Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay

Autoři: Benjamin W. Bauer aff001;  Sheeana Gangadoo aff001;  Yadav Sharma Bajagai aff001;  Thi Thu Hao Van aff002;  Robert J. Moore aff002;  Dragana Stanley aff001
Působiště autorů: Institute for Future Farming Systems, Central Queensland University, Rockhampton, Queensland, Australia aff001;  RMIT University, School of Science, Bundoora, Victoria, Australia aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0216853


Food borne illnesses have a world-wide economic impact and industries are continuously developing technologies to reduce the spread of disease caused by microorganisms. Antimicrobial growth promoters (AGPs) have been used to decrease microbiological infections in animals and their potential transfer to humans. In recent years there has been a global trend to remove AGPs from animal feed in an attempt to reduce the spread of antimicrobial resistant genes into the human population. Phytobiotics, such as oregano powder, are one of the potential replacements for AGPs due to their well-established antimicrobial components. 16S rRNA gene amplicons were used to determine the effect of oregano powder (1% w/v) on the microbiota of mixed bacterial cell cultures, which were obtained from the ceca of traditionally grown meat chickens (broilers). Oregano powder had a mild effect on the microbial cell cultures increasing Enterococcus faecium, rearranging ratios of members in the genus Lactobacillus and significantly reducing the genus Streptococcus (p = 1.6e-3). Beneficial short chain fatty acids (SCFA), acetic and butyric acid, were also significantly increased in oregano powder supplemented cultures. These results suggest that oregano powder at a concentration of 1% (w/v) may have beneficial influences on mixed microbial communities and SCFA production.

Klíčová slova:

Bacteria – Enterococcus – Filter sterilization – Gastrointestinal tract – Lactobacillus – Livestock – Microbiome – Streptococcus


1. Gandhi M, Chikindas ML. Listeria: A foodborne pathogen that knows how to survive. Int J Food Microbiol. 2007;113(1):1–15. doi: 10.1016/j.ijfoodmicro.2006.07.008 WOS:000243454600001. 17010463

2. Crisol-Martinez E, Stanley D, Geier MS, Hughes RJ, Moore RJ. Understanding the mechanisms of zinc bacitracin and avilamycin on animal production: linking gut microbiota and growth performance in chickens. Appl Microbiol Biotechnol. 2017;101(11):4547–59. doi: 10.1007/s00253-017-8193-9 WOS:000402008300017. 28243710

3. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489(7415):220–30. doi: 10.1038/nature11550 22972295; PubMed Central PMCID: PMC3577372.

4. Emborg HD, Ersboll AK, Heuer OE, Wegener HC. The effect of discontinuing the use of antimicrobial growth promoters on the productivity in the Danish broiler production. Prev Vet Med. 2001;50(1–2):53–70. doi: 10.1016/s0167-5877(01)00218-5 WOS:000170096000004. 11448495

5. Casewell M, Friis C, Marco E, McMullin P, Phillips I. The European ban on growth-promoting antibiotics and emerging consequences for human and animal health. J Antimicrob Chemoth. 2003;52(2):159–61. Epub 2003/07/03. doi: 10.1093/jac/dkg313 12837737.

6. Turnidge J. The Use of Antibiotics in Food-Producing Animals: Antibiotic-Resistant Bacteria in Animals and Humans. In: Commonwealth Department of Agrictulture FaF, editor. Canberra ACT 2601: Australian Government; 1999.

7. Jensen HH, Hayes DJ. Impact of Denmark's ban on antimicrobials for growth promotion. Curr Opin Microbiol. 2014;19:30–6. Epub 2014/07/06. doi: 10.1016/j.mib.2014.05.020 24997397.

8. Turnidge J. Antibiotic use in animals—prejudices, perceptions and realities. J Antimicrob Chemoth. 2004;53(1):26–7. Epub 2003/12/06. doi: 10.1093/jac/dkg493 14657093.

9. Betancourt L, Rodriguez F, Phandanouvong V, Ariza-Nieto C, Hume M, Nisbet D, et al. Effect of Origanum chemotypes on broiler intestinal bacteria. Poult Sci. 2014;93(10):2526–35. Epub 2014/07/30. doi: 10.3382/ps.2014-03944 25071230.

10. Karimi A, Yan F, Coto C, Park JH, Min Y, Lu C, et al. Effects of level and source of oregano leaf in starter diets for broiler chicks. J Appl Poult Res. 2010;19(2):137–45. doi: 10.3382/japr.2009-00088

11. Windisch W, Schedle K, Plitzner C, Kroismayr A. Use of phytogenic products as feed additives for swine and poultry. J Anim Sci. 2008;86(14 Suppl):E140–8. Epub 2007/12/13. doi: 10.2527/jas.2007-0459 18073277.

12. Onrust L, Ducatelle R, Van Driessche K, De Maesschalck C, Vermeulen K, Haesebrouck F, et al. Steering Endogenous Butyrate Production in the Intestinal Tract of Broilers as a Tool to Improve Gut Health. Front Vet Sci. 2015;2:75. Epub 2016/01/07. doi: 10.3389/fvets.2015.00075 26734618; PubMed Central PMCID: PMC4682374.

13. Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, et al. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemoth. 2004;53(1):28–52. Epub 2003/12/06. doi: 10.1093/jac/dkg483 14657094.

14. Brenes A, Roura E. Essential oils in poultry nutrition: Main effects and modes of action. Anim Feed Sci Technol. 2010;158(1–2):1–14. doi: 10.1016/j.anifeedsci.2010.03.007

15. Giannenas I, Florou-Paneri P, Papazahariadou M, Christaki E, Botsoglou NA, Spais AB. Effect of dietary supplementation with oregano essential oil on performance of broilers after experimental infection with Eimeria tenella. Arch Anim Nutr. 2003;57(2):99–106. doi: 10.1080/0003942031000107299 12866780

16. Boskabady MH, Jalali S. Effect of carvacrol on tracheal responsiveness, inflammatory mediators, total and differential WBC count in blood of sensitized guinea pigs. Exp Biol Med. 2013;238(2):200–8. Epub 2013/04/12. doi: 10.1177/1535370212474604 23576802.

17. Arigesavan K, Sudhandiran G. Carvacrol exhibits anti-oxidant and anti-inflammatory effects against 1, 2-dimethyl hydrazine plus dextran sodium sulfate induced inflammation associated carcinogenicity in the colon of Fischer 344 rats. BBRC. 2015;461(2):314–20. doi: 10.1016/j.bbrc.2015.04.030 25881504.

18. Lima Mda S, Quintans-Junior LJ, de Santana WA, Martins Kaneto C, Pereira Soares MB, Villarreal CF. Anti-inflammatory effects of carvacrol: evidence for a key role of interleukin-10. Eur J Pharmacol. 2013;699(1–3):112–7. Epub 2012/12/12. doi: 10.1016/j.ejphar.2012.11.040 23220159.

19. Silva FV, Guimaraes AG, Silva ER, Sousa-Neto BP, Machado FD, Quintans-Junior LJ, et al. Anti-inflammatory and anti-ulcer activities of carvacrol, a monoterpene present in the essential oil of oregano. J Med Food. 2012;15(11):984–91. Epub 2012/08/16. doi: 10.1089/jmf.2012.0102 22892022.

20. Dagli Gul AS, Fadillioglu E, Karabulut I, Yesilyurt A, Delibasi T. The effects of oral carvacrol treatment against H2O2 induced injury on isolated pancreas islet cells of rats. Islets. 2013;5(4):149–55. Epub 2013/07/03. doi: 10.4161/isl.25519 23817295.

21. De Vincenzi M, Stammati A, De Vincenzi A, Silano M. Constituents of aromatic plants: carvacrol. Fitoterapia. 2004;75(7–8):801–4. doi: 10.1016/j.fitote.2004.05.002 15567271.

22. Sivropoulou A, Papanikolaou E., Nikolaou C., Kokkini S., Lanaras T, Arsenakis M.,. Antimicrobial and cytotoxic activities of origanum essential oils. J Agr Food Chem. 1996;44:4.

23. Ultee A, Bennik MHJ, Moezelaar R. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol. 2002;68(4):1561–8. doi: 10.1128/AEM.68.4.1561-1568.2002 WOS:000174842200011. 11916669

24. Peng QY, Li JD, Li Z, Duan ZY, Wu YP. Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens. Anim Feed Sci Technol. 2016;214:148–53. doi: 10.1016/j.anifeedsci.2016.02.010

25. Yin D, Du E, Yuan J, Gao J, Wang Y, Aggrey SE, et al. Supplemental thymol and carvacrol increases ileum Lactobacillus population and reduces effect of necrotic enteritis caused by Clostridium perfringes in chickens. Sci Rep. 2017;7(1):7334. Epub 2017/08/06. doi: 10.1038/s41598-017-07420-4 28779076; PubMed Central PMCID: PMC5544757.

26. Van Immerseel F, Rood JI, Moore RJ, Titball RW. Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. Trends Microbiol. 2009;17(1):32–6. doi: 10.1016/j.tim.2008.09.005 WOS:000263016300005. 18977143

27. Mathlouthi N, Bouzaienne T, Oueslati I, Recoquillay F, Hamdi M, Urdaci M, et al. Use of rosemary, oregano, and a commercial blend of essential oils in broiler chickens: in vitro antimicrobial activities and effects on growth performance. J Anim Sci. 2012;90(3):813–23. Epub 2011/11/09. doi: 10.2527/jas.2010-3646 22064737.

28. Young JF, Stagsted J, Jensen SK, Karlsson AH, Henckel P. Ascorbic acid, alpha-tocopherol, and oregano supplements reduce stress-induced deterioration of chicken meat quality. Poult Sci. 2003;82(8):1343–51. Epub 2003/08/29. doi: 10.1093/ps/82.8.1343 12943308.

29. Bajpai VK, Baek KH, Kang SC. Control of Salmonella in foods by using essential oils: A review. Food Res Int. 2012;45(2):722–34. doi: 10.1016/j.foodres.2011.04.052 WOS:000302032200025.

30. Hyldgaard M, Mygind T, Meyer RL. Essential oils in food preservation: mode of action, synergies, and interactions with food matrix components. Front Microbiol. 2012;3:12. Epub 2012/02/01. doi: 10.3389/fmicb.2012.00012 22291693; PubMed Central PMCID: PMC3265747.

31. Lagouri V, Blekas G, Tsimidou M, Kokkini S, Boskou D. Composition and antioxidant activity of essential oils from oregano plants grown wild in Greece. Zeitschrift fur Lebensmittel-Untersuchung und -Forschung. 1993;197(1):20–3. doi: 10.1007/bf01202694

32. Olmedo R, Nepote V, Grosso NR. Antioxidant activity of fractions from oregano essential oils obtained by molecular distillation. Food Chem. 2014;156:212–9. doi: 10.1016/j.foodchem.2014.01.087 24629960.

33. Ocana-Fuentes A, Arranz-Gutierrez E, Senorans FJ, Reglero G. Supercritical fluid extraction of oregano (Origanum vulgare) essentials oils: anti-inflammatory properties based on cytokine response on THP-1 macrophages. Food Chem Toxicol. 2010;48(6):1568–75. Epub 2010/03/25. doi: 10.1016/j.fct.2010.03.026 20332013.

34. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012;336(6086):1262–7. Epub 2012/06/08. doi: 10.1126/science.1223813 22674330.

35. Lagier JC, Armougom F, Million M, Hugon P, Pagnier I, Robert C, et al. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect. 2012;18(12):1185–93. Epub 2012/10/05. doi: 10.1111/1469-0691.12023 23033984.

36. Svihus B. Function of the digestive system. J Appl Poult Res. 2014;23(2):306–14. doi: 10.3382/japr.2014-00937 WOS:000337352900022.

37. Stanley D, Hughes RJ, Moore RJ. Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease. Appl Microbiol Biot. 2014;98(10):4301–10. Epub 2014/03/20. doi: 10.1007/s00253-014-5646-2 24643736.

38. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. doi: 10.1038/nmeth.f.303 WOS:000277175100003. 20383131

39. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1. doi: 10.1093/bioinformatics/btq461 WOS:000282170000016. 20709691

40. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol. 2005;71(12):7724–36. doi: 10.1128/AEM.71.12.7724-7736.2005 WOS:000234417600011. 16332745

41. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–72. doi: 10.1128/AEM.03006-05 WOS:000238961000071. 16820507

42. Legendre P, Gallagher ED. Ecologically meaningful transformations for ordination of species data. Oecologia. 2001;129(2):271–80. doi: 10.1007/s004420100716 WOS:000171834100014. 28547606

43. Legendre P, De Caceres M. Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett. 2013;16(8):951–63. doi: 10.1111/ele.12141 WOS:000321696300001. 23809147

44. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12). doi: 10.1186/s13059-014-0550-8 WOS:000346609500022. 25516281

45. Zakrzewski M, Proietti C, Ellis JJ, Hasan S, Brion MJ, Berger B, et al. Calypso: a user-friendly web-server for mining and visualizing microbiome-environment interactions. Bioinformatics. 2017;33(5):782–3. doi: 10.1093/bioinformatics/btw725 WOS:000397265300030. 28025202

46. Kers JG, Velkers FC, Fischer EAJ, Hermes GDA, Stegeman JA, Smidt H. Host and environmental factors affecting the intestinal microbiota in chickens. Front Microbiol. 2018;9:235. Epub 2018/03/06. doi: 10.3389/fmicb.2018.00235 29503637; PubMed Central PMCID: PMC5820305.

47. Ahlman H NO. The gut as the largets endocrine organ in the body. Ann Oncol. 2001;2:6. doi: 10.1093/annonc/12.suppl_2.S63 11762354

48. Deplancke B GHR. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr. 2001;73(6):11.

49. Ursell LK, Metcalf JL, Parfrey LW, Knight R. Defining the human microbiome. Nutr Rev. 2012;70 Suppl 1:S38–44. Epub 2012/08/17. doi: 10.1111/j.1753-4887.2012.00493.x 22861806; PubMed Central PMCID: PMC3426293.

50. Seth EC, Taga ME. Nutrient cross-feeding in the microbial world. Front Microbiol. 2014;5. doi: 10.3389/fmicb.2014.00350 WOS:000338775400001. 25071756

51. Magi G, Marini E, Facinelli B. Antimicrobial activity of essential oils and carvacrol, and synergy of carvacrol and erythromycin, against clinical, erythromycin-resistant Group A Streptococci. Front Microbiol. 2015;6:165. Epub 2015/03/19. doi: 10.3389/fmicb.2015.00165 25784902; PubMed Central PMCID: PMC4347498.

52. Lakis ZM, D. Nicorescu I. Vulturescu V. Udeanu D. I. The antimicrobial activity of Thymus vulgaris and Origanum syriacum essential oils on Staphylococcus aureus, Streptococcus pneumoniae and Candida albicans. Farmacia. 2012;60(6):857–65. WOS:000315931200009.

53. Didry N, Dubreuil L., Pinkas M.,. Activity of thymol, carvacrol, cinnamaldehyde and eugenol on oral bacteria. Pharm Acta Helv. 1994;69:4.

54. Floret N, Bailly P, Thouverez M, Blanchot C, Alez-Martin D, Menget A, et al. A cluster of bloodstream infections caused by Streptococcus gallolyticus subspecies pasteurianus that involved 5 preterm neonates in a university hospital during a 2-month period. Infect Cont Hosp Ep. 2010;31(2):194–6. doi: 10.1086/650380 WOS:000273399100016. 20001733

55. Boleij A, van Gelder MMHJ, Swinkels DW, Tjalsma H. Clinical Importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis. Clin Infect Dis. 2011;53(9):870–8. doi: 10.1093/cid/cir609 WOS:000295683700015. 21960713

56. Abdulamir AS, Hafidh RR, Mahdi LK, Al-Jeboori T, Abubaker F. Investigation into the controversial association of Streptococcus gallolyticus with colorectal cancer and adenoma. Bmc Cancer. 2009;9:12. doi: 10.1186/1471-2407-9-12 WOS:000272339300002.

57. Abdulamir AS, Hafidh RR, Abu Bakar F. Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8. Mol Cancer. 2010;9:18. doi: 10.1186/1476-4598-9-18 WOS:000282464200001.

58. Rusniok C, Couve E, Da Cunha V, El Gana R, Zidane N, Bouchier C, et al. Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J Bacteriol. 2010;192(8):2266–76. doi: 10.1128/JB.01659-09 WOS:000276048300025. 20139183

59. Jordens JZ, Bates J, Griffiths DT. Faecal carriage and nosocomial spread of vancomycin-resistant Enterococcus faecium. J Antimicrob Chemoth. 1994;34(4):515–28. Epub 1994/10/01. doi: 10.1093/jac/34.4.515 7868404.

60. Scharek L, Guth J, Reiter K, Weyrauch KD, Taras D, Schwerk P, et al. Influence of a probiotic Enterococcus faecium strain on development of the immune system of sows and piglets. Vet Immunol Immunopathol. 2005;105(1–2):151–61. Epub 2005/03/31. doi: 10.1016/j.vetimm.2004.12.022 15797484.

61. Benyacoub J, Czarnecki-Maulden GL, Cavadini C, Sauthier T, Anderson RE, Schiffrin EJ, et al. Supplementation of food with Enterococcus faecium (SF68) stimulates immune functions in young dogs. J Nutr. 2003;133(4):1158–62. Epub 2003/04/04. doi: 10.1093/jn/133.4.1158 12672936.

62. Carina Audisio M, Oliver G, Apella MC. Protective effect of Enterococcus faecium J96, a potential probiotic strain, on chicks infected with Salmonella Pullorum. J Food Prot. 2000;63(10):1333–7. Epub 2000/10/21. doi: 10.4315/0362-028x-63.10.1333 11041131.

63. Cao GT, Zeng XF, Chen AG, Zhou L, Zhang L, Xiao YP, et al. Effects of a probiotic, Enterococcus faecium, on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with Escherichia coli K88. Poult Sci. 2013;92(11):2949–55. Epub 2013/10/19. doi: 10.3382/ps.2013-03366 24135599.

64. Million M, Maraninchi M, Henry M, Armougom F, Richet H, Carrieri P, et al. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obesity. 2012;36(6):817–25. doi: 10.1038/ijo.2011.153 WOS:000305282400009. 21829158

65. Sanchez M, Darimont C, Drapeau V, Emady-Azar S, Lepage M, Rezzonico E, et al. Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women. Br J Nutr. 2014;111(8):1507–19. Epub 2013/12/05. doi: 10.1017/S0007114513003875 24299712.

66. Stanley D, Hughes RJ, Geier MS, Moore RJ. Bacteria within the gastrointestinal tract microbiota correlated with improved growth and feed conversion: challenges presented for the identification of performance enhancing probiotic bacteria. Front Microbiol. 2016;7. doi: 10.3389/fmicb.2016.00187 WOS:000370563700001. 26925052

67. Fak F, Backhed F. Lactobacillus reuteri prevents diet-induced obesity, but not atherosclerosis, in a strain dependent fashion in Apoe-/- mice. PLoS One. 2012;7(10):e46837. doi: 10.1371/journal.pone.0046837 23056479; PubMed Central PMCID: PMC3467285.

68. Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr. 2009;139(9):1619–25. Epub 2009/07/25. doi: 10.3945/jn.109.104638 19625695; PubMed Central PMCID: PMC2728689.

69. Leeson S, Namkung H, Antongiovanni M, Lee EH. Effect of butyric acid on the performance and carcass yield of broiler chickens. Poult Sci. 2005;84(9):1418–22. Epub 2005/10/07. doi: 10.1093/ps/84.9.1418 16206563.

70. Beh BK, Mohamad NE, Yeap SK, Ky H, Boo SY, Chua JYH, et al. Anti-obesity and anti-inflammatory effects of synthetic acetic acid vinegar and Nipa vinegar on high-fat-diet-induced obese mice. Sci Rep. 2017;7(1):2045–322. Epub 2017/07/29. doi: 10.1038/s41598-017-01960-5 28751642; PubMed Central PMCID: PMC5532206.

71. Zhang WH, Jiang Y, Zhu QF, Gao F, Dai SF, Chen J, et al. Sodium butyrate maintains growth performance by regulating the immune response in broiler chickens. Br Poult Sci. 2011;52(3):292–301. Epub 2011/07/08. doi: 10.1080/00071668.2011.578121 21732874.

72. Ryssel H, Kloeters O, Germann G, Schafer T, Wiedemann G, Oehlbauer M. The antimicrobial effect of acetic acid—an alternative to common local antiseptics? Burns. 2009;35(5):695–700. Epub 2009/03/17. doi: 10.1016/j.burns.2008.11.009 19286325.

73. Andreatti RL, da Silva EN, Ribeiro AR, Kondo N, Curi PR. Use of anaerobic cecal microflora, lactose and acetic acid for the protection of broiler chicks against experimental infection with Salmonella typhimurium and Salmonella enteritidis. Braz J Microbiol. 2000;31(2):107–12.

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