Endolysin LysSA97 is synergistic with carvacrol in controlling Staphylococcus aureus in foods

International Journal of Food Microbiology

Volumn 244, Issue , 2017, Pages 19-26

  Chang, Yoonjee ^a   Yoon, Hyunjin ^b   Kang, Dong Hyun ^a,c,d   Chang, Pahn Shick ^a,c   Ryu, Sangryeol ^a,c,d  

^a Seoul National University   (South Korea)

^b Ajou University   (South Korea)

^c Seoul National University   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

Carvacrol; Endolysin; Staphylococcus aureus; Synergistic effect

Indexed keywords

BACTERICIDE; CARVACROL; CINNAMALDEHYDE; CINNAMIC ACID; ESSENTIAL OIL; HYDROLASE; LYSSA97 ENDOLYSIN; PEPTIDOGLYCAN; THYMOL; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BIOLOGICAL CONTROL AGENT; ENDOLYSIN; PROTEINASE; TERPENE;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL VIABILITY; BACTERIOLYSIS; BACTERIUM CONTAMINATION; BACTERIUM CULTURE; BEEF; BIOLOGICAL CONTROL AGENT; COLONY FORMING UNIT; DRUG EFFICACY; DRUG POTENTIATION; FOOD CONTAMINATION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MILK; MINIMUM INHIBITORY CONCENTRATION; ANIMAL; BACTERIOPHAGE; BOVINE; DRUG EFFECTS; FOOD CONTROL; FOODBORNE DISEASES; GENETICS; MEAT; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHARMACOLOGY; STAPHYLOCOCCAL INFECTIONS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOPHAGES; BIOLOGICAL CONTROL AGENTS; CATTLE; DRUG SYNERGISM; ENDOPEPTIDASES; FOOD MICROBIOLOGY; FOODBORNE DISEASES; MEAT; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MILK; MONOTERPENES; STAPHYLOCOCCAL INFECTIONS;

EID: 85008230646     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2016.12.007     Document Type: Article

References (43)

1. Abaev, I., Foster-Frey, J., Korobova, O., Shishkova, N., Kiseleva, N., Kopylov, P., Pryamchuk, S., Schmelcher, M., Becker, S.C., Donovan, D.M., Staphylococcal phage 2638A endolysin is lytic for Staphylococcus aureus and harbors an inter-lytic-domain secondary translational start site. Appl. Microbiol. Biotechnol. 97 (2013), 3449–3456.
2. Aiyegoro, O.A., Okoh, A.I., Use of bioactive plant products in combination with standard antibiotics: Implications in antimicrobial chemotherapy. J. Med. Plant Res. 3 (2009), 1147–1152.
3. Baba, T., Bae, T., Schneewind, O., Takeuchi, F., Hiramatsu, K., Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J. Bacteriol. 190 (2008), 300–310.
4. Bai, J., Kim, Y., Ryu, S., Lee, J.H., Biocontrol and rapid detection of food-borne pathogens using bacteriophages and endolysins. Front. Microbiol. 7 (2016), 1–15.
5. Becker, S.C., Foster-Frey, J., Donovan, D.M., The phage K lytic enzyme LysK and lysostaphin act synergistically to kill MRSA. FEMS Microbiol. Lett. 287 (2008), 185–191.
6. Bennis, S., Chami, F., Chami, N., Bouchikhi, T., Remmal, A., Surface alteration of Saccharomyces cerevisiae induced by thymol and eugenol. Lett. Appl. Microbiol. 38 (2004), 454–458.
7. Blaiotta, G., Ercolini, D., Pennacchia, C., Fusco, V., Casaburi, A., Pepe, O., Villani, F., PCR detection of staphylococcal enterotoxin genes in Staphylococcus spp. strains isolated from meat and dairy products. Evidence for new variants of seG and seI in S. aureus AB-8802. J. Appl. Microbiol. 97 (2004), 719–730.
8. Burt, S., Essential oils: their antibacterial properties and potential applications in foods-a review. Int. J. Food Microbiol. 94 (2004), 223–253.
9. Chang, Y., Ryu, S., Characterization of a novel cell wall binding domain-containing Staphylococcus aureus endolysin LysSA97. Appl. Microbiol. Biotechnol., 2016, 10.1007/s00253-016-7747-6.
10. Chang, Y., Lee, J.H., Shin, H., Heu, S., Ryu, S., Characterization and complete genome sequence analysis of Staphylococcus aureus bacteriophage SA12. Virus Genes 47 (2013), 389–393.
11. Chang, Y., Shin, H., Lee, J.H., Park, C.J., Paik, S.Y., Ryu, S., Isolation and genome characterization of the virulent Staphylococcus aureus bacteriophage SA97. Viruses 7 (2015), 5225–5242.
12. Chen, H., Davidson, P.M., Zhong, Q., Impacts of sample preparation methods on solubility and antilisterial characteristics of essential oil components in milk. Appl. Environ. Microbiol. 80 (2014), 907–916.
13. Dack, G.M., Staphylococci in relation to food poisoning. Am. J. Public Health Nations Health 27 (1937), 440–443.
14. Daniel, A., Euler, C., Collin, M., Chahales, P., Gorelick, K.J., Fischetti, V.A., Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 54 (2010), 1603–1612.
15. Denyer, S.P., Mechanisms of action of biocides. Int. Biodeterior. 26 (1990), 89–100.
16. Díez-Martínez, R., de Paz, H., Bustamante, N., García, E., Menéndez, M., García, P., Improving the lethal effect of Cpl-7, a pneumococcal phage lysozyme with broad bactericidal activity, by inverting the net charge of its cell wall-binding module. Antimicrob. Agents Chemother. 57 (2013), 5355–5365.
17. Dinges, M.M., Orwin, P.M., Schlievert, P.M., Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13 (2000), 16–34.
18. Djenane, D., Yanguela, J., Amrouche, T., Boubrit, S., Boussad, N., Roncales, P., Chemical composition and antimicrobial effects of essential oils of Eucalyptus globulus, Myrtus communis and Satureja hortensis against Escherichia coli O157:H7 and Staphylococcus aureus in minced beef. Food Sci. Technol. Int. 17 (2011), 505–515.
19. Faleiro, M.L., The mode of antibacterial action of essential oils. Mendez-Vilas, A., (eds.) Science Against Microbial Pathogens: Communicating Current Research and Technological Advances, 2011, Brown walker press, Florida, 1143–1156.
20. Garcia, P., Martinez, B., Rodriguez, L., Rodriguez, A., Synergy between the phage endolysin LysH5 and nisin to kill Staphylococcus aureus in pasteurized milk. Int. J. Food Microbiol. 141 (2010), 151–155.
21. Gaysinsky, S., Taylor, T.M., Davidson, P.M., Bruce, B.D., Weiss, J., Antimicrobial efficacy of eugenol microemulsions in milk against Listeria monocytogenes and Escherichia coli O157:H7. J. Food Prot. 70 (2007), 2631–2637.
22. Ginex, T., Spyrakis, F., Cozzini, P., FADB: a food additive molecular database for in silico screening in food toxicology. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 31 (2014), 792–798.
23. Horgan, M., O'Flynn, G., Garry, J., Cooney, J., Coffey, A., Fitzgerald, G.F., Ross, R.P., McAuliffe, O., Phage lysin LysK can be truncated to its CHAP domain and retain lytic activity against live antibiotic-resistant Staphylococci. Appl. Environ. Microbiol. 75 (2009), 872–874.
24. Landry, K.S., Chang, Y., McClements, D.J., McLandsborough, L., Effectiveness of a novel spontaneous carvacrol nanoemulsion against Salmonella enterica Enteritidis and Escherichia coli O157:H7 on contaminated mung bean and alfalfa seeds. Int. J. Food Microbiol. 187 (2014), 15–21.
25. Manoharadas, S., Witte, A., Blasi, U., Antimicrobial activity of a chimeric enzybiotic towards Staphylococcus aureus. J. Biotechnol. 139 (2009), 118–123.
26. McClements, D.J., Rao, J., Food-grade nanoemulsions: formulation, fabrication, properties, performance, biological fate, and potential toxicity. Crit. Rev. Food Sci. Nutr. 51 (2011), 285–330.
27. Nelson, D., Loomis, L., Fischetti, V.A., Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 4107–4112.
28. Nostro, A., Papalia, T., Antimicrobial activity of carvacrol: current progress and future prospectives. Recent Pat. Antiinfect. Drug Discov. 7 (2012), 28–35.
29. Obeso, J.M., Martinez, B., Rodriguez, A., Garcia, P., Lytic activity of the recombinant staphylococcal bacteriophage PhiH5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128 (2008), 212–218.
30. Park, K.H., Kurokawa, K., Zheng, L., Jung, D.J., Tateishi, K., Jin, J.O., Ha, N.C., Kang, H.J., Matsushita, M., Kwak, J.Y., Takahashi, K., Lee, B.L., Human serum mannose-binding lectin senses wall teichoic acid glycopolymer of Staphylococcus aureus, which is restricted in infancy. J. Biol. Chem. 285 (2010), 27167–27175.
31. Rogosic, M., Mencer, H.J., Gomzi, Z., Polydispersity index and molecular weight distributions of polymers. Eur. Polym. J. 32 (1996), 1337–1344.
32. Roller, S., Seedhar, P., Carvacrol and cinnamic acid inhibit microbial growth in fresh-cut melon and kiwifruit at 4 °C and 8 °C. Lett. Appl. Microbiol. 35 (2002), 390–394.
33. Schmelcher, M., Tchang, V.S., Loessner, M.J., Domain shuffling an module engineering of Listeria phage endolysins for enhanced lytic activity and binding affinity. Microb. Biotechnol. 4 (2011), 651–662.
34. Schmelcher, M., Donovan, D.M., Loessner, M.J., Bacteriophage endolysins as novel antimicrobials. Future Microbiol 7 (2012), 1147–1171.
35. Shah, B., Davidson, P.M., Zhong, Q.X., Nanodispersed eugenol has improved antimicrobial activity against Escherichia coli O157:H7 and Listeria monocytogenes in bovine milk. Int. J. Food Microbiol. 161 (2013), 53–59.
36. Shan, B., Cai, Y.Z., Brooks, J.D., Corke, H., Antibacterial properties and major bioactive components of cinnamon stick (Cinnamomum burmannii): activity against foodborne pathogenic bacteria. J. Agric. Food Chem. 55 (2007), 5484–5490.
37. Shimizu, K., Measurement of biological particles by laser light scattering. Jpn. J. Med. Electr. Biol. Eng. 19 (1981), 389–390.
38. Singh, P.K., Tack, B.F., McCray, P.B. Jr., Welsh, M.J., Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am. J. Phys. Lung Cell. Mol. Phys. 279 (2000), L799–L805.
39. Smith-Palmer, A., Stewart, L., Fyfe, L., The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiol. 18 (2001), 463–470.
40. Souza, E.L., Barros, J.C., Oliveira, C.E.V., Conceicao, M.L., Influence of Origanum vulgare L. essential oil on enterotoxin production, membrane permeability and surface characteristics of Staphylococcus aureus. Int. J. Food Microbiol. 137 (2010), 308–311.
41. Viazis, S., Akhtar, M., Feirtag, J., Diez-Gonzalez, F., Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol. 28 (2011), 149–157.
42. White, R.L., Burgess, D.S., Manduru, M., Bosso, J.A., Comparison of three different in vitro methods of detecting synergy: time-kill, checkerboard, and E test. Antimicrob. Agents Chemother. 40 (1996), 1914–1918.
43. Yoon, S.Y., Eo, S.K., Kim, Y.S., Lee, C.K., Han, S.S., Antimicrobial activity of Gnoderma lucidum extract alone and in combination with some antibiotics. Arch. Pharm. Res. 17 (1994), 438–442.