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The Antimicrobial Activity and Cellular Pathways Targeted by P-Anisaldehyde and Epigallocatechin Gallate in the Opportunistic Human Pathogen Pseudomonas Aeruginosa

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The Antimicrobial Activity and Cellular Pathways Targeted by P-Anisaldehyde and Epigallocatechin Gallate in the Opportunistic Human Pathogen Pseudomonas Aeruginosa The University of Southern Mississippi The Aquila Digital Community Faculty Publications 12-6-2019 The Antimicrobial Activity and Cellular Pathways Targeted By p-anisaldehyde and Epigallocatechin Gallate in the Opportunistic Human Pathogen Pseudomonas aeruginosa Yetunde Adewumni University of Southern Mississippi Sanchirmaa Namjilsuren University of Southern Mississippi William D. Walker University of Southern Mississippi Dahlia N. Amato University of Southern Mississippi Douglas V. Amato University of Southern Mississippi FSeeollow next this page and for additional additional works authors at: https:/ /aquila.usm.edu/fac_pubs Part of the Microbiology Commons Recommended Citation Adewumni, Y., Namjilsuren, S., Walker, W. D., Amato, D. N., Amato, D. V., Mavrodi, O. V., Patton, D. L., Mavrodi, D. V. (2019). The Antimicrobial Activity and Cellular Pathways Targeted By p-anisaldehyde and Epigallocatechin Gallate in the Opportunistic Human Pathogen Pseudomonas aeruginosa. Applied and Environmental Microbiology. Available at: https://aquila.usm.edu/fac_pubs/16858 This Article is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Faculty Publications by an authorized administrator of The Aquila Digital Community. For more information, please contact [email protected]. Authors Yetunde Adewumni, Sanchirmaa Namjilsuren, William D. Walker, Dahlia N. Amato, Douglas V. Amato, Olga V. Mavrodi, Derek L. Patton, and Dmitri V. Mavrodi This article is available at The Aquila Digital Community: https://aquila.usm.edu/fac_pubs/16858 1 2 The antimicrobial activity and cellular pathways targeted by p-anisaldehyde and 3 epigallocatechin gallate in the opportunistic human pathogen Pseudomonas aeruginosa. 4 5 Yetunde Adewunmi1, Sanchirmaa Namjilsuren1, William D. Walker2, Dahlia N. Amato2, Douglas 6 V. Amato2, Olga V. Mavrodi1,3, Derek L. Patton2*, and Dmitri V. Mavrodi1* 7 8 1 School oF Biological, Environmental, and Earth Sciences, The University oF Southern 9 Mississippi, Hattiesburg, MS, United States 10 2 School oF Polymer Science and Engineering, The University oF Southern Mississippi, 11 Hattiesburg, MS, United States 12 3 South MS Branch Experiment Station, Mississippi State University, Poplarville, MS, United 13 States 14 15 16 Keywords: Pseudomonas aeruginosa, p-anisaldehyde, epigallocatechin gallate, antimicrobial 17 activity, cellular targets 18 19 20 21 22 *Corresponding Authors: D. V. Mavrodi, E-mail: [email protected]; D. L. Patton, E-mail: 23 [email protected]. 24 1 25 ABSTRACT 26 Plant-derived aldehydes are constituents of essential oils that possess broad-spectrum 27 antimicrobial activity and kill microorganisms without promoting resistance. In our previous 28 study, we incorporated p-anisaldehyde from star anise into a polymer network called PANDAs 29 (Pro-Antimicrobial Networks via Degradable Acetals) and used it as a novel drug delivery 30 platForm. PANDAs released p-anisaldehyde upon a change in pH and humidity, and controlled 31 growth of the multi-drug resistant pathogen Pseudomonas aeruginosa PAO1. In this study, we 32 identified cellular pathways targeted by p-anisaldehyde, by generating 10,000 transposon 33 mutants oF PAO1 and screened them For hypersensitivity to p-anisaldehyde. To improve the 34 antimicrobial efFicacy of p-anisaldehyde, we combined it with epigallocatechin gallate (EGCG), a 35 polyphenol From green tea, and demonstrated that it acts synergistically with p-anisaldehyde in 36 killing P. aeruginosa. We then used RNA-seq to profile transcriptomic responses of P. 37 aeruginosa to p-anisaldehyde, EGCG, and their combination. The exposure to p-anisaldehyde 38 altered the expression of genes involved in the modiFication of cell envelope, membrane 39 transport, drug efflux, energy metabolism, molybdenum cofactor biosynthesis, and stress 40 response. We also demonstrated that the addition of EGCG reversed many p-anisaldehyde- 41 coping efFects and induced oxidative stress. Our results provide an insight into the antimicrobial 42 activity of p-anisaldehyde and its interactions with EGCG and may aid in the rational 43 identification oF new synergistically-acting combinations of plant metabolites. Our study also 44 confirms the utility of the thiol-ene polymer platForm For the sustained and efFective delivery of 45 hydrophobic and volatile antimicrobial compounds. 46 47 IMPORTANCE 48 Essential oils (EOs) are plant-derived products that have been long exploited For their 49 antimicrobial activities in medicine, agriculture, and Food preservation. EOs represent a 50 promising alternative to conventional antibiotics due to the broad-range antimicrobial activity, 2 51 low toxicity to human commensal bacteria, and the capacity to kill microorganisms without 52 promoting resistance. Despite the progress in the understanding of the biological activity of 53 EOs, many aspects oF their mode oF action remain inconclusive. The overarching aim oF this 54 work was to address these gaps by studying molecular interactions between an antimicrobial 55 plant aldehyde and the opportunistic human pathogen Pseudomonas aeruginosa. Results of 56 this study identified microbial genes and associated pathways involved in response to 57 antimicrobial phytoaldehydes and provided insights into molecular mechanisms governing the 58 synergistic efFects of individual constituents within essential oils. 59 3 60 INTRODUCTION 61 Pseudomonas aeruginosa is a ubiquitous Gram-negative bacterium that serves as an 62 important model For opportunistic inFections and bioFilm research (1, 2). This organism is 63 commonly Found in soil, water, and plants, but can readily infect immunocompromised 64 individuals causing septicemia and wound or urinary tract inFections (3). It also responsible for 65 pneumonia and causes increased morbidity and mortality in cystic Fibrosis patients. 66 Pseudomonas aeruginosa is resistant to multiple classes oF antibiotics and belongs to a class oF 67 pathogens with increased virulence, persistence and transmissibility known as the ESKAPE 68 group (also encompasses Enterococcus faecium, Staphylococcus aureus, Klebsiella 69 pneumoniae, Acinetobacter baumannii, and Enterobacter species) (4). The Centers for Disease 70 Control and Prevention (CDC) reports that, in the U.S. alone, P. aeruginosa is associated with 71 8% of all healthcare-acquired infections and over 400 deaths per year, which are often caused 72 by multi-drug resistant (MDR) strains (5). These MDR variants are insensitive to nearly all the 73 available β-lactams and aminoglycosides and are classified by the CDC as a serious threat that 74 requires close monitoring and prevention activities (6). Therefore, there is a need for the 75 development of antimicrobial agents, which do not promote antibiotic resistance and may help 76 to mitigate the spread of MDR phenotypes in P. aeruginosa and other bacterial pathogens. 77 Plant essential oils (EOs) represent a rich source of alcohols, aldehydes, terpenes, 78 ethers, ketones, and phenolic compounds with antimicrobial, antiFungal, and antiparasitic activity 79 (7). The antiseptic properties and low toxicity of EOs prompted their use in traditional Food 80 preservation and homeopathic medicine (8). However, despite the demonstrated biological 81 activity, the wider acceptance of EOs and their constituents as antimicrobial agents is limited by 82 the hydrophobicity, chemical instability, high concentrations needed to achieve sufFicient 83 antimicrobial efFect, and undefined mode oF action. In our previous work, we addressed some of 84 these issues by incorporating the antimicrobial EO constituent p-anisaldehyde into a polymer 85 network called Pro-Antimicrobial Networks via Degradable Acetals (PANDAs) (9, 10). The 4 86 resultant polymer material was designed to act as a pro-drug that releases p-anisaldehyde upon 87 a change in pH and humidity. The incorporation into PANDAs increased the bioavailability and 88 antimicrobial efFicacy of p-anisaldehyde and related phytoaldehydes against P. aeruginosa, 89 Escherichia coli, Burkholderia cenocepacia, S. aureus, and Candida albicans. We also 90 demonstrated that the inactivation of the MexAB-OprM multidrug eFFlux pump sensitizes P. 91 aeruginosa to the action of p-anisaldehyde (10). 92 MexAB-OprM is a member oF the resistance-nodulation-cell-division (RND) superFamily 93 of multidrug efFlux pumps, which are recognized as essential contributors to the emergence of 94 MDR phenotypes in pathogenic bacteria. These membrane transporters extrude a broad 95 spectrum of antimicrobial compounds (11), intercellular signals, and virulence factors (12, 13), 96 which makes them an attractive target For the development oF anti-resistance drugs. Such drugs, 97 known as efFlux pump inhibitors (EPIs), interFere with the Function, expression, or assembly of 98 efFlux pumps, and can signiFicantly reduce or completely reverse resistance against otherwise 99 ineFFective antibiotics (14). Despite the development of a number of effective synthetic and semi- 100 synthetic EPIs, none of these compounds are currently used in the treatment of bacterial 101 inFections because oF the instability, low selectivity, and cytotoxic side eFFects (15). Plants, like 102 animals, are attacked by bacterial pathogens and have evolved defense mechanisms to 103 counteract such infections. This Fact has prompted numerous plant-based studies aimed at the 104 isolation oF natural EPIs with lower toxicity and better tolerability. These efForts produced
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