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Transcriptomic analysis of multi-drug resistant Escherichia coli K-12 strain in response to Lavandula angustifolia essential oil

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Abstract

To better understand the synergistic antibacterial activity between piperacillin and Lavandula angustifolia essential oil (LEO) against multidrug-resistant Escherichia coli, we performed microarray transcriptomic analysis of LEO when used alone and in combination with piperacillin against the non-treated control. In total, 90 genes were differentially expressed after the combination of LEO and piperacillin treatment. Among the up-regulated genes, nfsB, nemA, fruA, nfsB, nemA are known to control microbial metabolism and nitrotoluene degradation, which were observed only in the LEO–piperacillin combinatory treatment. Four candidate genes from the microarray result, srIA, srID, waaR and nfsB, were validated by qRT-PCR as these genes showed differential expression consistently in the two methods. Biochemical pathway analysis showed that there was upregulation of genes involved in several biological processes including fructose and mannose metabolism, phosphotransferase system (PTS), lipopolysaccharide biosynthesis and nitrotoluene degradation. Genes involved in microbial metabolism in diverse environments were found both up- and down-regulated in LEO–piperacillin combinatory treatment. Our study provides new information concerning the transcriptional changes that occur during the LEO and piperacillin interaction against the multidrug-resistant bacteria and contributes to unravel the mechanisms underlying this synergism.

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References

  • Catalogue of life. https://www.gbif.org/dataset/7ddf754f-d193-4cc9-b351-99906754a03b. Cited 27 Feb 2018

  • Dapkevicius A, Venskutonis R, Van Beek TA, Linssen JPH (1998) Antioxidant activity of extracts obtained by different isolation procedures from some aromatic herbs grown in Lithuania. J Sci Food Agric 77:140–146

    Article  CAS  Google Scholar 

  • Dauria FD, Tecca M, Strippoli V, Salvatore G, Battinelli L, Mazzanti G (2005) Antifungal activity of Lavandula angustifolia essential oil against Candida albicans yeast and mycelial form. Med Mycol 43:391–396

    Article  CAS  Google Scholar 

  • De Rapper S, Viljoen A, Van Vuuren S (2016) The in vitro antimicrobial effects of Lavandula angustifolia essential oil in combination with conventional antimicrobial agents. Evid Based Complement Altern Med 2016:1–9

    Article  Google Scholar 

  • Elshafie HS, Mancini E, Sakr S, De Martino L, Mattia CA, De Feo V, Camele I (2015) Antifungal activity of some constituents of Origanum vulgare L. essential oil against postharvest disease of peach fruit. J Med Food 18:929–934

    Article  CAS  Google Scholar 

  • Evandri MG, Battinelli L, Daniele C, Mastrangelo S, Bolle P, Mazzanti G (2005) The antimutagenic activity of Lavandula angustifolia (lavender) essential oil in the bacterial reverse mutation assay. Food Chem Toxicol 43:1381–1387

    Article  CAS  Google Scholar 

  • Eveleigh T (1994) Lavender. Lorenz Books, Sydney

    Google Scholar 

  • Fabio A, Cermelli C, Fabio G, Nicoletti P, Quaglio P (2007) Screening of the antibacterial effects of a variety of essential oils on microorganisms responsible for respiratory infections. Phytother Res 21:374–377

    Article  CAS  Google Scholar 

  • Hajhashemi V, Ghannadi A, Sharif B (2003) Anti-inflammatory and analgesic properties of the leaf extracts and essential oil of Lavandula angustifolia Mill. J Ethnopharmacol 89:67–71

    Article  Google Scholar 

  • Hanamanthagouda MA, Kakkalameli SB, Naik PM, Nafella P, Seetharamareddy HR, Murthy HN (2010) Essential oils of Lavandula bipinnata and their antimicrobial activities. Food Chem 118:836–839

    Article  CAS  Google Scholar 

  • Holmes B, Richards DM, Brogden RN, Heel RC (1984) Piperacillin. A review of its antibacterial activity, pharmacokinetic properties and therapeutic use. Drugs 28(5):375–425

    Article  CAS  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57

    Article  CAS  Google Scholar 

  • Jianu C, Pop G, Gruia AT, Horhat FG (2013) Chemical composition and antimicrobial activity of essential oils of lavender (Lavandula angustifolia) and lavandin (Lavandula × intermedia) grown in Western Romania. Int J Agric Biol 15:772–776

    CAS  Google Scholar 

  • Mahizan NA, Yang SK, Moo CL, Song AAL, Chong CM, Chong CW, Abushelaibi A, Lim SHE, Lai KS (2019) Terpene derivatives as a potential agent against antimicrobial resistance (AMR) pathogens. Molecules 24:2631

    Article  CAS  Google Scholar 

  • Mancini E, Camele I, Elshafie HS, De Martino L, Pellegrino C, Grulova D, De Feo V (2014) Chemical composition and biological activity of the essential oil of Origanum vulgare ssp. hirtum from different areas in the Southern Apennines (Italy). Chem Biodivers 11:639–651

    Article  CAS  Google Scholar 

  • Moo CL, Yang SK, Yusoff K, Ajat M, Thomas W, Abushelaibi A, Lim SHE, Lai KS (2019) Mechanisms of antimicrobial resistance (AMR) and alternative approaches to overcome AMR. Curr Drug Discov Technol. https://doi.org/10.2174/1570163816666190304122219

    Article  PubMed  Google Scholar 

  • Nelson RRS (1997) In-vitro activities of five plant essential oils against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus faecium. J Antimicrob Chemother 40(2):305–306

    Article  CAS  Google Scholar 

  • Odds FC (2003) Synergy, antagonism, and what the checquerboard puts between then. J Antimicrob Chemother 52(1):1

    Article  CAS  Google Scholar 

  • Prusinowska R, Śmigielski KB (2014) Composition, biological properties and therapeutic effects of lavender (Lavandula angustifolia L.). A review. Herba Polonica. https://doi.org/10.2478/hepo-2014-0010

    Article  Google Scholar 

  • Shah PJ, Ryzner L (2013) Evaluating the appropriate use of piperacillin/tazobactam in a community health system: a retrospective chart review. P T 38(8):462–483

    PubMed  PubMed Central  Google Scholar 

  • Soković M, Glamočlija J, Marin PD, Brkic D, van Griensven LJ (2010) Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model. Molecules 15(11):7532–7546

    Article  Google Scholar 

  • Walsh C (2000) Molecular mechanisms that confer antibacterial drug resistance. Nature 406:775–781

    Article  CAS  Google Scholar 

  • Wolska KI, Grześ K, Kurek A (2012) A Synergy between novel antimicrobials and conventional antibiotics or bacteriocins. Pol J Microbiol 61(2):95–104

    Article  CAS  Google Scholar 

  • World Health Organization (2014) Antimicrobial resistance. Glob Rep Surveill 61(3):12–28. https://doi.org/10.1007/s13312-014-0374-3

    Article  Google Scholar 

  • Yang SK, Low LY, Yap PSX, Yusoff K, Mai CW, Lai KS, Lim SH (2018) Plant-derived antimicrobials: insights into mitigation of antimicrobial resistance. Rec Nat Prod 12:295–316. https://doi.org/10.25135/rnp.41.17.09.058

    Article  CAS  Google Scholar 

  • Yang SK, Yusoff K, Ajat M, Thomas W, Abushelaibi A, Akseer R, Lim SHE, Lai KS (2019) Disruption of KPC-producing Klebsiella pneumoniae membrane via induction of oxidative stress by cinnamon bark (Cinnamomum verum J. Presl) essential oil. PLoS ONE 14:e0214326. https://doi.org/10.1371/journal.pone.0214326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SK, Yusoff K, Thomas W, Akseer R, Sultan Alhosani M, Abushelaibi A, Lim SHE, Lai KS (2020) Lavender essential oil induces oxidative stress which modifies the bacterial membrane permeability of carbapenemase producing Klebsiella pneumoniae. Sci Rep 10:1–14

    Article  Google Scholar 

  • Yap PSX, Krishnan T, Yiap BC, Hu CP, Chan KG, Lim SH (2014) Membrane disruption and anti-quorum sensing effects of synergistic interaction between Lavandula angustifolia (lavender oil) in combination with antibiotic against plasmid-conferred multi-drug-resistant Escherichia coli. J Appl Microbiol 116(5):1119–1128

    Article  CAS  Google Scholar 

  • Yap PSX, Lim SHE, Hu CP, Yiap BC (2013) Combination of essential oils and antibiotics reduce antibiotic resistance in plasmid-conferred multidrug resistant bacteria. Phytomedicine 20(8–9):710–713

    Article  CAS  Google Scholar 

  • Zhang G, Meredith TC, Kahne D (2013) On the essentiality of lipopolysaccharide to Gram-negative bacteria. Curr Opin Microbiol 16:779–785

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the Higher Colleges of Technology Interdisciplinary Research Grant (113118). We gratefully acknowledge Dr. George A. Jacoby for his kind gift of bacterial strains in this study. We also thank Ms. Nur Atiqah Azhar for her technical assistance and constructive suggestions on the bioinformatics analysis.

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Authors and Affiliations

  1. Department of Cell and Molecular Biology, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia

    Pey-Jiun Lai, Ee-Von Ng, Shun-Kai Yang & Chew-Li Moo

  2. School of Pharmacy, International Medical University, Bukit Jalil, 57000, Kuala Lumpur, Malaysia

    Ee-Von Ng

  3. Centre for Bioinformatics, School of Data Sciences, Perdana University, MAEPS Buildings, 43400, Serdang, Selangor, Malaysia

    Wai Yee Low

  4. The Davies Research Centre, School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy, SA, 5371, Australia

    Wai Yee Low

  5. Department of Medical Microbiology, Faculty of Medicine, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Polly Soo-Xi Yap

  6. Health Sciences Division, Abu Dhabi Women’s College, Higher Colleges of Technology, 41012, Abu Dhabi, United Arab Emirates

    Swee-Hua Erin Lim & Kok-Song Lai

Authors
  1. Pey-Jiun Lai
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  2. Ee-Von Ng
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  3. Shun-Kai Yang
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  4. Chew-Li Moo
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  5. Wai Yee Low
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  6. Polly Soo-Xi Yap
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  7. Swee-Hua Erin Lim
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  8. Kok-Song Lai
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Contributions

E-VN drafted the manuscript, P-JL, S-KY, C-LM, WYL, PS-XY, S-HEL and K-SL edited the draft. All authors read and approved the final manuscript.

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Correspondence to Swee-Hua Erin Lim or Kok-Song Lai.

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Lai, PJ., Ng, EV., Yang, SK. et al. Transcriptomic analysis of multi-drug resistant Escherichia coli K-12 strain in response to Lavandula angustifolia essential oil. 3 Biotech 10, 313 (2020). https://doi.org/10.1007/s13205-020-02304-3

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