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An Antiviral Trap Made of Protein Nanofibrils and Iron Oxyhydroxide Nanoparticles

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An Antiviral Trap Made of Protein Nanofibrils and Iron Oxyhydroxide Nanoparticles ARTICLES https://doi.org/10.1038/s41565-021-00920-5 An antiviral trap made of protein nanofibrils and iron oxyhydroxide nanoparticles Archana Palika1, Antonius Armanious 1, Akram Rahimi1,2, Chiara Medaglia3, Matteo Gasbarri 4, Stephan Handschin1, Antonella Rossi 5,6, Marie O. Pohl7, Idoia Busnadiego7, Christian Gübeli1, Ravi B. Anjanappa8, Sreenath Bolisetty1,2, Mohammad Peydayesh 1, Silke Stertz7, Benjamin G. Hale 7, Caroline Tapparel3, Francesco Stellacci 4,9 and Raffaele Mezzenga 1,6 ✉ Minimizing the spread of viruses in the environment is the first defence line when fighting outbreaks and pandemics, but the current COVID-19 pandemic demonstrates how difficult this is on a global scale, particularly in a sustainable and environmen- tally friendly way. Here we introduce and develop a sustainable and biodegradable antiviral filtration membrane composed of amyloid nanofibrils made from food-grade milk proteins and iron oxyhydroxide nanoparticles synthesized in situ from iron salts by simple pH tuning. Thus, all the membrane components are made of environmentally friendly, non-toxic and widely available materials. The membrane has outstanding efficacy against a broad range of viruses, which include enveloped, non-enveloped, airborne and waterborne viruses, such as SARS-CoV-2, H1N1 (the influenza A virus strain responsible for the swine flu pandemic in 2009) and enterovirus 71 (a non-enveloped virus resistant to harsh conditions, such as highly acidic pH), which highlights a possible role in fighting the current and future viral outbreaks and pandemics. he current ongoing COVID-19 pandemic illustrates the For airborne viruses, suitable face masks, although effective, pose importance of valid therapeutic tools1, but also the notable the risk of further dissemination of the viruses when improperly Tlack of technologies capable of fighting the spread of viruses in handled20 and/or disposed21,22. Additionally, the generated plastic the environment. Many viruses diffuse and transmit in the environ- waste eventually emerges as a parallel environmental problem, espe- ment in water, some in their bulk form (waterborne viruses)2–4 and cially in times of pandemics10–12. For waterborne viruses, and despite others in small droplets suspended in the air (airborne viruses)5–9. decades-long technological developments, contaminated drinking A key defence strategy against infectious diseases is always the pre- water is still responsible for 500,000 annual deaths, of which more vention of pathogen transmission from an infected person to an than half occur in children under five years of age23. Non-enveloped uninfected one. This is achieved by using masks, gloves, physical enteric viruses, such as enteroviruses, adenoviruses and rotaviruses, barriers and disinfection, which introduces other challenges on a can cause gastrointestinal infections with diseases such as diarrhoea global scale, such as achieving the goal in a fully sustainable and and dysentery. It is estimated that ~40% of often-fatal childhood environmentally friendly way10–12. diarrhoea in developing countries is connected to viral agents24. In particular, the COVID-19 pandemic revealed the paradox Non-enveloped viruses can persist in water bodies for long periods that, although both technological and scientific knowledge are of time25 and can resist even some of the harshest treatments26,27. available to develop a vaccine within the record time of less than a This challenge is not only exclusive to unfavoured communities, year13,14, there is still a lack of preparedness to fight the rapid spread but extends also to countries with state-of-the-art water and waste- of new viruses until such vaccines are developed and a substantial water treatment facilities2. Furthermore, even enveloped viruses, portion of the population is vaccinated15. Without the appropriate such as influenza viruses and coronaviruses, which were often readiness, viruses spread widely and rapidly and, eventually, new regarded as unstable in water environments, have now been shown virus strains emerge via mutations16,17, which could potentially con- to remain highly infective for long times in bulk water bodies28,29: fer resistance to vaccines that target the original strain or increase SARS-CoV-2, for example, can retain its infectivity for longer than the virulence of the virus, and possibly lead to an endless vicious seven days in tap water and wastewater at room temperature30. cycle. Viruses can spread through many different routes, but mostly Therefore, the development of efficient barriers against the through fomites18, small water droplets5–9 and bulk water bodies spread of viruses via diffusing environmental fluids becomes cru- (which include wastewater)2–4. Proper hand hygiene serves as a very cial if global contamination is to be prevented. In spite of decades effective practice against the spread of infections through fomites19. of scientific and technological development, no existing tech- In all the other cases, however, virus inactivation must be tackled nology can universally eliminate viruses from water, unless it is in the hosting fluid, and the overarching strategy is then to target extremely energy intensive (for example, reverse osmosis)31 or starts the virus in its surrounding aqueous environment, may this be in to pose the risk of toxicity towards humans and the environment the form of microscopic suspended water droplets or bulk waters. (for example, silver-based technologies)32,33. All these limitations 1Department of Health Sciences and Technology, ETH Zurich, Zurich, Switzerland. 2BluAct Technologies GmbH, Zurich, Switzerland. 3Department of Microbiology and Molecular Medicine, University of Geneva, Geneva, Switzerland. 4Institute of Materials, Ecolé Polytechnique Fedé ralé de Lausanne (EPFL), Lausanne, Switzerland. 5Department of Chemical and Geological Science, University of Cagliari, Cagliari, Italy. 6Department of Materials, ETH Zurich, Zurich, Switzerland. 7Institute of Medical Virology, University of Zurich, Zurich, Switzerland. 8Department of Biology, ETH Zurich, Zurich, Switzerland. 9Department of Bioengineering, Ecolé Polytechnique Fedé ralé de Lausanne (EPFL), Lausanne, Switzerland. ✉e-mail: [email protected] 918 NatURE NanotECHNOLOGY | VOL 16 | August 2021 | 918–925 | www.nature.com/naturenanotechnology NATURE NANOTECHNOLOGY ARTICLES a b pH 2, 90 °C FeCl ·6H O Fabrication 3 2 5 h NaOH BLG AF–Fe BLG monomers BLG AF BLG AF–Fe Infectious viruses c d e Cellulose support 1 µm 1 µm Characterization No infectious viruses 1 µm 100 nm 1 µm Fig. 1 | Schematic, fabrication and characterization of BLG AF–Fe membranes. a, A schematic showing the filtration set-up. b, A schematic showing the fabrication processes of the BLG AF–Fe membranes. c, Cryo-SEM micrographs of freeze-fractured and freeze-etched hydrated BLG AF–Fe hybrids at two magnifications. d, Cryo-TEM image of the BLG AF–Fe hybrids; the BLG AF–Fe hybrids were prepared using a fivefold lower Fe concentration (10 mgFe ml−1) than the concentration normally used to prepare the membranes to enable the visualization of single Fe NPs. e, SEM micrographs of a chemically fixed and critical point-dried sample of the filter bulk material at two magnifications. Representations of the virions in a are reproduced from pictures on ViralZone51. The cartoon structure of the BLG monomers in b is based on the crystallographic structures 5IO552 obtained from the Protein Data Bank53 (http://www. rcsb.org/, accessed October 2020). render the existing technologies obsolete facing global challenges high-contrast images, the dense packing of the Fe NPs on the such as pandemics. surface of AFs. It is important to mention that the observed dif- To address such a challenge, we developed an antiviral mem- ference in the Fe NP density between the cryo-SEM (Fig. 1c) and brane trap composed of amyloid nanofibrils obtained from a the SEM (Fig. 1e) micrographs is due to the shrinkage of the sam- food-grade milk protein, β-lactoglobulin (BLG), modified in situ ple during preparation and drying. with iron oxyhydroxide nanoparticles (NPs) (Fig. 1a). The con- version of BLG monomers into a network of amyloid fibrils (AFs) Performance of membranes on enveloped viruses is a straightforward process achieved by simply lowering the pH We first tested this filtration membrane trap by filtering water that to 2.0 with simultaneous heating up to 90 °C; afterwards, the iron contained three different types of enveloped viruses: (1) Φ6, an oxyhydroxide NPs are precipitated directly on the formed network enveloped bacteriophage that infects Pseudomonas syringae bacte- 34 of AFs by raising the pH in the presence of FeCl3·6H2O. Figure 1b ria and is often used as a surrogate of human enveloped viruses , shows a schematic of the process; the detailed chemical analy- (2) H1N1, an influenza A virus strain responsible for the swine flu sis and composition of the iron NPs as studied by X-ray photo- pandemic in 200935 and (3) SARS-CoV-2, the coronavirus strain electron spectroscopy (XPS) reveals the presence of both iron(ii) responsible for the ongoing COVID-19 pandemic. The membrane and iron(iii) oxide and iron chloride species that coexist with the showed an efficiency of more than six orders of magnitude reduc- majority of iron oxyhydroxide NPs (Supplementary Fig. 1). By tion in infectivity for all three viruses (Fig. 2). The infectious virus depositing the produced material on a porous solid support, we concentrations went from ~106 PFU ml−1 before filtration to below
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