Copper Oxide Nanoparticles Induce Lysogenic Bacteriophage and Metal-Resistance Genes in Pseudomonas aeruginosa PAO1

ACS Applied Materials and Interfaces

Volumn 9, Issue 27, 2017, Pages 22298-22307

  Guo, Jianhua ^a   Gao, Shu Hong ^a   Lu, Ji ^a   Bond, Philip L ^a   Verstraete, Willy ^b   Yuan, Zhiguo ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

bacteriophage; denitrification; emerging contaminations; genome wide RNA sequencing; nanoparticles

Indexed keywords

BACTERIA; BACTERIOPHAGES; COPPER; COPPER OXIDES; DENITRIFICATION; ECOLOGY; ECOSYSTEMS; GENE EXPRESSION; GENES; HEALTH RISKS; MICROORGANISMS; NANOPARTICLES; NITRATION; PHYSIOLOGICAL MODELS; PUBLIC RISKS; RNA; TRANSCRIPTION;

CATION DIFFUSION FACILITATORS; COPPER OXIDE NANOPARTICLES; MICROBIAL ECO SYSTEM; MOLECULAR MECHANISM; NITRITE ACCUMULATION; PSEUDOMONAS AERUGINOSA; RNA SEQUENCING; TRANSCRIPTIONAL LEVELS;

METAL NANOPARTICLES;

COPPER; CUPRIC OXIDE; METAL NANOPARTICLE;

BACTERIOPHAGE; PSEUDOMONAS AERUGINOSA;

BACTERIOPHAGES; COPPER; METAL NANOPARTICLES; PSEUDOMONAS AERUGINOSA;

EID: 85024130262     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.7b06433     Document Type: Article

References (51)

1. Siripattanakul-Ratpukdi, S.; Fürhacker, M. Review: Issues of Silver Nanoparticles in Engineered Environmental Treatment Systems Water, Air, Soil Pollut. 2014, 225 (4) 1939 10.1007/s11270-014-1939-4
2. Bondarenko, O.; Juganson, K.; Ivask, A.; Kasemets, K.; Mortimer, M.; Kahru, A. Toxicity of Ag, Cuo and Zno Nanoparticles to Selected Environmentally Relevant Test Organisms and Mammalian Cells in Vitro: A Critical Review Arch. Toxicol. 2013, 87 (7) 1181-1200 10.1007/s00204-013-1079-4
3. Future Markets, Inc. The Global Market for Copper Oxide Nanoparticles, 2010-2025, 2015. http://www.futuremarketsinc.com/global-market-copper-oxide-nanoparticles-2010-2025.
4. Keller, A. A.; McFerran, S.; Lazareva, A.; Suh, S. Global Life Cycle Releases of Engineered Nanomaterials J. Nanopart. Res. 2013, 15 (6) 1692 10.1007/s11051-013-1692-4
5. Lin, S. J.; Zhao, Y.; Xia, T.; Meng, H.; Ji, Z. X.; Liu, R.; George, S.; Xiong, S. J.; Wang, X.; Zhang, H. Y.; Pokhrel, S.; Madler, L.; Damoiseaux, R.; Lin, S.; Nel, A. E. High Content Screening in Zebrafish Speeds up Hazard Ranking of Transition Metal Oxide Nanoparticles ACS Nano 2011, 5 (9) 7284-7295 10.1021/nn202116p
6. Kaweeteerawat, C.; Chang, C. H.; Roy, K. R.; Liu, R.; Li, R. B.; Toso, D.; Fischer, H.; Ivask, A.; Ji, Z. X.; Zink, J. I.; Zhou, Z. H.; Chanfreau, G. F.; Telesca, D.; Cohen, Y.; Holden, P. A.; Nel, A. E.; Godwin, H. A. Cu Nanoparticles Have Different Impacts in Escherichia Coli and Lactobacillus Brevis Than Their Microsized and Ionic Analogues ACS Nano 2015, 9 (7) 7215-7225 10.1021/acsnano.5b02021
7. Fahmy, B.; Cormier, S. A. Copper Oxide Nanoparticles Induce Oxidative Stress and Cytotoxicity in Airway Epithelial Cells Toxicol. In Vitro 2009, 23 (7) 1365-1371 10.1016/j.tiv.2009.08.005
8. Ivask, A.; ElBadawy, A.; Kaweeteerawat, C.; Boren, D.; Fischer, H.; Ji, Z.; Chang, C. H.; Liu, R.; Tolaymat, T.; Telesca, D.; Zink, J. I.; Cohen, Y.; Holden, P. A.; Godwin, H. A. Toxicity Mechanisms in Escherichia Coli Vary for Silver Nanoparticles and Differ from Ionic Silver ACS Nano 2014, 8 (1) 374-386 10.1021/nn4044047
9. Yang, Y.; Quensen, J.; Mathieu, J.; Wang, Q.; Wang, J.; Li, M. Y.; Tiedje, J. M.; Alvarez, P. J. J. Pyrosequencing Reveals Higher Impact of Silver Nanoparticles Than Ag+ on the Microbial Community Structure of Activated Sludge Water Res. 2014, 48, 317-325 10.1016/j.watres.2013.09.046
10. George, S.; Lin, S. J.; Ji, Z. X.; Thomas, C. R.; Li, L. J.; Mecklenburg, M.; Meng, H.; Wang, X.; Zhang, H. Y.; Xia, T.; Hohman, J. N.; Lin, S.; Zink, J. I.; Weiss, P. S.; Nel, A. E. Surface Defects on Plate-Shaped Silver Nanoparticles Contribute to Its Hazard Potential in a Fish Gill Cell Line and Zebrafish Embryos ACS Nano 2012, 6 (5) 3745-3759 10.1021/nn204671v
11. Godwin, H.; Nameth, C.; Avery, D.; Bergeson, L. L.; Bernard, D.; Beryt, E.; Boyes, W.; Brown, S.; Clippinger, A. J.; Cohen, Y.; Doa, M.; Hendren, C. O.; Holden, P.; Houck, K.; Kane, A. B.; Klaessig, F.; Kodas, T.; Landsiedel, R.; Lynch, I.; Malloy, T.; Miller, M. B.; Muller, J.; Oberdorster, G.; Petersen, E. J.; Pleus, R. C.; Sayre, P.; Stone, V.; Sullivan, K. M.; Tentschert, J.; Wallis, P.; Nel, A. E. Nanomaterial Categorization for Assessing Risk Potential to Facilitate Regulatory Decision-Making ACS Nano 2015, 9 (4) 3409-3417 10.1021/acsnano.5b00941
12. Wang, Z. Y.; Li, N.; Zhao, J.; White, J. C.; Qu, P.; Xing, B. S. Cuo Nanoparticle Interaction with Human Epithelial Cells: Cellular Uptake, Location, Export, and Genotoxicity Chem. Res. Toxicol. 2012, 25 (7) 1512-1521 10.1021/tx3002093
13. Xiu, Z. M.; Zhang, Q. B.; Puppala, H. L.; Colvin, V. L.; Alvarez, P. J. J. Negligible Particle-Specific Antibacterial Activity of Silver Nanoparticles Nano Lett. 2012, 12 (8) 4271-4275 10.1021/nl301934w
14. Liu, G. Q.; Wang, J. M. Effects of Nano-Copper(Ii) Oxide and Nano-Magnesium Oxide Particles on Activated Sludge Water Environ. Res. 2012, 84 (7) 569-576 10.2175/106143012X13373575830593
15. Clar, J. G.; Li, X.; Impellitteri, C. A.; Bennett-Stamper, C.; Luxton, T. P. Copper Nanoparticle Induced Cytotoxicity to Nitrifying Bacteria in Wastewater Treatment: A Mechanistic Copper Speciation Study by X-Ray Absorption Spectroscopy Environ. Sci. Technol. 2016, 50 (17) 9105-9113 10.1021/acs.est.6b01910
16. Ivask, A.; Bondarenko, O.; Jepihhina, N.; Kahru, A. Profiling of the Reactive Oxygen Species-Related Ecotoxicity of Cuo, Zno, Tio2, Silver and Fullerene Nanoparticles Using a Set of Recombinant Luminescent Escherichia Coli Strains: Differentiating the Impact of Particles and Solubilised Metals Anal. Bioanal. Chem. 2010, 398 (2) 701-716 10.1007/s00216-010-3962-7
17. Chen, L.; Zhou, L.; Liu, Y.; Deng, S.; Wu, H.; Wang, G. Toxicological Effects of Nanometer Titanium Dioxide (Nano-Tio2) on Chlamydomonas Reinhardtii Ecotoxicol. Environ. Saf. 2012, 84, 155-162 10.1016/j.ecoenv.2012.07.019
18. Akhavan, O.; Ghaderi, E. Toxicity of Graphene and Graphene Oxide Nanowalls against Bacteria ACS Nano 2010, 4 (10) 5731-5736 10.1021/nn101390x
19. Ingle, A. P.; Duran, N.; Rai, M. Bioactivity, Mechanism of Action, and Cytotoxicity of Copper-Based Nanoparticles: A Review Appl. Microbiol. Biotechnol. 2014, 98 (3) 1001-1009 10.1007/s00253-013-5422-8
20. Rosenfeld, M.; Ramsey, B. W.; Gibson, R. L. Pseudomonas Acquisition in Young Patients with Cystic Fibrosis: Pathophysiology, Diagnosis, and Management Curr. Opin. Pulm. Med. 2003, 9 (6) 492-497 10.1097/00063198-200311000-00008
21. Morita, Y.; Tomida, J.; Kawamura, Y. Responses of Pseudomonas Aeruginosa to Antimicrobials Front. Microbiol. 2014, 4, 422 10.3389/fmicb.2013.00422
22. Christena, L. R.; Mangalagowri, V.; Pradheeba, P.; Ahmed, K. B. A.; Shalini, B. I. S.; Vidyalakshmi, M.; Anbazhagan, V.; Sai Subramanian, N. Copper Nanoparticles as an Efflux Pump Inhibitor to Tackle Drug Resistant Bacteria RSC Adv. 2015, 5 (17) 12899-12909 10.1039/C4RA15382K
23. Zheng, X.; Su, Y. L.; Chen, Y. G.; Wan, R.; Liu, K.; Li, M.; Yin, D. Q. Zinc Oxide Nanoparticles Cause Inhibition of Microbial Denitrification by Affecting Transcriptional Regulation and Enzyme Activity Environ. Sci. Technol. 2014, 48 (23) 13800-13807 10.1021/es504251v
24. Yang, Y.; Mathieu, J. M.; Chattopadhyay, S.; Miller, J. T.; Wu, T. P.; Shibata, T.; Guo, W. H.; Alvarez, P. J. J. Defense Mechanisms of Pseudomonas Aeruginosa Pao1 against Quantum Dots and Their Released Heavy Metals ACS Nano 2012, 6 (7) 6091-6098 10.1021/nn3011619
25. Gao, S. H.; Fan, L.; Yuan, Z. G.; Bond, P. L. The Concentration-Determined and Population-Specific Antimicrobial Effects of Free Nitrous Acid on Pseudomonas Aeruginosa Pao1 Appl. Microbiol. Biotechnol. 2015, 99 (5) 2305-2312 10.1007/s00253-014-6211-8
26. Gao, S.-H.; Fan, L.; Peng, L.; Guo, J.; Agulló-Barceló, M.; Yuan, Z.; Bond, P. L. Determining Multiple Responses of Pseudomonas Aeruginosa Pao1 to an Antimicrobial Agent, Free Nitrous Acid Environ. Sci. Technol. 2016, 50 (10) 5305-5312 10.1021/acs.est.6b00288
27. Patel, R. K.; Jain, M. Ngs Qc Toolkit: A Toolkit for Quality Control of Next Generation Sequencing Data PLoS One 2012, 7 (2) e30619 10.1371/journal.pone.0030619
28. Trapnell, C.; Roberts, A.; Goff, L.; Pertea, G.; Kim, D.; Kelley, D. R.; Pimentel, H.; Salzberg, S. L.; Rinn, J. L.; Pachter, L. Differential Gene and Transcript Expression Analysis of Rna-Seq Experiments with Tophat and Cufflinks Nat. Protoc. 2012, 7 (3) 562-578 10.1038/nprot.2012.016
29. Gao, S. H.; Ho, J. Y.; Fan, L.; Richardson, D. J.; Yuan, Z. G.; Bond, P. L. Antimicrobial Effects of Free Nitrous Acid on Desulfovibrio Vulgaris: Implications for Sulfide-Induced Corrosion of Concrete Appl. Environ. Microbiol. 2016, 82 (18) 5563-5575 10.1128/AEM.01655-16
30. Mu, J. C.; Jiang, H.; Kiani, A.; Mohiyuddin, M.; Bani Asadi, N.; Wong, W. H. Fast and Accurate Read Alignment for Resequencing Bioinformatics 2012, 28 (18) 2366-2373 10.1093/bioinformatics/bts450
31. Krzywinski, M.; Schein, J.; Birol, I.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S. J.; Marra, M. A. Circos: An Information Aesthetic for Comparative Genomics Genome Res. 2009, 19 (9) 1639-1645 10.1101/gr.092759.109
32. Sullivan, M. J.; Gates, A. J.; Appia-Ayme, C.; Rowley, G.; Richardson, D. J. Copper Control of Bacterial Nitrous Oxide Emission and Its Impact on Vitamin B-12-Dependent Metabolism Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (49) 19926-19931 10.1073/pnas.1314529110
33. Korshed, P.; Li, L.; Liu, Z.; Wang, T. The Molecular Mechanisms of the Antibacterial Effect of Picosecond Laser Generated Silver Nanoparticles and Their Toxicity to Human Cells PLoS One 2016, 11 (8) e0160078 10.1371/journal.pone.0160078
34. Sharma, V.; Noriega, C. E.; Rowe, J. J. Involvement of Nark1 and Nark2 Proteins in Transport of Nitrate and Nitrite in the Denitrifying Bacterium Pseudomonas Aeruginosa Pao1 Appl. Environ. Microb. 2006, 72 (1) 695-701 10.1128/AEM.72.1.695-701.2006
35. Su, Y.; Zheng, X.; Chen, Y.; Li, M.; Liu, K. Alteration of Intracellular Protein Expressions as a Key Mechanism of the Deterioration of Bacterial Denitrification Caused by Copper Oxide Nanoparticles Sci. Rep. 2015, 5, 15824 10.1038/srep15824
36. Altimira, F.; Yáñez, C.; Bravo, G.; González, M.; Rojas, L. A.; Seeger, M. Characterization of Copper-Resistant Bacteria and Bacterial Communities from Copper-Polluted Agricultural Soils of Central Chile BMC Microbiol. 2012, 12, 193-193 10.1186/1471-2180-12-193
37. Elguindi, J.; Wagner, J.; Rensing, C. Genes Involved in Copper Resistance Influence Survival of Pseudomonas Aeruginosa on Copper Surfaces J. Appl. Microbiol. 2009, 106 (5) 1448-1455 10.1111/j.1365-2672.2009.04148.x
38. Teitzel, G. M.; Geddie, A.; De Long, S. K.; Kirisits, M. J.; Whiteley, M.; Parsek, M. R. Survival and Growth in the Presence of Elevated Copper: Transcriptional Profiling of Copper-Stressed Pseudomonas Aeruginosa J. Bacteriol. 2006, 188 (20) 7242-7256 10.1128/JB.00837-06
39. Kumar, A.; Schweizer, H. P. Bacterial Resistance to Antibiotics: Active Efflux and Reduced Uptake Adv. Drug Delivery Rev. 2005, 57 (10) 1486-1513 10.1016/j.addr.2005.04.004
40. Nies, D. H. Efflux-Mediated Heavy Metal Resistance in Prokaryotes FEMS Microbiol. Rev. 2003, 27 (2-3) 313-339 10.1016/S0168-6445(03)00048-2
41. Hassan, M. E. T.; van der Lelie, D.; Springael, D.; Romling, U.; Ahmed, N.; Mergeay, M. Identification of a Gene Cluster, Czr, Involved in Cadmium and Zinc Resistance in Pseudomonas Aeruginosa Gene 1999, 238 (2) 417-425 10.1016/S0378-1119(99)00349-2
42. Rensing, C.; Pribyl, T.; Nies, D. H. New Functions for the Three Subunits of the Czccba Cation-Proton Antiporter J. Bacteriol. 1997, 179 (22) 6871-6879 10.1128/jb.179.22.6871-6879.1997
43. Rice, S. A.; Tan, C. H.; Mikkelsen, P. J.; Kung, V.; Woo, J.; Tay, M.; Hauser, A.; McDougald, D.; Webb, J. S.; Kjelleberg, S. The Biofilm Life Cycle and Virulence of Pseudomonas Aeruginosa Are Dependent on a Filamentous Prophage ISME J. 2009, 3 (3) 271-282 10.1038/ismej.2008.109
44. Platt, M. D.; Schurr, M. J.; Sauer, K.; Vazquez, G.; Kukavica-Ibrulj, I.; Potvin, E.; Levesque, R. C.; Fedynak, A.; Brinkman, F. S. L.; Schurr, J.; Hwang, S. H.; Lau, G. W.; Limbach, P. A.; Rowe, J. J.; Lieberman, M. A.; Barraud, N.; Webb, J.; Kjelleberg, S.; Hunt, D. F.; Hassett, D. J. Proteomic, Microarray, and Signature-Tagged Mutagenesis Analyses of Anaerobic Pseudomonas Aeruginosa at Ph 6.5, Likely Representing Chronic, Late-Stage Cystic Fibrosis Airway Conditions J. Bacteriol. 2008, 190 (8) 2739-2758 10.1128/JB.01683-07
45. Barraud, N.; Hassett, D. J.; Hwang, S. H.; Rice, S. A.; Kjelleberg, S.; Webb, J. S. Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas Aeruginosa J. Bacteriol. 2006, 188 (21) 7344-7353 10.1128/JB.00779-06
46. Whiteley, M.; Bangera, M. G.; Bumgarner, R. E.; Parsek, M. R.; Teitzel, G. M.; Lory, S.; Greenberg, E. P. Gene Expression in Pseudomonas Aeruginosa Biofilms Nature 2001, 413 (6858) 860-864 10.1038/35101627
47. Yang, Y.; Alvarez, P. J. J. Sublethal Concentrations of Silver Nanoparticles Stimulate Biofilm Development Environ. Sci. Technol. Lett. 2015, 2 (8) 221-226 10.1021/acs.estlett.5b00159
48. Boles, B. R.; Thoendel, M.; Singh, P. K. Self-Generated Diversity Produces ″Insurance Effects″ in Biofilm Communities Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (47) 16630-16635 10.1073/pnas.0407460101
49. Campbell, A. The Future of Bacteriophage Biology Nat. Rev. Genet. 2003, 4 (6) 471-477 10.1038/nrg1089
50. Furuya, E. Y.; Lowy, F. D. Antimicrobial-Resistant Bacteria in the Community Setting Nat. Rev. Microbiol. 2006, 4 (1) 36-45 10.1038/nrmicro1325
51. Guo, J.; Peng, Y.; Wang, S.; Ma, B.; Ge, S.; Wang, Z.; Huang, H.; Zhang, J.; Zhang, L. Pathways and Organisms Involved in Ammonia Oxidation and Nitrous Oxide Emission Crit. Rev. Environ. Sci. Technol. 2013, 43 (21) 2213-2296 10.1080/10643389.2012.672072