Synergistic antibacterial mechanism of the Lactobacillus crispatus surface layer protein and nisin on Staphylococcus saprophyticus

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Sun, Zhilan ^a   Li, Pengpeng ^a   Liu, Fang ^a   Bian, Huan ^a   Wang, Daoying ^a,b   Wang, Xiaomeng ^a   Zou, Ye ^a   Sun, Chong ^a   Xu, Weimin ^a,b  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; MEMBRANE PROTEIN; NISIN; S-LAYER PROTEINS;

ANIMAL; CELL MEMBRANE; CHEMISTRY; CHICKEN; CONFOCAL MICROSCOPY; DRUG EFFECT; DRUG POTENTIATION; ELECTRON MICROSCOPY; FLOW CYTOMETRY; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LACTOBACILLUS CRISPATUS; MEAT; MEMBRANE POTENTIAL; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; MICROBIOLOGY; STAPHYLOCOCCUS SAPROPHYTICUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CELL MEMBRANE; CHICKENS; DRUG SYNERGISM; FLOW CYTOMETRY; LACTOBACILLUS CRISPATUS; MEAT; MEMBRANE GLYCOPROTEINS; MEMBRANE POTENTIALS; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NISIN; STAPHYLOCOCCUS SAPROPHYTICUS;

EID: 85038959058     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-00303-8     Document Type: Article

References (44)

1. Coton, E. et al. Biodiversity of coagulase-negative staphylococci in French cheeses, dry fermented sausages, processing environments and clinical samples. Int. J. Food Microbial. 2, 221-229 (2010).
2. Flores-Mireles, A. L., Walker, J. N., Caparon, M. & Hultgren, S. J. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat. Rev. Microbiol. 13, 269-284 (2015).
3. von Eiff, C., Arciola, C. R., Montanaro, L., Becker, K. & Campoccia, D. Emerging Staphylococcus species as new pathogens in implant infections. Int. J. Artif. Organs 29, 360-367 (2006).
4. Talon, R. & Leroy, S. Diversity and safety hazards of bacteria involved in meat fermentations. Meat Sci. 89, 303-309 (2011).
5. Saeidi, S. et al. Antibacterial activity of silver nanoparticles produced by Rosmarinus officinalis L leaf extract against some human pathogenic bacteria. Int. J. Adv. Biol. Biome. Res 4, 108-111 (2016).
6. Lucera, A., Costa, C., Conte, A. & Del Nobile, M. A. Food applications of natural antimicrobial compounds. Front Microbiol 3, 287 (2012).
7. Gharsallaoui, A., Oulahal, N., Joly, C. & Degraeve, P. Nisin as a food preservative: part 1: physicochemical properties, antimicrobial activity, and main uses. Crit. Rev. Food Sci 56, 1262-1274 (2016).
8. Delves-Broughton. Nisin and its application as a food preservative. Int. J. Dairy Technol. 43, 73-76 (1990).
9. Sadiq, S. et al. Potential of monolaurin based food-grade nano-micelles loaded with nisin Z for synergistic antimicrobial action against Staphylococcus aureus. LWT-Food Sci. Technol. 71, 227-233 (2016).
10. Liu, H., Pei, H., Han, Z., Feng, G. & Li, D. The antimicrobial effects and synergistic antibacterial mechanism of the combination of e-Polylysine and nisin against Bacillus subtilis. Food Control 47, 444-450 (2015).
11. Murdock, C. A., Cleveland, J., Matthews, K. R. & Chikindas, M. L. The synergistic effect of nisin and lactoferrin on the inhibition of Listeria monocytogenes and Escherichia coli O157: H7. Lett. Appl. Microbiol. 44, 255-261 (2007).
12. Pum, D., Toca-Herrera, J. L. & Sleytr, U. B. S-layer protein self-assembly. Int. J. Mol. Sci. 14, 2484-2501 (2013).
13. Hynönen, U. & Palva, A. Lactobacillus surface layer proteins: structure, function and applications. Appl. Microbiol. Biotechnol. 97, 5225-5243 (2013).
14. Uroic, K. et al. The role of S-layer in adhesive and immunomodulating properties of probiotic starter culture Lactobacillus brevis D6 isolated from artisanal smoked fresh cheese. LWT-Food Sci. Technol. 69, 623-632 (2016).
15. Acosta, M. P., Palomino, M. M., Allievi, M. C., Rivas, C. S. & Ruzal, S. M. Murein hydrolase activity in the surface layer of Lactobacillus acidophilus ATCC 4356. Appl. Environ. Microbiol. 4, 7824-7827 (2008).
16. Acosta, M. P., Ruzal, S. M., Allievi, M. C., Palomino, M. M. & Rivas, C. S. Synergistic effects of the Lactobacillus acidophilus surface layer and nisin on bacterial growth. Appl. Environ. Microbiol. 76, 974-977 (2010).
17. Punyauppa-path, S., Phumkhachorn, P. & Rattanachaikunsopon, P. Nisin: production and mechanism of antimicrobial action. Int. J. Curr. Res. Rev 7, 47 (2015).
18. Hart, P. 't, Oppedijk, S. F., Breukink, E. & Martin, N. I. New insights into nisin's antibacterial mechanism revealed by binding studies with synthetic lipid II analogues. Biochemistry 55, 232-237 (2015).
19. Sun, Z. et al. Characterization of a S-layer protein from Lactobacillus crispatus K313 and the domains responsible for binding to cell wall and adherence to collagen. Appl. Microbiol. Biotechnol. 97, 1941-1952 (2013).
20. Padmavathy, N. & Vijayaraghavan, R. Enhanced bioactivity of ZnO nanoparticles-an antimicrobial study. Sci. Technol. Adv. Mat. 9, 43-48 (2016).
21. Teethaisong, Y. et al. Synergistic activity and mechanism of action of Stephania suberosa Forman extract and ampicillin combination against ampicillin-resistant Staphylococcus aureus. J. Biomedi. sci. (1), 1 (2014).
22. Li, J. et al. Evaluation of ultrasound-induced damage to Escherichia coli and Staphylococcus aureus by flow cytometry and transmission electron microscopy. Appl. Environ. Microbiol. 82, 1828-1837 (2016).
23. Liu, F. et al. Synergistic antibacterial effect of the combination of e-polylysine and nisin against Enterococcus faecalis. J. Food. Protect. 78, 2200-2206 (2015).
24. Pantazi, D., Papavergou, A., Pournis, N., Kontominas, M. G. & Savvaidis, I. N. Shelf-life of chilled fresh Mediterranean swordfish (Xiphias gladius) stored under various packaging conditions: Microbiological, biochemical and sensory attributes. Food Microbiol. 25, 136-143 (2008).
25. Hultman, J., Rahkila, R., Ali, J., Rousu, J. & Björkroth, K. J. Meat processing plant microbiome and contamination patterns of coldtolerant bacteria causing food safety and spoilage risks in the manufacture of vacuum-packaged cooked sausages. Appl. Environ. Microbiol. 81, 7088-7097 (2015).
26. Lavieri, N. A. et al. Control of Listeria monocytogenes on alternatively cured ready-to-eat ham using natural antimicrobial ingredients in combination with post-lethality interventions. J. Food Process. Pres 6, 1 (2015).
27. Sung, S. Y. et al. Antimicrobial agents for food packaging applications. Trends Food Sci. Tech 33, 110-123 (2013).
28. Inanç, T. & Maskan, M. The potential application of plant essential oils/extracts as natural preservatives in oils during processing: a review. J. Food Sci. Eng 2, 1 (2012).
29. Li, T., Li, J., Hu, W., Zhang, X., Li, X. & Zhao, J. Shelf-life extension of crucian carp (Carassius auratus) using natural preservatives during chilled storage. Food Chem. 135, 140-145 (2012).
30. Branen, J. K. & Davidson, P. M. Enhancement of nisin, lysozyme, and monolaurin antimicrobial activities by ethylenediaminetetraacetic acid and lactoferrin. Int. J. Food Microbiol. 90, 63-74 (2004).
31. Bag, A. & Chattopadhyay, R. R. Evaluation of synergistic antibacterial and antioxidant efficacy of essential oils of spices and herbs in combination. PloS one 10, e0131321 (2015).
32. Pillet, F., Formosa-Dague, C., Baaziz, H., Dague, E. & Rols, M. P. Cell wall as a target for bacteria inactivation by pulsed electric fields. Sci. Rep. 6 (2016).
33. Szweda, P. et al. Peptidoglycan hydrolases-potential weapons against Staphylococcus aureus. Appl. Microbiol. Biotechnol. 5, 1157-1174 (2012).
34. Kong, M., Chen, X. G., Xing, K. & Park, H. J. Antimicrobial properties of chitosan and mode of action: a state of the art review. Int. J. Food Microbiol. 1, 51-63 (2010).
35. Loessner, M. J., Kramer, K., Ebel, F. & Scherer, S. C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol. Microbiol 2, 335-349 (2002).
36. Meng, J., Gao, S. M., Zhang, Q. X. & Lu, R. R. Murein hydrolase activity of surface layer proteins from Lactobacillus acidophilus against Escherichia coli. Int. J. Biol. Macromol. 79, 527-532 (2015).
37. Raafat, D., Von Bargen, K., Haas, A. & Sahl, H. G. Insights into the mode of action of chitosan as an antibacterial compound. Appl. Environ. Microbiol. 12, 3764-3773 (2008).
38. Baneyx, F. & Mujacic, M. Recombinant protein folding and misfolding in Escherichia coli. Nature Biotechnol. 11, 1399-1408 (2004).
39. Guo, T., Xin, Y., Zhang, C., Ouyang, X. & Kong, J. The potential of the endolysin Lysdb from Lactobacillus delbrueckii phage for combating Staphylococcus aureus during cheese manufacture from raw milk. Appl. Microbiol. Biotechnol. 100, 3545-3554 (2016).
40. Liu, G. et al. Antibacterial mechanism of bifidocin A, a novel broad-spectrum bacteriocin produced by Bifidobacterium animalis BB04. Food Control 62, 309-316 (2016).
41. Brannan, R. G. Effect of grape seed extract on physicochemical properties of ground, salted, chicken thigh meat during refrigerated storage at different relative humidity levels. J. Food Sci 1, C36-C40 (2008).
42. Barmpalia, I. M. et al. Effect of antimicrobials as ingredients of pork bologna for Listeria monocytogenes control during storage at 4 or 10 C. Food Microbiol. 2, 205-211 (2005).
43. Aymerich, T. et al. Application of enterocins as biopreservatives against Listeria innocua in meat products. J. Food Protect. 6, 721-726 (2000).
44. Wang, D. et al. Postmortem changes in actomyosin dissociation, myofibril fragmentation and endogenous enzyme activities of grass carp (Ctenopharyngodon idellus) muscle. Food Chem. 197, 340-344 (2016).