Research PaperProteinaceous porous nanofiber membrane-type adsorbent derived from amyloid lysozyme protofilaments for highly efficient lead(II) biologic scavenging
Graphical Abstract
Introduction
Water contamination by heavy metals is one of the gravest threats observed around the world for humanity and the aquatic ecosystem (Chai et al., 2021, Reddy and Lee, 2013). Among the most hazardous heavy metals, lead (Pb) ions that enter into hydrological cycles are very harmful to lung, kidney, brain, and central nervous system when human exposure, eventually resulting in loss of memory ability and cognitive competence of individuals decline (Zhang et al., 2021). In recent years, various remediation techniques such as flocculation, membrane filtration, adsorption, and electrodialysis are suggested to remove lead ions from wastewater (Hua et al., 2013). Among the aforesaid techniques, adsorption is selected as a candidate for the most promising water remediation, owing to its operational simplicity, low cost, and little secondary pollution. The key of adsorption technology is upon the construction of ideal adsorbents with rational microstructure and sufficient surface chemistry. Nevertheless, the conventional powder adsorbents typically suffer from removal performance and renewability, due to formless structure and deficiency of surface chemistry. Therefore, the development of novel functional materials with ordered structure remains a challenge for enhancing the pollutant removal capacity while maintaining environmental sustainability.
As an appealing biomacromolecule, protein functional materials have appeared as new-generation candidates for biosorption of heavy metals, thanks to the presence of abundant amino-acids components along with wide-ranging binding capabilities (Jiménez-Rosado et al., 2021). Hen lysozyme, one kind of low-cost food protein, can exactly make lead salt adsorbed into the largest pocket associated with the catalytic residues (Glu 35, Asp 52) and the fluorophores (Trp 62, Trp 108) (Zhang et al., 2013). However, the water-soluble property of lysozyme limits its practical application as one adsorbent. To strengthen its availability and insolubility, lysozyme as adsorption ligands is usually modified by immobilization or crosslinking on solid matrix into the usable adsorption technology. For example, Kasher, etc. (Rathinam et al., 2018) immobilized the lysozyme onto chitosan to form biocomposite through crosslinking for enhancing the removal performances of heavy metals. However, the immobilization of adsorption ligands exists a possible risk of ligands leaching during operation while also compromising the advanced values and effective utilization of protein itself. Hence, the realization of processing into the insoluble matter with highly ordered microstructure and rich surface chemistry for lysozyme appeals strongly. Recently, protein amyloid denaturation provides the possibility to design functional artificial materials. In the pathology, amyloid fibrils formed in the extracellular space of tissues are culpable for their implications in the majority of degenerative and debilitating diseases, like Alzheimer’s disease and other incurable degenerative diseases (Knowles et al., 2014). In particular, when fibrillation occurs in vitro, the resultant lysozyme nanofibrils acquire an ultrahigh surface-to-volume ratio, placing amino-acid constituents densely on the surfaces, thus contributing to excellent scavenging ability for the majority of heavy metals (Bolisetty and Mezzenga, 2016, Zhang et al., 2019). However, while amyloid fibrils are undoubted adsorbents for toxic heavy metals due to strong metal-ligand interactions, one of the main issues of facing the usage of amyloid fibrils is the colloid nature stemmed from their tiny dimensions, leading to knotty separation problems in large-scale wastewater purification as well as the tremendous difficulty in recovery that may re-pollute treated water. Additionally, lysozyme may reject the positively charged lead ions because of its high isoelectric point (~11.0). To conquer these obstacles, the conventional solution is to hybridize amyloid fibrils with other organic/inorganic materials. For instance, Carmen, etc. (Silva et al., 2020) prepared the bio-sorbent films made up of lysozyme nanofibrils and nanocellulose for trace mercury removal. However, it's noteworthy that one of the dominating trigger factors for enhanced interactions between metal ions and adsorbents is the surface area, since the sorption energy decreases rapidly when the increased concentrations at surfaces of adsorbates. The above-mentioned hybrid approach inevitably sacrifices the function superiority of lysozyme fibrils, such as nanofibrous morphology, surface chemistry, and high surface area, incurring the actuality that adsorption performances are far from satisfactory. Hence, the production of nanofiber-based bioadsorbent with a high surface area is extremely advisable. Currently, there’s been little research on the reconstruction of lysozyme nanofibrils other than hybridization, and the traditional phase transition only relying on the natural evolution of individual protofilaments into mature fibrils cannot already satisfy the requirement of environmental engineering. Therefore, the choice of suitable adjuvant begins to get our attention.
Dopamine (DA), a mussel adhesive protein, can spontaneously be oxidized into dark polydopamine (pDA) via self-crosslinking ad intramolecular rearrangement, which is a representative polyphenol because of its versatility and eco-friendliness (Yang et al., 2022). Rich amine and catechol groups of pDA chains provide adequate active sites for removing lead ions, which can further react with amino-rich amyloid lysozyme by classical Michael addition reaction and/or Schiff base reaction. However, simple pDA microspheres are restricted by their easy aggregation and difficult separation. To enhance the applicability of pDA, the pDA has been widely used in surface modification onto substrate materials with various shapes and sizes, owing to super adhesive features and plentiful functional groups. Interestingly, the modification of the pDA has an immense performance enhancement on the scavenging of target pollutants (Chen et al., 2020). More importantly, this adhesive character will readily form a versatile coating layer on the surface of original substrate materials with no morphology damage and also improve their surface chemistry when appropriate conditions. In this view, amyloid lysozyme protofilaments seem to afford an excellent platform to carry the deposition of the pDA, bettering the colloidal nature and high isoelectric point of lysozyme species mentioned in the previous paragraph.
Based on the aforesaid ideas, we propose a co-operative (two-stages) strategy to successfully achieve the transition from water-soluble lysozyme proteins into lysozyme complex nanofibers using pDA as a complementary adjuvant. In the first stage, dissolved lysozyme monomers unfold, hydrolyze, and firstly self-assemble into protofilaments under the conditions of low pH and elevated temperature, laying a linear foundation for nanofiber membrane. When the second stage, multistranded protofilaments are “seamed” and converted into robust complex nanofibers under the assistance of active catechol from pDA components. The formation of lysozyme complex nanofibers destroys the stable colloidal limitation owing to the diameter expansion and improves the surface chemistry owing to the pDA coating. Then the hierarchical porous nanofiber membrane-type adsorbent is expectably prepared with a high surface area using complex nanofibers as building blocks via the simple vacuum filtration for the decontaminating of lead-containing wastewater. The membrane property, ions' selectivity, adsorption kinetic and isotherms, possible adsorption mechanism as well as reusability are investigated in detail. We believe that this work offers a universal transformation path from water-soluble globular proteins into exercisable nanofiber membrane for environmental applications.
Section snippets
Materials
All used chemical reagents were of analytical grade and were commercially provided from the Kelong Chemical Reagent Co., Ltd (Sichuan, China) unless otherwise specified. Bio-PURE lysozyme, dopamine hydrochloride (purity ≥ 98.5%), and thioflavin T (ThT) dye (purity ≥ 75%) were supplied from Yuanye Biotechnology Co., Ltd (Shanghai, China). The polyether sulfone (PES) and mixed cellulose ester (MCE) microfiltration membranes with 0.22 µm mean pore size were commercially available from Shanghai
Principle of Lys-CNFs membrane
Fig. 1 illustrates the possible principle of Lys-CNFs membrane formation by using lysozyme complex nanofibers as building blocks, which includes the macroscopic and microcosmic levels. As we know, lysozyme is a very low-cost food protein that is typically extracted from hen egg white. Given that, lysozyme was chosen as proteins resource for constructing the protein-based porous materials. During the fabrication process, the lysozyme was exposed at high temperature in an acidic environment
Conclusion
To summarize, we designed and successfully prepared a lysozyme-based nanofiber membrane-type adsorbent consisting of amyloid protofilaments coupled to pDA for the remediation of lead-containing wastewater. The lysozyme nanofibrils with a high aspect ratio provide the structural basis, and pDA mainly takes charge of diameter expansion and enhancing surface chemistry. The obtained membrane with hierarchical porous and layer stacking structure discloses a large specific surface area (220.4 m2/g)
CRediT authorship contribution statement
Kaifeng Du: Conceptualization, Writing – review & editing, Supervision, Funding acquisition. Chao Liang: Investigation, Data curation, Writing – original draft preparation, Methodology, Software. Liangshen Zhao: Visualization, Data curation, Validation. Liangzhi Qiao: Formal analysis, Validation.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work was financially funded by the National Natural Science Foundation of China (21676170). Thanks to the Engineering Experimental Teaching Center, School of Chemical Engineering, Sichuan University for the atomic flame spectrophotometer and FTIR technical assistance. We also thank Yanping Huang from Center of Engineering Experimental Teaching, School of Chemical Engineering, Sichuan University for the help of SEM images, as well as eceshi (www.eceshi.com) for the CD spectra. C.L. would
References (43)
- et al.
A review on conventional and novel materials towards heavy metal adsorption in wastewater treatment application
J. Clean. Prod.
(2021) - et al.
Polydopamine modified cyclodextrin polymer as efficient adsorbent for removing cationic dyes and Cu2+
J. Hazard. Mater.
(2020) - et al.
Synthesis of membrane-type graphene oxide immobilized manganese dioxide adsorbent and its adsorption behavior for lithium ion
Chemosphere
(2021) - et al.
Adsorptive removal of Pb2+, Co2+ and Ni2+ by hydroxyapatite/chitosan composite from aqueous solution
J. Taiwan Inst. Chem. Eng.
(2012) - et al.
Eco-friendly protein-based materials for a sustainable fertilization in horticulture
J. Clean. Prod.
(2021) - et al.
Study on the adsorption behavior of glutaric acid modified Pb(II) imprinted chitosan-based composite membrane to Pb(II) in aqueous solution
Mater. Lett.
(2019) - et al.
Functional fibrous materials-based adsorbents for uranium adsorption and environmental remediation
Chem. Eng. J.
(2020) - et al.
An environmentally-friendly chitosan-lysozyme biocomposite for the effective removal of dyes and heavy metals from aqueous solutions
Carbohydr. Polym.
(2018) - et al.
Synthesis of biomass trans-anethole based magnetic hollow polymer particles and their applications as renewable adsorbent
Chem. Eng. J.
(2018) - et al.
Kinetics and equilibrium adsorption study of lead(II) onto activated carbon prepared from coconut shell
J. Colloid Interface Sci.
(2004)
Dual nanofibrillar-based bio-sorbent films composed of nanocellulose and lysozyme nanofibrils for mercury removal from spring waters
Carbohydr. Polym.
Crayfish shell biochar for the mitigation of Pb contaminated water and soil: characteristics, mechanisms, and applications
Environ. Pollut.
Supramolecular proteinaceous biofilms as trapping sponges for biologic water treatment and durable catalysis
J. Colloid Interface Sci.
High performance nanocomposite nanofiltration membranes with polydopamine-modified cellulose nanocrystals for efficient dye/salt separation
Desalination
Development of effective nano-biosorbent based on poly m-phenylenediamine grafted dextrin for removal of Pb (II) and methylene blue from water
Carbohydr. Polym.
Interactions of lead (II) acetate with the enzyme lysozyme: a spectroscopic investigation
J. Lumin.
Superior selective removal of lead via sulfate doped flower like layered double oxide: an example of high value-added utilization of organic waste
J. Clean. Prod.
Distinguished Cr(VI) capture with rapid and superior capability using polydopamine microsphere: behavior and mechanism
J. Hazard. Mater.
Highly effective lead (II) removal by sustainable alkaline activated β-lactoglobulin nanofibrils from whey protein
J. Clean. Prod.
Horseradish peroxidase-catalyzed formation of polydopamine for ultra-sensitive magnetic relaxation sensing of aflatoxin B1
J. Hazard. Mater.
Study of tentacle-like cationic macroporous cellulose spherical adsorbent for heavy metals
J. Clean. Prod.
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