Host-mediated biofilm forming promotes post-graphene pathogen expansion via graphene micron-sheet

Abstract

Graphene is a potential candidate for applications in biomedical field. It is inevitable that graphene is in contact with the ubiquitous bacterial environment. More attention has been paid to the antimicrobial activity of graphene derivatives (graphene oxide, reduced graphene oxide) than the interaction between graphene and bacteria. Herein, we explore interaction between graphene micron-sheet and bacteria from micro (gene expression) and macro (colonies) perspectives. Results demonstrate that graphene micron-sheet accelerates the biofilm forming thus promoting pathogen expansion toward both Gram-negative bacteria E. coli and Gram-positive bacteria S. aureus. The graphene micron-sheet acts as a “habitat” for increasing bacterial attachment and biofilm forming. For E. coli, graphene micron-sheet, firstly changes the integrity of periplasmic and outer membrane components, then makes membrane-associated and cell division genes increased, and finally promotes bacterial proliferation; For S. aureus, graphene micron-sheet can accelerate biofilm forming and develop bacterial expansion owing to the regulation of the quorum-sensing system and global regulatory proteins. The work can shed new light on the range of possible mode of actions, developing a better understanding of the capabilities of graphene micron-structures.

Keywords

graphene micron-sheet / bacteria / gene expression / biofilm forming

References

[1] Zhu Y, Murali S, Cai W, . Graphene and graphene oxide: synthesis, properties, and applications. Advanced Materials, 2010, 22(35): 3906–3924

[2] James D K, Tour J M. Graphene: powder, flakes, ribbons, and sheets. Accounts of Chemical Research, 2013, 46(10): 2307–2318

[3] Jia Z, Shi Y, Xiong P, . From solution to biointerface: graphene self-assemblies of varying lateral sizes and surface properties for biofilm control and osteodifferentiation. ACS Applied Materials & Interfaces, 2016, 8(27): 17151–17165

[4] Shim G, Kim M G, Park J Y, . Graphene-based nanosheets for delivery of chemotherapeutics and biological drugs. Advanced Drug Delivery Reviews, 2016, 105(Pt B): 205–227

[5] Chung C, Kim Y K, Shin D, . Biomedical applications of graphene and graphene oxide. Accounts of Chemical Research, 2013, 46(10): 2211–2224

[6] Zou X, Zhang L, Wang Z, . Mechanisms of the antimicrobial activities of graphene materials. Journal of the American Chemical Society, 2016, 138(7): 2064–2077

[7] Kang S, Pinault M, Pfefferle L D, . Single-walled carbon nanotubes exhibit strong antimicrobial activity. Langmuir, 2007, 23(17): 8670–8673

[8] Akhavan O, Ghaderi E. Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano, 2010, 4(10): 5731–5736

[9] Nel A, Xia T, Mädler L, . Toxic potential of materials at the nanolevel. Science, 2006, 311(5761): 622–627

[10] Hui L, Piao J G, Auletta J, . Availability of the basal planes of graphene oxide determines whether it is antibacterial. ACS Applied Materials & Interfaces, 2014, 6(15): 13183–13190

[11] Tu Y, Lv M, Xiu P, . Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nature Nanotechnology, 2013, 8(8): 594–601

[12] Pham V T H, Truong V K, Quinn M D J, . Graphene induces formation of pores that kill spherical and rod-shaped bacteria. ACS Nano, 2015, 9(8): 8458–8467

[13] Akhavan O, Ghaderi E, Esfandiar A. Wrapping bacteria by graphene nanosheets for isolation from environment, reactivation by sonication, and inactivation by near-infrared irradiation. The Journal of Physical Chemistry B, 2011, 115(19): 6279–6288

[14] Li J, Wang G, Zhu H, . Antibacterial activity of large-area monolayer graphene film manipulated by charge transfer. Scientific Reports, 2014, 4(1): 4359

[15] Liu S, Hu M, Zeng T H, . Lateral dimension-dependent antibacterial activity of graphene oxide sheets. Langmuir, 2012, 28(33): 12364–12372

[16] Zhang K, Liu X. One step synthesis and characterization of CdS nanorod/graphene nanosheet composite. Applied Surface Science, 2011, 257(24): 10379–10383

[17] Gurunathan S, Han J W, Dayem A A, . Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. International Journal of Nanomedicine, 2012, 7: 5901–5914

[18] Krishnamoorthy K, Veerapandian M, Zhang L H, . Antibacterial efficiency of graphene nanosheets against pathogenic bacteria via lipid peroxidation. The Journal of Physical Chemistry C, 2012, 116(32): 17280–17287

[19] Salas E C, Sun Z, Lüttge A, . Reduction of graphene oxide via bacterial respiration. ACS Nano, 2010, 4(8): 4852–4856

[20] Zhang N, Hou J, Chen S M, . Rapidly probing antibacterial activity of graphene oxide by mass spectrometry-based metabolite fingerprinting. Scientific Reports, 2016, 6(1): 28045

[21] Dallavalle M, Calvaresi M, Bottoni A, . Graphene can wreak havoc with cell membranes. ACS Applied Materials & Interfaces, 2015, 7(7): 4406–4414

[22] Huc V, Bendiab N, Rosman N, . Large and flat graphene flakes produced by epoxy bonding and reverse exfoliation of highly oriented pyrolytic graphite. Nanotechnology, 2008, 19(45): 455601

[23] Geim A K, Novoselov K S. The rise of graphene. Nature Materials, 2007, 6(3): 183–191

[24] Lück A, Klimmasch L, Großmann P, . Computational investigation of environment-noise interaction in single-cell organisms: the merit of expression stochasticity depends on the quality of environmental fluctuations. Scientific Reports, 2018, 8(1): 333

[25] Hengge R. The general stress response in Gram-negative bacteria. In: Hengge R, Storz G, eds. Bacterial Stress Responses. 2nd ed. Washington DC: American Society for Microbiology, 2011, 251–289

[26] Rolhion N, Carvalho F A, Darfeuille-Michaud A. OmpC and the σ^E regulatory pathway are involved in adhesion and invasion of the Crohn’s disease-associated Escherichia coli strain LF82. Molecular Microbiology, 2007, 63(6): 1684–1700

[27] Little J W, Mount D W. The SOS regulatory system of Escherichia coli. Cell, 1982, 29(1): 11–22

[28] Walker G C. The SOS response of Escherichia coli. In: Neidhardt F C, Ingraham J L, Low K B, et al., eds. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd ed. Washington DC: American Society for Microbiology, 1996, 1579–1601

[29] Ruiz C, Levy S B. Regulation of acrAB expression by cellular metabolites in Escherichia coli. The Journal of Antimicrobial Chemotherapy, 2014, 69(2): 390–399

[30] Hächler H, Cohen S P, Levy S B. marA, a regulated locus which controls expression of chromosomal multiple antibiotic resistance in Escherichia coli. Journal of Bacteriology, 1991, 173(17): 5532–5538

[31] Martin R G, Bartlett E S, Rosner J L, . Activation of the Escherichia coli marA/soxS/rob regulon in response to transcriptional activator concentration. Journal of Molecular Biology, 2008, 380(2): 278–284

[32] Wang P, Yu Z, Li B, . Development of an efficient conjugation-based genetic manipulation system for Pseudoalteromonas. Microbial Cell Factories, 2015, 14(1): 11

[33] Zhang X S, García-Contreras R, Wood T K. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. Journal of Bacteriology, 2007, 189(8): 3051–3062

[34] Wang S, Deng K, Zaremba S, . Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Applied and Environmental Microbiology, 2009, 75(19): 6110–6123

[35] May T, Ito A, Okabe S. Induction of multidrug resistance mechanism in Escherichia coli biofilms by interplay between tetracycline and ampicillin resistance genes. Antimicrobial Agents and Chemotherapy, 2009, 53(11): 4628–4639

[36] Peano C, Wolf J, Demol J, . Characterization of the Escherichia coliσ^S core regulon by Chromatin Immunoprecipitation-sequencing (ChIP-seq) analysis. Scientific Reports, 2015, 5(1): 10469

[37] Jensen S O, Thompson L S, Harry E J. Cell division in Bacillus subtilis: FtsZ and FtsA association is Z-ring independent, and FtsA is required for efficient midcell Z-ring assembly. Journal of Bacteriology, 2005, 187(18): 6536–6544

[38] Srivastava S K, Rajasree K, Fasim A, . Influence of the AgrC-AgrA complex on the response time of Staphylococcus aureus quorum sensing. Journal of Bacteriology, 2014, 196(15): 2876–2888

[39] Vuong C, Saenz H L, Götz F, . Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. The Journal of Infectious Diseases, 2000, 182(6): 1688–1693

[40] Xiong Y Q, Willard J, Yeaman M R, . Regulation of Staphylococcus aureus α-toxin gene (hla) expression by agr, sarA, and sae in vitro and in experimental infective endocarditis. The Journal of Infectious Diseases, 2006, 194(9): 1267–1275

[41] Boles B R, Horswill A R. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathogens, 2008, 4(4): e1000052

[42] Yarwood J M, Schlievert P M. Quorum sensing in Staphylococcus infections. The Journal of Clinical Investigation, 2003, 112(11): 1620–1625

[43] Pavithra D, Doble M. Biofilm formation, bacterial adhesion and host response on polymeric implants — issues and prevention. Biomedical Materials, 2008, 3(3): 034003

[44] Salehzadeh A, Zamani H, Langeroudi M K, . Molecular typing of nosocomial Staphylococcus aureus strains associated to biofilm based on the coagulase and protein A gene polymor-phisms. Iranian Journal of Basic Medical Sciences, 2016, 19(12): 1325–1330

[45] Hookey J V, Richardson J F, Cookson B D. Molecular typing of Staphylococcus aureus based on PCR restriction fragment length polymorphism and DNA sequence analysis of the coagulase gene. Journal of Clinical Microbiology, 1998, 36(4): 1083–1089

[46] Valle J, Toledo-Arana A, Berasain C, . SarA and not σ^B is essential for biofilm development by Staphylococcus aureus. Molecular Microbiology, 2003, 48(4): 1075–1087

[47] Abdelhady W, Bayer A S, Seidl K, . Impact of vancomycin on sarA-mediated biofilm formation: role in persistent endovascular infections due to methicillin-resistant Staphylococcus aureus. The Journal of Infectious Diseases, 2014, 209(8): 1231–1240

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