Characterization, high production and antimicrobial activity of exopolysaccharides from Lactococcus lactis F-mou

Microbial Pathogenesis

Volumn 132, Issue , 2019, Pages 10-19

  Nehal, Fatima ^a   Sahnoun, Mouna ^b   Smaoui, Slim ^c   Jaouadi, Bassem ^b   Bejar, Samir ^b   Mohammed, Sebaihia ^a  

^a HASSIBA BENBOUALI UNIVERSITY OF CHLEF   (Algeria)

^b CENTRE DE BIOTECHNOLOGIE DE SFAX   (Tunisia)

^c UNIVERSITY OF SFAX   (Tunisia)

Author keywords

Antimicrobial; Antioxidant; Box Behnken design; Exopolysaccharide; Lactococcus lactis; Mech Degla juice

Indexed keywords

1,1 DIPHENYL 2 PICRYLHYDRAZYL; AMIDE; BETA CAROTENE; CARBOXYL GROUP; EXOPOLYSACCHARIDE; HYDROXYL GROUP; SULFATE; ANTIINFECTIVE AGENT; ANTIOXIDANT; EMULSIFYING AGENT; POLYSACCHARIDE; RNA 16S;

ACINETOBACTER BAUMANNII; ALGERIA; ANTIBACTERIAL ACTIVITY; ANTICOAGULATION; ANTIFUNGAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BACILLUS CEREUS; BACTERIAL STRAIN; BIOTECHNOLOGICAL PRODUCTION; BLOOD CLOTTING TEST; BOX BEHNKEN DESIGN; CAMEL MILK; CANDIDA ALBICANS; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; COSMETIC INDUSTRY; DPPH RADICAL SCAVENGING ASSAY; DRUG INDUSTRY; DRUG ISOLATION; DRUG STRUCTURE; EMULSION; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; EXPERIMENTAL DESIGN; FOOD INDUSTRY; FOURIER TRANSFORM INFRARED SPECTROSCOPY; INCUBATION TIME; INOCULATION; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; NONHUMAN; OIL HOLDING CAPACITY; PHYSICAL PARAMETERS; PLACKETT BURMAN DESIGN; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEUS MIRABILIS; PSEUDOMONAS AERUGINOSA; SCANNING ELECTRON MICROSCOPY; STAPHYLOCOCCUS AUREUS; WATER HOLDING CAPACITY; ANIMAL; BACTERIUM; BIOSYNTHESIS; CAMEL; DRUG EFFECT; FUNGUS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MILK;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIOXIDANTS; BACTERIA; CAMELUS; EMULSIFYING AGENTS; FUNGI; LACTOCOCCUS LACTIS; MICROBIAL SENSITIVITY TESTS; MILK; POLYSACCHARIDES; RNA, RIBOSOMAL, 16S;

EID: 85064525029     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2019.04.018     Document Type: Article

References (72)

1. Badel, S., Bernardi, T., Michaud, P., New perspectives for Lactobacilli exopolysaccharides. Biotechnol. Adv. 29:1 (2011), 54–66.
2. Caggianiello, G., Kleerebezem, M., Spano, G., Exopolysaccharides produced by lactic acid bacteria: from health-promoting benefits to stress tolerance mechanisms. Appl. Microbiol. Biotechnol. 100:9 (2016), 3877–3886.
3. Knoshaug, E.P., Ahlgren, J.A., Trempy, J.E., Growth associated exopolysaccharide expression in Lactococcus lactis subspecies cremoris Ropy352. J. Dairy Sci. 83:4 (2000), 633–640.
4. Zhou, Y., Cui, Y., Qu, X., Exopolysaccharides of lactic acid bacteria: structure, bioactivity and associations: a review. Carbohydr. Polym. 207 (2019), 317–332.
5. Mende, S., Rohm, H., Jaros, D., Influence of exopolysaccharides on the structure, texture, stability and sensory properties of yoghurt and related products. Int. Dairy J. 52 (2016), 57–71.
6. Costa, N.E., Hannon, J.A., Guinee, T.P., Auty, M.A., McSweeney, P.L., Beresford, T.P., Effect of exopolysaccharide produced by isogenic strains of Lactococcus lactis on half-fat Cheddar cheese. J. Dairy Sci. 93:8 (2010), 3469–3486.
7. Kristo, E., Miao, Z., Corredig, M., The role of exopolysaccharide produced by Lactococcus lactis subsp. cremoris in structure formation and recovery of acid milk gels. Int. Dairy J. 21:9 (2011), 656–662.
8. Devi, P.B., Kavitake, D., Shetty, P.H., Physico-chemical characterization of galactan exopolysaccharide produced by Weissella confusa KR780676. Int. J. Biol. Macromol. 93:Pt A (2016), 822–828.
9. Saravanan, C., Shetty, P.K., Isolation and characterization of exopolysaccharide from Leuconostoc lactis KC117496 isolated from idli batter. Int. J. Biol. Macromol. 90 (2016), 100–106.
10. Hou, Z., Gao, Y., Yuan, F., Liu, Y., Li, C., Xu, D., Investigation into the physicochemical stability and rheological properties of beta-carotene emulsion stabilized by soybean soluble polysaccharides and chitosan. J. Agric. Food Chem. 58:15 (2010), 8604–8611.
11. Pan, D., Mei, X., Antioxidant activity of an exopolysaccharide purified from Lactococcus lactis subsp. lactis 12. Carbohydr. Polym. 80:3 (2010), 908–914.
12. Drogoz, A., Munier, S., Verrier, B., David, L., Domard, A., Delair, T., Towards biocompatible vaccine delivery systems: interactions of colloidal PECs based on polysaccharides with HIV-1 p24 antigen. Biomacromolecules 9:2 (2008), 583–591.
13. Ayadi, F., Bayer, I.S., Marras, S., Athanassiou, A., Synthesis of water dispersed nanoparticles from different polysaccharides and their application in drug release. Carbohydr. Polym. 136 (2016), 282–291.
14. Gorska, S., Hermanova, P., Ciekot, J., Schwarzer, M., Srutkova, D., Brzozowska, E., Kozakova, H., Gamian, A., Chemical characterization and immunomodulatory properties of polysaccharides isolated from probiotic Lactobacillus casei LOCK 0919. Glycobiology 26:9 (2016), 1014–1024.
15. Lee, I.C., Caggianiello, G., van, S., II. Taverne, N., Meijerink, M., Bron, P.A., Spano, G., Kleerebezem, M., Strain-specific features of extracellular polysaccharides and their impact on Lactobacillus plantarum-host interactions. J. Appl. Environ. Microbiol. 82:13 (2016), 3959–3970.
16. Zaporozhets, T., Besednova, N., Prospects for the therapeutic application of sulfated polysaccharides of brown algae in diseases of the cardiovascular system: review. Pharm. Biol. 54:12 (2016), 3126–3135.
17. Jiang, Y., Yang, Z., A functional and genetic overview of exopolysaccharides produced by Lactobacillus plantarum. J. Funct. Foods 47 (2018), 229–240.
18. Mahdhi, A., Leban, N., Chakroun, I., Bayar, S., Mahdouani, K., Majdoub, H., Kouidhi, B., Use of extracellular polysaccharides, secreted by Lactobacillus plantarum and Bacillus spp., as reducing indole production agents to control biofilm formation and efflux pumps inhibitor in Escherichia coli. Microb. Pathog. 125 (2018), 448–453.
19. Mahdhi, A., Leban, N., Chakroun, I., Chaouch, M.A., Hafsa, J., Fdhila, K., Mahdouani, K., Majdoub, H., Extracellular polysaccharide derived from potential probiotic strain with antioxidant and antibacterial activities as a prebiotic agent to control pathogenic bacterial biofilm formation. Microb. Pathog. 109 (2017), 214–220.
20. 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 Chem. 138:1 (2013), 84–89.
21. Niknezhad, S., Asadollahi, M., Zamani, A., Biria, D., Production of xanthan gum by Xanthomonas species using starch as carbon source. Minerva Biotecnol. 26:3 (2014), 191–197.
22. Li, P., Li, T., Zeng, Y., Li, X., Jiang, X., Wang, Y., Xie, T., Zhang, Y., Biosynthesis of xanthan gum by Xanthomonas campestris LRELP-1 using kitchen waste as the sole substrate. Carbohydr. Polym. 151 (2016), 684–691.
23. Niknezhad, S.V., Asadollahi, M.A., Zamani, A., Biria, D., Doostmohammadi, M., Optimization of xanthan gum production using cheese whey and response surface methodology. Food Sci. Biotechnol. 24:2 (2015), 453–460.
24. Woiciechowski, A.L., Soccol, C.R., Rocha, S.N., Pandey, A., Xanthan gum production from cassava bagasse hydrolysate with Xanthomonas campestris using alternative sources of nitrogen. Biotechnol. Appl. Biochem. 118:1–3 (2004), 305–312.
25. Yoo, S.D., Harcum, S.W., Xanthan gum production from waste sugar beet pulp. Bioresour. Technol. 70:1 (1999), 105–109.
26. Druzian, J., Paula Pagliarini, A., Xanthan gum production by fermentation from residue of apple juice. Cienc. Tecnol. Aliment. 27:1 (2007), 26–31.
27. Razack, S., Velayutham, V., Thangavelu, V., Medium optimization for production of Exopolysaccharide by Bacillus subtilis using synthetic sources and agro wastes. Turkish J. Biol. 37:3 (2013), 280–288.
28. Banik, R.M., Santhiagu, A., Upadhyay, S.N., Optimization of nutrients for gellan gum production by Sphingomonas paucimobilis ATCC-31461 in molasses based medium using response surface methodology. Bioresour. Technol. 98:4 (2007), 792–797.
29. Mehta, A., Prasad, G.S., Choudhury, A.R., Cost effective production of pullulan from agri-industrial residues using response surface methodology. Int. J. Biol. Macromol. 64 (2014), 252–256.
30. Mansouri, A., Rihani, R., Laoufi, A.N., Özkan, M., Production of bioethanol from a mixture of agricultural feedstocks: biofuels characterization. Fuel 185 (2016), 612–621.
31. DuBois, M., E. Gilles, K.A., Hamilton, J.K., Rebers, P.A.J., Smith, F., Calorimetric Dubois method for determination of sugar and related substances. Anal. Chem. 28:3 (1956), 350–356.
32. Miller, G.L., Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31:3 (1959), 426–428.
33. Townshend, A., Official Methods of Analysis of the Association of Official Analytical Chemists. fourteenth ed., 1987 New York.
34. Nehal, F., Jallouli, R., Krayem, N., Bou Ali, M., Dilmi Bouras, A., Fendri, A., Gargouri, Y., Biochemical and molecular characterization of a lipase from an Algerian isolated Staphylococcus aureus strain. J. Basic Microbiol. 57:3 (2017), 253–264.
35. Sambrook, J., Fritsch, E.F., Maniatis, T., Molecular Cloning: a Laboratory Manual. 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Trabelsi, I., Slima, S.B., Chaabane, H., Riadh, B.S., Purification and characterization of a novel exopolysaccharides produced by Lactobacillus sp. Ca6. Int. J. Biol. Macromol. 74 (2015), 541–546.
37. Elleuch, L., Shaaban, M., Smaoui, S., Mellouli, L., Karray-Rebai, I., Fourati-Ben Fguira, L., Shaaban, K.A., Laatsch, H., Bioactive secondary metabolites from a new terrestrial Streptomyces sp. TN262. Biotechnol. Appl. Biochem. 162:2 (2010), 579–593.
38. Daoud, A., Malika, D., Bakari, S., Hfaiedh, N., Mnafgui, K., Kadri, A., Gharsallah, N., Assessment of polyphenol composition, antioxidant and antimicrobial properties of various extracts of Date Palm Pollen (DPP) from two Tunisian cultivars. Arab. J. Chem. 7 (2015), 2–14.
39. You, L., Zhao, M., Regenstein, J.M., Ren, J., In vitro antioxidant activity and in vivo anti-fatigue effect of loach (Misgurnus anguillicaudatus) peptides prepared by papain digestion. Food Chem. 124:1 (2011), 188–194.
40. Koleva II, van Beek, T.A., Linssen, J.P., de Groot, A., Evstatieva, L.N., Screening of plant extracts for antioxidant activity: a comparative study on three testing methods. Phytochem. Anal.PCA 13:1 (2002), 8–17.
41. Prieto, P., Pineda, M., Aguilar, M., Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal. Biochem. 269:2 (1999), 337–341.
42. Freitas, F., Alves, V.D., Pais, J., Costa, N., Oliveira, C., Mafra, L., Hilliou, L., Oliveira, R., Reis, M.A., Characterization of an extracellular polysaccharide produced by a Pseudomonas strain grown on glycerol. Bioresour. Technol. 100:2 (2009), 859–865.
43. Zotta, T., Piraino, P., Parente, E., Salzano, G., Ricciardi, A., Characterization of lactic acid bacteria isolated from sourdoughs for Cornetto, a traditional bread produced in Basilicata (Southern Italy). World J. Microbiol. Biotechnol. 24:9 (2008), 1785–1795.
44. Wang, K., Li, W., Rui, X., Chen, X., Jiang, M., Dong, M., Characterization of a novel exopolysaccharide with antitumor activity from Lactobacillus plantarum 70810. Int. J. Biol. Macromol. 63 (2014), 133–139.
45. Maria, S.F., Russell, L.M., Turpin, B.J., Porcja, R.J., FTIR measurements of functional groups and organic mass in aerosol samples over the Caribbean. Atmos. Environ. 36:33 (2002), 5185–5196.
46. Finore, I., Di Donato, P., Mastascusa, V., Nicolaus, B., Poli, A., Fermentation technologies for the optimization of marine microbial exopolysaccharide production. Mar. Drugs 12:5 (2014), 3005–3024.
47. Yadav, V., Gurudutt Prappulla, S., Jha, A., Poonia, A., A novel exopolysaccharide from probiotic Lactobacillus fermentum CFR 2195: production, purification and characterization. Biotechnol. Bioinf. Bioeng. 1:4 (2011), 415–421.
48. Kanamarlapudi, S.L.R.K., Muddada, S., Characterization of exopolysaccharide produced by Streptococcus thermophilus CC30. BioMed Res. Int., 2017, 2017, 4201809.
49. Sivasankar, P., Seedevi, P., Poongodi, S., Sivakumar, M., Murugan, T., Sivakumar, L., Sivakumar, K., Balasubramanian, T., Characterization, antimicrobial and antioxidant property of exopolysaccharide mediated silver nanoparticles synthesized by Streptomyces violaceus MM72. Carbohydr. Polym. 181 (2018), 752–759.
50. Maina, N.H., Tenkanen, M., Maaheimo, H., Juvonen, R., Virkki, L., NMR spectroscopic analysis of exopolysaccharides produced by Leuconostoc citreum and Weissella confusa. Carbohydr. Res. 343:9 (2008), 1446–1455.
51. Funane, K., Ishii, T., Matsushita, M., Hori, K., Mizuno, K., Takahara, H., Kitamura, Y., Kobayashi, M., Water-soluble and water-insoluble glucans produced by Escherichia coli recombinant dextransucrases from Leuconostoc mesenteroides NRRL B-512F. Carbohydr. Res. 334:1 (2001), 19–25.
52. Lundborg, M., Widmalm, G., Structural analysis of glycans by NMR chemical shift prediction. Anal. Chem. 83:5 (2011), 1514–1517.
53. Farias, W.R., Nazareth, R.A., Mourao, P.A., Dual effects of sulfated D-galactans from the red algae Botryocladia occidentalis preventing thrombosis and inducing platelet aggregation. Thromb. Haemostasis 86:6 (2001), 1540–1546.
54. Abid, Y., Casillo, A., Gharsallah, H., Joulak, I., Lanzetta, R., Corsaro, M.M., Attia, H., Azabou, S., Production and structural characterization of exopolysaccharides from newly isolated probiotic lactic acid bacteria. Int. J. Biol. Macromol. 108 (2018), 719–728.
55. Zhang, J., Cao, Y., Wang, J., Guo, X., Zheng, Y., Zhao, W., Mei, X., Guo, T., Yang, Z., Physicochemical characteristics and bioactivities of the exopolysaccharide and its sulphated polymer from Streptococcus thermophilus GST-6. Carbohyd. Polym. 146 (2016), 368–375.
56. Reyes, A.W., Arayan, L.T., Simborio, H.L., Hop, H.T., Min, W., Lee, H.J., Kim, D.H., Chang, H.H., Kim, S., Dextran sulfate sodium upregulates MAPK signaling for the uptake and subsequent intracellular survival of Brucella abortus in murine macrophages. Microb. Pathog. 91 (2016), 68–73.
57. Pustylnikov, S., Sagar, D., Jain, P., Khan, Z.K., Targeting the C-type lectins-mediated host-pathogen interactions with dextran. J. Pharm. Pharm. Sci. 17:3 (2014), 371–392.
58. Guo, Y., Pan, D., Sun, Y., Xin, L., Li, H., Zeng, X., Antioxidant activity of phosphorylated exopolysaccharide produced by Lactococcus lactis subsp. lactis. Carbohydr. Polym. 97:2 (2013), 849–854.
59. Tang, W., Dong, M., Wang, W., Han, S., Rui, X., Chen, X., Jiang, M., Zhang, Q., Wu, J., Li, W., Structural characterization and antioxidant property of released exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus SRFM-1. Carbohydr. Polym. 173 (2017), 654–664.
60. Mendes, S.F., dos Santos, O. Jr., Barbosa, A.M., Vasconcelos, A.F., Aranda-Selverio, G., Monteiro, N.K., Dekker, R.F., Sa Pereira, M., Tovar, A.M., Mourao, P.A., da Silva Mde, L., Sulfonation and anticoagulant activity of botryosphaeran from Botryosphaeria rhodina MAMB-05 grown on fructose. Int. J. Biol. Macromol. 45:3 (2009), 305–309.
61. Matsubara, K., Matsuura, Y., Hori, K., Miyazawa, K., An anticoagulant proteoglycan from the marine green alga, Codium pugniformis. J. Appl. Phycol. 12:1 (2000), 9–14.
62. Cornell, J.A., Response Surfaces: Designs and Analyses. 1987, Marcel Dekker, Inc.
63. Galindo, E., Peña, C., Núñez, C., Segura, D., Espín, G., Molecular and bioengineering strategies to improve alginate and polydydroxyalkanoate production by Azotobacter vinelandii. Microb. Cell Factories, 6(1), 2007, 7.
64. Palaniraj, A., Jayaraman, V., Production, recovery and applications of xanthan gum by Xanthomonas campestris. J. Food Eng. 106:1 (2011), 1–12.
65. Chao, Y., Sugano, Y., Shoda, M., Bacterial cellulose production under oxygen-enriched air at different fructose concentrations in a 50-liter, internal-loop airlift reactor. Appl. Microbiol. Biotechnol. 55:6 (2001), 673–679.
66. Cimini, D., Rosa, M.D., Schiraldi, C., Production of glucuronic acid-based polysaccharides by microbial fermentation for biomedical applications. Biotechnol. J. 7:2 (2012), 237–250.
67. Zhang, T., Li, R., Qian, H., Mu, W., Miao, M., Jiang, B., Biosynthesis of levan by levansucrase from Bacillus methylotrophicus SK 21.002. Carbohydr. Polym. 101 (2014), 975–981.
68. Wang, X.Y., Dong, J.J., Xu, G.C., Han, R.Z., Ni, Y., Enhanced curdlan production with nitrogen feeding during polysaccharide synthesis by Rhizobium radiobacter. Carbohydr. Polym. 150 (2016), 385–391.
69. Ohba, T., Uemura, K., Nabetani, H., Moderate pulsed electric field treatment enhances exopolysaccharide production by Lactococcus lactis subspecies cremoris. Process Biochem. 51:9 (2016), 1120–1128.
70. Taskin, M., Erdal, S., Canli, O., Utilization of waste loquat (Eriobotrya Japonica Lindley) kernels as substrate for scleroglucan production by locally isolated Sclerotium rolfsii. Food Sci. Biotechnol. 19:4 (2010), 1069–1075.
71. Survase, S.A., Saudagar, P.S., Singhal, R.S., Use of complex media for the production of scleroglucan by Sclerotium rolfsii MTCC 2156. Bioresour. Technol. 98:7 (2007), 1509–1512.
72. Malick, A., Khodaei, N., Benkerroum, N., Karboune, S., Production of exopolysaccharides by selected Bacillus strains: optimization of media composition to maximize the yield and structural characterization. Int. J. Biol. Macromol. 102 (2017), 539–549.