Comparative effects of nisin and monensin on pure cultures of rumen bacteria

Abstract

Nisin is a low molecular weight bacteriocin which is produced by Lactococcus lactis. Literature about the effects of nisin on pure cultures of rumen bacteria is scarce. The objective of the present study was to investigate the comparative effects of nisin and monensin on pure cultures of some Gram-positive and Gram-negative rumen bacteria. The antibacterial activity assays of nisin and monensin were carried out using broth microdilution method in anaerobic conditions. Antibacterial effect of monensin on Gram-positive rumen bacteria was higher than nisin. Ruminococcus albus and Eubacterium ruminantium were the most sensitive bacteria to monensin. Growth of these bacteria was inhibited completely by monensin, at 6 and 12 µg/mL concentrations respectively. Nisin exhibited stimulatory effects on R. albus, E. ruminantium and, Streptecoccus bovis (p<0.05), unlike monensin.  Both nisin and monensin showed potential antibacterial activity on Ruminococcus flavefaciens and Butyrivibrio fibrisolvens (p<0.05), although they did not inhibit these bacteria completely. Nisin and monensin also did not show inhibitory effect on Methanobacterium formicicum, however the potential antimicrobial activity of monensin on this methanogen was more evident. Gram-negative rumen bacteria, Megasphaera elsdenii and Fibrobacter succinogenes, were resistant to both of nisin and monesin. It was concluded that the different effects of nisin and monensin particularly on some Gram-positive rumen bacteria may be responsible for their inconsistent effects on ruminal fermentation.

Keywords

• Antibacterial,nisin,Minimum inhibitory concentration (MIC),monensin,rumen bacteria

Nisin ve monensinin rumen bakterilerinin saf kültürleri üzerine karşılaştırmalı etkileri

Öz

Nisin, Lactococcus lactis tarafından üretilen düşük moleküler ağırlıklı bir bakteriyosindir. Nisinin rumen bakterilerinin saf kültürleri üzerine etkileri hakkında literatür sınırlıdır. Bu çalışmanın amacı, nisin ve monensinin bazı Gram-pozitif ve Gram-negatif rumen bakterilerinin saf kültürleri üzerine karşılaştırmalı etkilerini araştırmaktır. Nisin ve monensinin antibakteriyal aktivite deneyleri, anaerobik koşullarda mikrodilüsyon yöntemi kullanılarak yapılmıştır. Monensinin Gram-pozitif rumen bakterileri üzerine antibakteriyal etkisi nisinden daha yüksek bulunmuştur. Ruminococcus albus ve Eubacterium ruminantium monensine karşı en duyarlı bakteriler olarak belirlenmiştir. Bu bakterilerin büyümesi,  monensin tarafından sırasıyla 6 ve 12 µg/mL konsantrasyonlarında tamamen baskılanmıştır. Nisin, monensinden farklı olarak R. albus, E. ruminantium ve Streptecoccus bovis üzerine uyarıcı etkiler göstermiştir (p<0,05). Hem nisin hem de monensin, Ruminococcus flavefaciens ve Butyrivibrio fibrisolvens üzerine potansiyel antibakteriyal aktivite sergilemişler (p<0,05), ancak bu bakterileri tamamen baskılamamışlardır. Nisin ve monensin ayrıca Methanobacterium formicicum üzerine baskılayıcı etki göstermemekle birlikte, monensinin bu methanojen üzerine potansiyel antimikrobiyal etkinliğinin daha belirgin olduğu gözlenmiştir. Gram-negatif rumen bakterileri olan Megasphaera elsdenii ve Fibrobacter succinogenes’in, hem nisin hem de monesine karşı dirençli oldukları belirlenmiştir. Nisin ve monensinin özellikle bazı Gram-pozitif rumen bakterileri üzerine olan farklı etkilerinin ruminal fermentasyon üzerine uyumlu olmayan etkilerinden sorumlu olabileceği sonucuna varılmıştır.

Anahtar Kelimeler

• Antibakteriyal,nisin,Minimal inhibitör konsantrasyon (MİK),monensin,rumen bakterileri

Kaynakça

1. 1. Aura AM (2008): Microbial metabolism of dietary phenolic compounds in the colon. Phytochem Rev, 7: 407–429.
2. 2. Breukink E, de Kruijff B (1999): The lantibiotic nisin, a special case or not? BBA-Biomembranes 1462, 223–234.
3. 3. Brulc JM, Antonopoulos DA, Miller ME, Wilson MK, Yannarell AC, Dinsdale EA, Edwards RE, Frank, ED, Emerson JB, Wacklin P, Coutinho PM, Henrissat B, Nelson KE, White BA (2009): Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci USA, 106, 1948–1953.
4. 4. Callaway TR, De Melo AMC, Russell JB (1997): The effect of nisin and monensin on ruminal fermentations in vitro. Curr Microbiol, 35, 90–96.
5. 5. Castillejos L, Calsamiglia S, Ferret A, Losa R (2007): Effects of dose and adaptation time of a specific blend of essential oil compounds on rumen fermentation. Anim Feed Sci Tech, 132, 186–201.
6. 6. Chalupa W (1977): Manipulating rumen fermentation. J Anim Sci, 46, 585–599.
7. 7. Chung KT, Dickson JS, Crouse JD (1989): Effects of nisin on growth of bacteria attached to meat. Appl Environ Microbiol, 55, 1329–1333.
8. 8. CLSI (Clinical and Laboratory Standards Institute) (2016): Performance Standards for Antimicrobial Susceptibility Testing: 26th Informational Supplement. In: M100-S26, CLSI, Wayne, PA.

9. 9. Dawson KA, Boling JA (1984): Factors affecting resistance of monensin-resistant and sensitive strains of Bacteroides ruminicola. Can J Anim Sci, 64, 132–133.
10. 10. DeVuyst L (1994): Nisin production variability between natural Lactococcus lactis subsp. lactis strains. Biotechnol Lett, 16, 287–292.
11. 11. Henderson C, Stewart CS, Nekrep FV (1981): The effect of monensin on pure and mixed cultures of rumen bacteria. J Appl Bacteriol, 51, 159–169.
12. 12. Jack RW, Tagg JR, Ray B (1995): Bacteriocins of Gram-positive bacteria. Microbiol Rev, 59, 171–200.
13. 13. Jalc D, Lauková A (2002): Effect of nisin and monensin on rumen fermentation in the artificial rumen. Berl Munch Tierarztl, 115, 6–10.
14. 14. Jami E, Mizrahi I (2012): Composition and similarity of bovine rumen microbiota across individual animals. Plos One, 7, e33306.
15. 15. Kang MS, Oh JS, Kang IC, Hong SJ, Choi CH (2008): Inhibitory effect of methyl gallate and gallic acid on oral bacteria. J Microbiol, 46, 744–750.
16. 16. Kišidayová S, Laukova A, Jalč D (2009): Comparison of nisin and monensin effects on ciliate and selected bacterial populations in artificial rumen. Folia Microbiol, 54, 527–532.
17. 17. Ko HH, Lareu RR, Dix BR, Hughes JD (2018): In vitro antibacterial effects of statins against bacterial pathogens causing skin infections. Eur J Clin Microbiol, 37, 1125–1135.
18. 18. Mantovani HC, Russell JB (2001): Nisin resistance of Streptococcus bovis. Appl Environ Microbiol, 67, 808–813.
19. 19. Nagaraja TG, Taylor MB (1987): Susceptibility and resistance of ruminal bacteria to antimicrobial feed additives. Appl Environ Microbiol, 53, 1620–1625.
20. 20. Oeztuerk H, Emre B, Sagmanligil V, Piskin I, Fidanci UR, Pekcan M (2010): Effects of nisin and propolis on ruminal fermentation in vitro. J Anim Vet Adv, 9, 2752–2758.
21. 21. OJEU (2003): OJEU Regulation (EC) No 1831/2003 of the European Parliament and the Council of 22 September 2003 on Additives for Use in Animal Nutrition. Official Journal of European Union. Page L268/36 in OJEU of 18/10/2003.
22. 22. Orpin CG (1976): Studies on the rumen flagellate Sphaeromonas communis. J Gen Microbiol, 94, 270–280.
23. 23. Patra AK, Stiverson J, Yu Z (2012): Effects of quillaja and yucca saponins on communities and select populations of rumen bacteria and archaea, and fermentation in vitro. J Appl Microbiol, 113, 1329–1340.
24. 24. Pol IE, Smid EJ (1999): Combined action of nisin and carvacrol on Bacillus cereus and Listeria monocytogenes. Lett Appl Microbiol, 29, 166–170.
25. 25. Russell JB, Mantovani HC (2002): The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. J Mol Microb Biotech, 4, 347–355.
26. 26. Russell JB, Strobel HJ (1989): Mini-Review: The effect of ionophores on ruminal fermentation. Appl Environ Microbiol, 55, 1–6.
27. 27. Rychlik JL, Russell JB (2002): Bacteriocin-like activity of Butyrivibrio fibrisolvens JL5 and its effect on other ruminal bacteria and ammonia production. Appl Environ Microbiol, 68, 1040–1046.
28. 28. Severina E, Severin A, Tomasz A (1998): Antibacterial efficacy of nisin against multidrug-resistant Gram-positive pathogens. J Antimicrob Chemoth, 41, 341–347.
29. 29. Shen J, Liu Z, Yu Z, Zhu W (2017): Monensin and nisin affect rumen fermentation and microbiota differently in vitro. Front Microbiol, 8, 1111.
30. 30. Slyter LL, Tung RS, Kung Jr L (1992): Effect of monensin and lysocellin on growth and fermentation by pure cultures of ruminal bacteria. J Appl Anim Res, 1, 1–12.