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Antibacterial mechanism and activities of black pepper chloroform extract

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Abstract

Black pepper extracts reportedly inhibit food spoilage and food pathogenic bacteria. This study explored the antimicrobial activity of black pepper chloroform extract (BPCE) against Escherichia coli and Staphylococcus aureus. The antibacterial mechanism of BPCE was elucidated by analyzing the cell morphology, respiratory metabolism, pyruvic acid content, and ATP levels of the target bacteria. Scanning electron micrographs showed that the bacterial cells were destroyed and that plasmolysis was induced. BPCE inhibited the tricarboxylic acid pathway of the bacteria. The extract significantly increased pyruvic acid concentration in bacterial solutions and reduced ATP level in bacterial cells. BPCE destroyed the permeability of the cell membrane, which consequently caused metabolic dysfunction, inhibited energy synthesis, and triggered cell death.

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References

  • Butt MS, Pasha I, Sultan MT, Randhawa MA, Saeed F, Ahmed W (2012) Black pepper and health claims: a comprehensive treatise. Crit Rev Food Sci 53:875–886

    Article  Google Scholar 

  • Camper AK, Mcfeters GA (1979) Chlorine injury and the enumeration of waterborne coliform bacteria. Appl Environ Microb 37:633–641

    CAS  Google Scholar 

  • Carvajal-Arroyo JM, Puyol D, Li G, Sierra-Álvarez R, Field JA (2014) The intracellular proton gradient enables anaerobic ammonia oxidizing (anammox) bacteria to tolerate NO2- inhibition. J Biotechnol 192(Part A):265–267

    Article  CAS  Google Scholar 

  • Causey TB, Shanmugam KT, Yomano LP, Ingram LO (2004) Engineering escherichia coli for efficient conversion of glucose to pyruvate. Proc Natl Acad Sci U S A 101:2235–2240

    Article  CAS  Google Scholar 

  • Chaudhry NM, Tariq P (2006) Bactericidal activity of black pepper, bay leaf, aniseed and coriander against oral isolates. Pak J Pharm Sci 19:214–218

    Google Scholar 

  • Cox SD, Mann CM, Markham JL, Bell HC, Gustafson JE, Warmington JR, Wyllie SG (2000) The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). J Appl Microbiol 88:170–175

    Article  CAS  Google Scholar 

  • Cui Y, Zhao Y, Tian Y, Zhang W, Lü X, Jiang X (2012) The molecular mechanism of action of bactericidal gold nanoparticles on Escherichia coli. Biomaterials 33:2327–2333

    Article  CAS  Google Scholar 

  • Dong Z, Liu X, Zhao G, Zhen H (2010) Anti-bacterial mechanism of pomegranate peel on Staphylococcus aureus. 2010 First International Conference on CMBB 5:10–14

  • Dorman H, Deans SG (2000) Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol 88:308–316

    Article  CAS  Google Scholar 

  • Hao G, Shi Y, Tang Y, Le G (2009) The membrane action mechanism of analogs of the antimicrobial peptide Buforin 2. Peptides 30:1421–1427

    Article  CAS  Google Scholar 

  • He F, Yang Y, Yang G, Yu L (2010) Studies on antibacterial activity and antibacterial mechanism of a novel polysaccharide from streptomyces virginia H03. Food Control 21:1257–1262

    Article  CAS  Google Scholar 

  • Heng W, Ling Z, Na W, Youzhi G, Zhen W, Zhiyong S, Deping X, Yunfei X, Weirong Y (2014) Analysis of the bioactive components of Sapindus saponins. Ind Crop Prod 61:422–429

    Article  CAS  Google Scholar 

  • Jallali I, Zaouali Y, Missaoui I, Smeoui A, Abdelly C, Ksouri R (2014) Variability of antioxidant and antibacterial effects of essential oils and acetonic extracts of two edible halophytes: Crithmum maritimum L. and Inula crithmoїdes L. Food Chem 145:1031–1038

  • Kito M, Takimoto R, Onji Y, Yoshida T, Nagasawa T (2003) Purification and characterization of an ε-poly-l-lysine-degrading enzyme from the ε-poly-l-lysine-tolerant Chryseobacterium sp. OJ7. J Biosci Bioeng 96:92–94

    Article  CAS  Google Scholar 

  • Koshlukova SE, Lloyd TL, Araujo MW, Edgerton M (1999) Salivary histatin 5 induces Non-lytic release of ATP fromCandida albicans leading to cell death. J Biol Chem 274:18872–18879

    Article  CAS  Google Scholar 

  • Li X, Feng X, Yang S, Fu G, Wang T, Su Z (2010) Chitosan kills escherichia coli through damage to be of cell membrane mechanism. Carbohydr Polym 79:493–499

    Article  CAS  Google Scholar 

  • Lv F, Liang H, Yuan Q, Li C (2011) In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Res Int 44:3057–3064

    Article  CAS  Google Scholar 

  • Ma Y, Yang B, Guo T, Xie L (2010) Antibacterial mechanism of Cu2+ -ZnO /cetylpyridinium-montmorillonite in vitro. Appl Clay Sci 50:348–353

    Article  CAS  Google Scholar 

  • Mader JS, Richardson A, Salsman J, Top D, de Antueno R, Duncan R, Hoskin DW (2007) Bovine lactoferricin causes apoptosis in Jurkat T-leukemia cells by sequential permeabilization of the cell membrane and targeting of mitochondria. Exp Cell Res 313:2634–2650

    Article  CAS  Google Scholar 

  • Meghwal M, Goswami TK (2013) Piper nigrum and piperine: an update. Phytother Res 27:1121–1130

    Article  CAS  Google Scholar 

  • Nalini N, Sabitha K, Viswanathan P, Menon VP (1998) Spices and glycoprotein metabolism in experimental colon cancer rats. Med Sci Res 26:781–784

    CAS  Google Scholar 

  • Palmer GE, Kelly MN, Sturtevant JE (2007) Autophagy in the pathogen Candida albicans. Microbiology 153:51–58

    Article  CAS  Google Scholar 

  • Pan Y, Zhu Z, Huang Z, Wang H, Liang Y, Wang K, Lei Q, Liang M (2009) Characterisation and free radical scavenging activities of novel red pigment from Osmanthus fragrans’ seeds. Food Chem 112:909–913

    Article  CAS  Google Scholar 

  • Pang W, Zhang Y, Zhao N, Darwiche SS, Fu X, Xiang W (2013) Low expression of Mfn2 is associated with mitochondrial damage and apoptosis in the placental villi of early unexplained miscarriage. Placenta 34:613–618

    Article  CAS  Google Scholar 

  • Pradhan KJ, Variyar PS, Bandekar JR (1999) Antimicrobial activity of novel phenolic compounds from green pepper (Piper nigrum L.). LWT Food Sci Technol 32:121–123

    Article  CAS  Google Scholar 

  • Ravindran PN, Kallupurackal JA (2012) 6 - Black pepper. In Peter KV (ed) Handbook of herbs and spices, 2nd edn. Woodhead Publishing, pp.86–115

  • Rhayour K, Bouchikhi T, Tantaoui-Elaraki A, Sendide K, Remmal A (2003) The mechanism of bactericidal action of oregano and clove essential oils and of their phenolic major components on Escherichia coli and Bacillus subtilis. J Essent Oil Res 15:286–292

    Article  CAS  Google Scholar 

  • Salie F, Eagles PFK, Leng HMJ (1996) Preliminary antimicrobial screening of four South African Asteraceae species. J Ethnopharmacol 52:27–33

    Article  CAS  Google Scholar 

  • Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351

    Article  CAS  Google Scholar 

  • Sumathykutty MA, Rao JM (1988) Lignans from leaves of piper-nigrum linn. pp.388-389: Council Scientific Industrial Research Publ & Info Directorate, New Delhi 110012, India

  • Thiel A, Buskens C, Woehrle T, Etheve S, Schoenmakers A, Fehr M, Beilstein P (2014) Black pepper constituent piperine: Genotoxicity studies in vitro and in vivo. Food Chem Toxicol 66:350–357

    Article  CAS  Google Scholar 

  • Tomar A, Eiteman MA, Altman E (2003) The effect of acetate pathway mutations on the production of pyruvate in Escherichia coli. Appl Microbiol Biotechnol 62:76–82

    Article  CAS  Google Scholar 

  • Tong G, Yulong M, Peng G, Zirong X (2005) Antibacterial effects of the Cu(II)-exchanged montmorillonite on escherichia coli K88 and salmonella choleraesuis. Vet Microbiol 105:113–122

    Article  CAS  Google Scholar 

  • Wang D, Wang L, Hou L, Deng X, Gao Q, Gao N (2015) Metabolic engineering of saccharomyces cerevisiae for accumulating pyruvic acid. Ann Microbiol. doi:10.1007/s13213-015-1074-5

    Google Scholar 

  • Yao X, Zhu X, Pan S, Fang Y, Jiang F, Phillips GO, Xu X (2012) Antimicrobial activity of nobiletin and tangeretin against Pseudomonas. Food Chem 132:1883–1890

    Article  CAS  Google Scholar 

  • Yoon YC, Kim S, Kim MJ, Yang HJ, Rhyu M, Park J (2015) Piperine, a component of black pepper, decreases eugenol-induced cAMP and calcium levels in non-chemosensory 3T3-L1 cells. FEBS Open Bio 5:20–25

    Article  CAS  Google Scholar 

  • Zamaraeva MV, Sabirov RZ, Maeno E, Ando-Akatsuka Y, Bessonova SV, Okada Y (2005) Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase. Cell Death Differ 12:1390–1397

    Article  CAS  Google Scholar 

  • Zhong L, Lv M, Zhang H, Chen H (2001) Antimicrobial mechanism of protamine. J Fish China 25:171–175

    CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Natural Science Foundation of Hainan Province, China (312073); Dr Foundation of Hainan University (kyqd1224).

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Correspondence to Wen-Xue Chen.

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Zou, L., Hu, YY. & Chen, WX. Antibacterial mechanism and activities of black pepper chloroform extract. J Food Sci Technol 52, 8196–8203 (2015). https://doi.org/10.1007/s13197-015-1914-0

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  • DOI: https://doi.org/10.1007/s13197-015-1914-0

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