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Antimicrobial Properties of 2D Mno2 and Mos2 Nanomaterials Vertically Aligned on Graphene Materials and Ti3c2 Mxene

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Antimicrobial Properties of 2D Mno2 and Mos2 Nanomaterials Vertically Aligned on Graphene Materials and Ti3c2 Mxene Subscriber access provided by Temple University Libraries Biological and Environmental Phenomena at the Interface Antimicrobial Properties of 2D MnO2 and MoS2 Nanomaterials Vertically Aligned on Graphene Materials and Ti3C2 MXene Farbod Alimohammadi, Mohammad Sharifian Gh., Nuwan H. Attanayake, Akila C. Thenuwara, Yury Gogotsi, Babak Anasori, and Daniel R. Strongin Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b00262 • Publication Date (Web): 21 May 2018 Downloaded from http://pubs.acs.org on May 29, 2018 Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts. is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties. Page 1 of 21 Langmuir 1 2 3 4 Antimicrobial Properties of 2D MnO2 and MoS2 Nanomaterials 5 Vertically Aligned on Graphene Materials and Ti3C2 MXene 6 7 Farbod Alimohammadi1,2, Mohammad Sharifian Gh.1, Nuwan H. Attanayake1,2, Akila C. Thenuwara1,2, 8 Yury Gogotsi3, Babak Anasori3, and Daniel R. Strongin1,2* 9 1 Department of Chemistry, Temple University, 1901 N. 13th Street, Philadelphia, Pennsylvania 19122, USA. 10 2 Center for Computational Design of Functional Layered Materials (CCDM), Temple University, 1925 North 12th Street, 11 Philadelphia, Pennsylvania 19122, United States 12 3 Department of Materials Science and Engineering, and A. J. Drexel Nanomaterials Institute, Drexel University, Philadelphia, 13 Pennsylvania 19104, USA 14 15 16 ABSTRACT 17 Two dimensional (2D) nanomaterials have attracted considerable attention in biomedical and environmental applications due to their antimicrobial activity. In the interest of investigating the primary 18 antimicrobial mode-of-action of 2D nanomaterials, we studied the antimicrobial properties of MnO and 19 MoS , toward Gram-positive and Gram-negative bacteria. Bacillus subtilis and Escherichia coli bacteria 20 2 were treated individually with 100 µg/mL of randomly oriented and vertically aligned nanomaterials for ∼3 21 2 h in the dark. The vertically aligned 2D MnO2 and MoS2 were grown on 2D sheets of graphene oxide, 22 reduced graphene oxide and Ti3C2 MXene. Measurements to determine the viability of bacteria in the 23 presence of the 2D nanomaterials performed by using two complementary techniques, flow cytometry 24 and fluorescence imaging showed that while MnO and MoS nanosheets show different antibacterial 25 activities, in both cases, Gram-positive bacteria show a higher loss in membrane integrity. Scanning 2 2 26 electron microscopy (SEM) images suggest that the 2D nanomaterials, which have a detrimental effect on 27 bacteria viability, compromise the cell wall, leading to significant morphological changes. We propose 28 that the peptidoglycan mesh (PM) in the bacterial wall is likely the primary target of the 2D nanomaterials. 29 Vertically aligned 2D MnO nanosheets showed the highest antimicrobial activity, suggesting that the 30 edges of the nanosheets were likely compromising the cell walls upon contact. 2 31 32 KEYWORDS 33 2D nanomaterials, antimicrobial, birnessite, mode-of-action, nano-knife, cell wall, peptidoglycan mesh 34 35 INTRODUCTION 36 37 According to the World Health Organization (WHO), antibiotic resistance has become one of the 38 biggest concerns to human health and food security, demanding a continuous development of new 39 40 classes of antimicrobial agents 1-4. In the interest of dealing with the antibiotic resistance, nanomaterials 41 with antibacterial properties (e.g., Ag nanoparticles) have been widely studied for various applications 42 5 6 7 8-9 43 such as water treatment , food packaging , medical devices , and in textile industries . Among the 44 various types of nanomaterials, ones with a two-dimensional (2D) motif and antimicrobial activity have 45 10-12 46 been recently introduced for biomedical and environmental applications . 47 Understanding the primary antimicrobial mode-of-action (MoA) of 2D nanomaterials is crucial in 48 designing new nanomaterials with higher antibacterial activity and lower toxicity toward human cells. 49 50 Among 2D nanomaterials, the graphite family (i.e., graphite, graphene oxide (GO), graphite oxide, and 51 reduced graphene oxide (rGO)) has been well studied for antibacterial applications 10, 13-15. Research has 52 53 shown that antibacterial properties of the graphite family are driven by both chemical and physical factors 54 10, 16-17. For instance, it has been reported that sharp edges of GO nanosheets (i.e., called ‘nano-knives’) 55 10- 56 damage bacterial membranes, which results in the release of cytoplasmic materials and bacteria death 57 58 1 59 60 ACS Paragon Plus Environment Langmuir Page 2 of 21 1 2 3 12, 16-17. It is proposed that smaller nanosheets might permeate into the microorganism through direct 4 10-12 5 physical penetration or via endocytosis . 6 A goal of the present study is to evaluate the role of ‘nano-knife’ characteristics of 2D 7 8 nanomaterials on their antibacterial properties. While there have been many studies on graphite family 9 nanosheets, there is a little understanding about the antibacterial properties of other common 2D 10 nanomaterials, such as MnO and MoS . Among transition metal chalcogenides 18-20, MoS has been 11 12 widely used for various applications2 that2 have included catalysis 21, energy storage22, drug delivery2 23-26, 13 and environmental chemistry 27. To the best of our knowledge, however, there are only a few studies on 14 15 antibacterial properties of those nanomaterials. Yang et. al. have shown that monolayer MoS with less 16 aggregation has higher antibacterial activity than bulk MoS which is due to their morphology differences,2 17 28 18 including shape and specific surface area . Research has2 reported that production of reactive oxygen 19 species (ROS) is increased in the presence of vertically aligned MoS on a glassy carbon substrate, which 20 29 21 results in higher antibacterial activity of the nanomaterial . Prior 2work has also shown that the basal 22 plane of GO- MoS nanocomposite has antibacterial properties30. MnO nanomaterial has found use in 23 the environmental2 arena as a material capable of destroying aqueous2 pollutants31-32 and showing 24 25 antibacterial activities 31, 33-36 as well. For example, it has been shown that MnO coated onto an 26 ultrafiltration membrane can be used in drinking water treatment. Moreover, antibacterial2 properties of - 27 34 28 MnO are enhanced when decorated onto carbon nanotubes . However, the antibacterial activity αof 29 layer2ed MnO (i.e., birnessite phase) has not been studied yet. 30 31 In the2 current study, we build on prior research and investigate antibacterial properties of MnO 32 toward both Gram-positive (i.e., Gram+) and Gram-negative (i.e., Gram ) bacteria. Our scientific2 33 34 hypothesis to be tested is that the sharp edges of 2D nanosheets play a− key role in damaging the 35 bacterial cell wall, which results in the loss of membrane integrity and bacteria death. To this end, we 36 MnO MoS 37 compare the antibacterial activity of randomly oriented (i.e., dispersed flower-like and ) versus 38 vertically aligned MnO and MoS nanomaterials grown individually on GO , rGO , 2and Ti3C22 MXene 39 MnO /GO2 MoS /rGO2 MoS /MXene 40 substrates (i.e., , , and ). The scientific logic used to test our hypothesis 41 is that if sharp edges2 of the 2D2 nanomaterials 2play a significant role in reducing the bacteria membrane 42 integrity, the antibacterial activity of the nanosheets vertically grown on 2D substrates should be greater 43 44 compared to the randomly oriented sheets of the respective nanomaterial. Escherichia (E.) coli and 45 Bacillus (B.) subtilis bacteria species were chosen as Gram and Gram+ model systems, respectively. To 46 47 reduce the effects of oxidative stress (i.e., mainly ROS−-dependent oxidative stress) in antibacterial 48 properties, we incubated bacteria with the nanomaterials in the dark. Flow cytometry (FC) and 49 50 fluorescence imaging (FI) techniques were used for bacteria viability measurements and scanning 51 electron microscopy (SEM) was used to evaluate interactions of 2D nanomaterials with the bacteria. 52 53 54 55 56 57 58 2 59 60 ACS Paragon Plus Environment Page 3 of 21 Langmuir 1 2 3 RESULTS AND DISCUSSION 4 5 6 Characterization of the 2D nanomaterials 7 GO 8 Atomic force microscopy (AFM) was used to characterize the thickness and lateral size of the 9 and MXene nanomaterials after deposition onto an atomically flat mica surface (see Figure S1 and S2). 10 Visual inspection of the micrographs shows that the GO monolayer has a thickness of ∼1 nm and a lateral 11 12 size varying between 0.3 and 10 µm.
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