z and exopolysaccharides during continuous prefermentation of milk with immobilized cells. J Dairy Sci 90:5361–5373

    CAS  PubMed  Google Scholar 

  13. Smid EJ, Lacroix C (2013) Microbe-microbe interactions in mixed culture food fermentations. Curr Opin Biotechnol 24:148–154

    CAS  PubMed  Google Scholar 

  14. Simova E, Beshkova D, Angelov A, Hristozova TS, Frengova G, Spasov Z (2002) Lactic acid bacteria and yeasts in kefir grains and kefir made from them. J Ind Microbiol Biotechnol 28:1–6

    CAS  PubMed  Google Scholar 

  15. Digaitiene A, Hansen ÅS, Juodeikiene G, Eidukonyte D, Josephsen J (2012) Lactic acid bacteria isolated from rye sourdoughs produce bacteriocin-like inhibitory substances active against Bacillus subtilis and fungi. J Appl Microbiol 112:732–742

    CAS  PubMed  Google Scholar 

  16. García C, Rendueles M, Díaz M (2019) Liquid-phase food fermentations with microbial consortia involving lactic acid bacteria: a review. Food Res Int 119:207–220

    PubMed  Google Scholar 

  17. Adebola OO, Corcoran O, Morgan WA (2014) Synbiotics: the impact of potential prebiotics inulin, lactulose and lactobionic acid on the survival and growth of lactobacilli probiotics. J Funct Foods 10:75–84

    CAS  Google Scholar 

  18. Gutiérrez LF, Hamoudi S, Belkacemi K (2012) Lactobionic acid: a high value-added lactose derivative for food and pharmaceutical applications. Int Dairy J 26:103–111

    Google Scholar 

  19. Alonso S, Rendueles M, Díaz M (2011) Efficient lactobionic acid production from whey by Pseudomonas taetrolens under pH-shift conditions. Bioresour Technol 102:9730–9736

    CAS  PubMed  Google Scholar 

  20. Alonso S, Rendueles M, Díaz M (2012) Role of dissolved oxygen availability on lactobionic acid production from whey by Pseudomonas taetrolens. Bioresour Technol 109:140–147

    CAS  PubMed  Google Scholar 

  21. Alonso S, Rendueles M, Díaz M (2013) Selection method of pH conditions to establish Pseudomonas taetrolens physiological states and lactobionic acid production. Appl Microbiol Biotechnol 97:3843–3854

    CAS  PubMed  Google Scholar 

  22. García C, Rendueles M, Díaz M (2017) Microbial amensalism in Lactobacillus casei and Pseudomonas taetrolens mixed culture. Bioprocess Biosyst Eng 40:1111–1122

    PubMed  Google Scholar 

  23. Yousseef M, Lafarge C, Valentin D, Lubbers S, Husson F (2016) Fermentation of cow milk and/or pea milk mixtures by different starter cultures: physico-chemical and sensorial properties. LWT Food Sci Technol 69:430–437

    CAS  Google Scholar 

  24. Sultana K, Godward G, Reynolds N, Arumugaswamy R, Peiris P, Kailasapathy K (2000) Encapsulation of probiotic bacteria with alginate-starch and evaluation of survival in simulated gastrointestinal conditions and in yoghurt. Int J Food Microbiol 62:47–55

    CAS  PubMed  Google Scholar 

  25. López-Córdoba A, Deladino L, Martino M (2013) Effect of starch filler on calcium-alginate hydrogels loaded with yerba mate antioxidants. Carbohydr Polym 95:315–323

    PubMed  Google Scholar 

  26. Sandoval-Castilla O, Lobato-Calleros C, García-Galindo HS, Alvarez-Ramírez J, Vernon-Carter EJ (2010) Textural properties of alginate-pectin beads and survivability of entrapped Lb. casei in simulated gastrointestinal conditions and in yoghurt. Food Res Int 43:111–117

    CAS  Google Scholar 

  27. Chou S, Luo L, Lai J, Ma DH (2016) On the importance of Bloom number of gelatin to the development of biodegradable in situ gelling copolymers for intracameral drug delivery. Int J Pharm 511:30–43

    CAS  PubMed  Google Scholar 

  28. Saxena A, Sachin K, Bohidar HB, Verma AK (2005) Effect of molecular weight heterogeneity on drug encapsulation efficiency of gelatin nano-particles. Colloids Surf B Biointerfaces 45:42–48

    CAS  PubMed  Google Scholar 

  29. Heidebach T, Först P, Kulozik U (2012) Microencapsulation of probiotic cells for food applications. Crit Rev Food Sci Nutr 52:291–311

    CAS  PubMed  Google Scholar 

  30. Hosseini SM, Hosseini H, Mohammadifar MA, German JB, Mortazavian AM, Mohammadi A, Khosravi-Darani K, Shojaee-Aliabadi S, Khaksar R (2014) Preparation and characterization of alginate and alginate-resistant starch microparticles containing nisin. Carbohydr Polym 103:573–580

    CAS  PubMed  Google Scholar 

  31. Rathore S, Desai PM, Liew CV, Chan LW, Heng PWS (2013) Microencapsulation of microbial cells. J Food Eng 116:369–381

    CAS  Google Scholar 

  32. Krasaekoopt W, Bhandari B, Deeth H (2003) Evaluation of encapsulation techniques of probiotics for yoghurt. Int Dairy J 13:3–13

    CAS  Google Scholar 

  33. Baldwin C, Akashe A, Zeller AL, Márquez-Sánchez M (2007) Mineral complexes of lactobionic acid and method of using for mineral fortification of food products. United States Patent Application Pub. No.: US 2007/0026110A1.

  34. Paşcalău V, Popescu V, Popescu GL, Dudescu MC, Borodi G, Dinescu A, Perhaiţa I, Paul M (2012) The alginate/k-carrageenan ratio’s influence on the properties of the cross-linked composite films. J Alloy Compd 536:418–423

    Google Scholar 

  35. Mooranian A, Negrulj R, Al-Sallami HS, Fang Z, Mikov M, Golocorbin-Kon S, Fakhoury M, Arfuso F, Al-Salami H (2015) Release and swelling studies of an innovative antidiabetic-bile acid microencapsulated formulation, as a novel targeted therapy for diabetes treatment. J Microencapsul 32:151–216

    CAS  PubMed  Google Scholar 

  36. Abdel-Rahman MA, Tashiro Y, Sonomoto K (2013) Recent advances in lactic acid production by microbial fermentation processes. Biotechnol Adv 31:877–902

    CAS  PubMed  Google Scholar 

  37. Genisheva Z, Mussatto SI, Oliveira JM, Teixeira JA (2013) Malolactic fermentation of wines with immobilized lactic acid bacteria—influence of concentration, type of support material and storage conditions. Food Chem 138:1510–1514

    CAS  PubMed  Google Scholar 

  38. Zhao Z, Xie X, Wang Z, Tao Y, Niu X, Huang X, Liu L, Li Z (2016) Immobilization of Lactobacillus rhamnosus in mesoporous silica-based material: an efficiency continuous cell-recycle fermentation system for lactic acid production. J Biosci Bioeng 121:645–651

    CAS  PubMed  Google Scholar 

  39. Zhang Z, Zhang R, Chen L, McClements DJ (2016) Encapsulation of lactase (β-galactosidase) into k-carrageenan-based hydrogel beads: impact of environmental conditions on enzyme activity. Food Chem 200:69–75

    CAS  PubMed  Google Scholar 

  40. Zwietering MH, Jongenburger I, Rombouts FM, van’T Riet K (1990) Modelling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Wallenius J, Uuksulainen T, Salonen K, Rautio J, Eerikäinen T (2011) The effect of temperature and pH gradients on Lactobacillus rhamnosus gene expression of stress-related genes. Bioprocess Biosyst Eng 34:1169–1176

    CAS  PubMed  Google Scholar 

  42. Wu C, Zhang J, Wang M, Du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biotechnol 39:1031–1039

    CAS  PubMed  Google Scholar 

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Acknowledgements

Authors thank the financial support from the Government of the Principality of Asturias by the project FC-GRUPIN-IDI/2018/000127. Authors also wish to thank the technical assistance of Marta Alonso (Process Image Area, Scientific-Technical Services, University of Oviedo).

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Correspondence to Mario Díaz.

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García, C., Ranieri, G., Rendueles, M. et al. Exploring encapsulation strategies as a protective mechanism to avoid amensalism in mixed populations of Pseudomonas taetrolens and Lactobacillus casei. Bioprocess Biosyst Eng 43, 55–66 (2020). https://doi.org/10.1007/s00449-019-02204-8

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