Cryptosporidium parvum oocyst directed assembly of gold nanoparticles and graphene oxide

Abstract

Understanding the interactions between inorganic nanomaterials and biological species is an important topic for surface and environmental chemistry. In this work, we systematically studied the oocysts of Cryptosporidium parvum as a model protozoan parasite and its interaction with gold nanoparticles (AuNPs) and graphene oxide (GO). The as-prepared citrate-capped AuNPs adsorb strongly on the oocysts leading to a vivid color change. The adsorption of the AuNPs was confirmed by transmission electron microscopy. Heat treatment fully inhibited the color change, indicating a large change of surface chemistry of the oocysts that can be probed by the AuNPs. Adding proteases such as trypsin and proteinase K partially inhibited the color change. DNA-capped AuNPs, on the other hand, could not be adsorbed by the oocysts. GO was found to wrap around the oocysts forming a conformal shell reflecting the shape of the oocysts. Both citrate-capped AuNPs and GO compromised the membrane integrity of the oocysts as indicated by the propidium iodide staining experiment, and they may be potentially used for inactivating the oocysts. This is the first example of using nanomaterials to probe the surface of the oocysts, and it suggests the possibility of using such organisms to template the assembly of nanomaterials.

Graphical abstract

Keywords

nanomaterials / toxicology / water / biosensors

References

[1] Macfarlane R J, Lee B, Jones M R, Harris N, Schatz G C, Mirkin C A. Nanoparticle superlattice engineering with DNA. Science, 2011, 334(6053): 204–208

[2] Geim A K. Graphene: Status and prospects. Science, 2009, 324(5934): 1530–1534

[3] Montini T, Melchionna M, Monai M, Fornasiero P. Fundamentals and catalytic applications of CeO₂-based materials. Chemical Reviews, 2016, 116(10): 5987–6041

[4] Daniel M C, Astruc D. Gold nanoparticles: Assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. Chemical Reviews, 2004, 104(1): 293–346

[5] Ghafari P, St-Denis C H, Power M E, Jin X, Tsou V, Mandal H S, Bols N C, Tang X. Impact of carbon nanotubes on the ingestion and digestion of bacteria by ciliated protozoa. Nature Nanotechnology, 2008, 3(6): 347–351

[6] Krysanov E Y, Pavlov D S, Demidova T B, Dgebuadze Y Y. Effect of nanoparticles on aquatic organisms. Biological Bulletin, 2010, 37(4): 406–412

[7] Klaine S J, Alvarez P J J, Batley G E, Fernandes T F, Handy R D, Lyon D Y, Mahendra S, McLaughlin M J, Lead J R. Nanomaterials in the environment: Behavior, fate, bioavailability, and effects. Environmental Toxicology and Chemistry, 2008, 27(9): 1825–1851

[8] Dogan-Topal B, Uslu B, Ozkan S A. Detection of DNA damage induced by nanomaterials. In: Nanoscale Fabrication, Optimization, Scale-Up and Biological Aspects of Pharmaceutical Nanotechnology. New York: William Andrew Publishing, 2018, 547–577

[9] Jahan S, Yusoff I B, Alias Y B, Bakar A F B A. Reviews of the toxicity behavior of five potential engineered nanomaterials (ENMs) into the aquatic ecosystem. Toxicology Reports, 2017, 4: 211–220

[10] Wang F, Salvati A, Boya P. Lysosome-dependent cell death and deregulated autophagy induced by amine-modified polystyrene nanoparticles. Open Biology, 2018, 8(4): 1–13

[11] Leitch G J, He Q. Cryptosporidiosis––an overview. Journal of Biomedical Research, 2011, 25(1): 1–16

[12] Nanduri J, Williams S, Aji T, Flanigan T P. Characterization of an immunogenic glycocalyx on the surfaces of Cryptosporidium parvum oocysts and sporozoites. Infection and Immunity, 1999, 67(4): 2022–2024

[13] Kuznar Z A, Elimelech M. Role of surface proteins in the deposition kinetics of Cryptosporidium parvum oocysts. Langmuir, 2005, 21(2): 710–716

[14] Liu Y, Kuhlenschmidt M S, Kuhlenschmidt T B, Nguyen T H. Composition and conformation of Cryptosporidium parvum oocyst wall surface macromolecules and their effect on adhesion kinetics of oocysts on quartz surface. Biomacromolecules, 2010, 11(8): 2109–2115

[15] Storhoff J L, Elghanian R, Mucic R C, Mirkin C A, Letsinger R L. One-pot colorimetric differentiation of polynucleotides with single base imperfections using gold nanoparticle probes. Journal of the American Chemical Society, 1998, 120(9): 1959–1964

[16] Liu J, Lu Y. Preparation of aptamer-linked gold nanoparticle purple aggregates for colorimetric sensing of analytes. Nature Protocols, 2006, 1(1): 246–252

[17] Liu B, Wu P, Huang Z, Ma L, Liu J. Bromide as a robust backfiller on gold for precise control of DNA conformation and high stability of spherical nucleic acids. Journal of the American Chemical Society, 2018, 140(13): 4499–4502

[18] Bushkin G G, Motari E, Carpentieri A, Dubey J P, Costello C E, Robbins P W, Samuelson J. Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria. mBio, 2013, 4(5): 1–8

[19] Jenkins M B, Eaglesham B S, Anthony L C, Kachlany S C, Bowman D D, Ghiorse W C. Significance of wall structure, macromolecular composition, and surface polymers to the survival and transport of Cryptosporidium parvum oocysts. Applied and Environmental Microbiology, 2010, 76(6): 1926–1934

[20] Rosi N L, Mirkin C A. Nanostructures in biodiagnostics. Chemical Reviews, 2005, 105(4): 1547–1562

[21] Liu B, Liu J. Methods for preparing DNA-functionalized gold nanoparticles, a key reagent of bioanalytical chemistry. Analytical Methods, 2017, 9(18): 2633–2643

[22] Otten L, Vlachou D, Richards S J, Gibson M I. Glycan heterogeneity on gold nanoparticles increases lectin discrimination capacity in label-free multiplexed bioassays. Analyst (London), 2016, 141(14): 4305–4312

[23] Wang F, Liu J. Self-healable and reversible liposome leakage by citrate-capped gold nanoparticles: Probing the initial adsorption/desorption induced lipid phase transition. Nanoscale, 2015, 7(38): 15599–15604

[24] Wang F, Curry D E, Liu J. Driving adsorbed gold nanoparticle assembly by merging lipid gel/fluid interfaces. Langmuir, 2015, 31(49): 13271–13274

[25] Liu B, Huang Z, Liu J. Polyvalent spherical nucleic acids for universal display of functional DNA with ultrahigh stability. Angewandte Chemie International Edition, 2018, 57(30): 9439–9442

[26] Cutler J I, Auyeung E, Mirkin C A. Spherical nucleic acids. Journal of the American Chemical Society, 2012, 134(3): 1376–1391

[27] Tan L H, Xing H, Lu Y. DNA as a powerful tool for morphology control, spatial positioning, and dynamic assembly of nanoparticles. Accounts of Chemical Research, 2014, 47(6): 1881–1890

[28] Wang J, Zhang L, Peng F, Shi X, Leong D T. Targeting endothelial cell junctions with negatively charged gold nanoparticles. Chemistry of Materials, 2018, 30(11): 3759–3767

[29] Huang M L, Godula K. Nanoscale materials for probing the biological functions of the glycocalyx. Glycobiology, 2016, 26(8): 797–803

[30] Novoselov K S, Falko V I, Colombo L, Gellert P R, Schwab M G, Kim K. A roadmap for graphene. Nature, 2012, 490(7419): 192–200

[31] Liu J. Adsorption of DNA onto gold nanoparticles and graphene oxide: Surface science and applications. Physical Chemistry Chemical Physics, 2012, 14(30): 10485–10496

[32] Ip A C F, Liu B, Huang P J J, Liu J. Oxidation level-dependent zwitterionic liposome adsorption and rupture by graphene-based materials and light-induced content release. Small, 2013, 9(7): 1030–1035

[33] Ang P K, Jaiswal M, Lim C H, Wang Y, Sankaran J, Li A, Lim C T, Wohland T, Barbaros O, Loh K P. A bioelectronic platform using a graphene-lipid bilayer interface. ACS Nano, 2010, 4(12): 7387–7394

[34] Tu Y, Lv M, Xiu P, Huynh T, Zhang M, Castelli M, Liu Z, Huang Q, Fan C, Fang H, Zhou R. Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nature Nanotechnology, 2013, 8(8): 594–601

[35] Xue J, BinAhmed S, Wang Z, Karp N G, Stottrup B L, Romero-Vargas Castrillón S. Bacterial adhesion to graphene oxide (GO)-functionalized interfaces is determined by hydrophobicity and GO sheet spatial orientation. Environmental Science & Technology Letters, 2018, 5(1): 14–19

[36] Kempaiah R, Chung A, Maheshwari V. Graphene as cellular interface: Electromechanical coupling with cells. ACS Nano, 2011, 5(7): 6025–6031

[37] Zhang B, Wei P, Zhou Z, Wei T. Interactions of graphene with mammalian cells: Molecular mechanisms and biomedical insights. Advanced Drug Delivery Reviews, 2016, 105: 145–162

[38] Li B L, Wang J, Gao Z F, Shi H, Zou H L, Ariga K, Leong D T. Ratiometric immunoassays built from synergistic photonic absorption of size-diverse semiconducting MoS₂ nanostructures. Materials Horizons, 2018, 6: 563–570

[39] Li B L, Wang J, Zou H L, Garaj S, Lim C T, Xie J, Li N B, Leong D T. Low-dimensional transition metal dichalcogenide nanostructures based sensors. Advanced Functional Materials, 2016, 26(39): 7034–7056

[40] Li B L, Setyawati M I, Zou H L, Dong J X, Luo H Q, Li N B, Leong D T. Emerging 0D transition-metal dichalcogenides for sensors, biomedicine, and clean energy. Small, 2017, 13(31): 1–20

[41] Mokhtarzadeh A, Eivazzadeh-Keihan R, Pashazadeh P, Hejazi M, Gharaatifar N, Hasanzadeh M, Baradaran B, de la Guardia M. Nanomaterial-based biosensors for detection of pathogenic virus. Trends in Analytical Chemistry, 2017, 97: 445–457

[42] Fayer R. Effect of high temperature on infectivity of Cryptosporidium parvum oocysts in water. Applied and Environmental Microbiology, 1994, 60(8): 2732–2735

[43] Cameron P, Gaiser B K, Bhandari B, Bartley P M, Katzer F, Bridle H. Silver nanoparticles decrease the viability of Cryptosporidium parvum oocysts. Applied and Environmental Microbiology, 2016, 82(2): 431–437

[44] Maiti S, Krishnan D, Barman G, Ghosh S K, Laha J K. Antimicrobial activities of silver nanoparticles synthesized from Lycopersiconesculentum extract. Journal of Analytical Science and Technology, 2014, 5(40): 1–7

[45] Giljohann D A, Seferos D S, Daniel W L, Massich M D, Patel P C, Mirkin C A. Gold nanoparticles for biology and medicine. Angewandte Chemie International Edition, 2010, 49(19): 3280–3284

Acknowledgements

Funding for this work was from the Advancing Water Technologies (AWT) program of the Southern Ontario Water Consortium.

RIGHTS & PERMISSIONS

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