Surface engineering of microbial cells: Strategies and applications

Sabella Jelimo Kiprono^{1, 2, 3, #} , Muhammad Wajid Ullah ^{1, 2, #}  and Guang Yang ^{1, 2, *}

¹ Department of Biomedical Engineering, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan 430074, PR China

² National Engineering Research Centre for Nano-Medicine, Huazhong University of Science and Technology, Wuhan 430074, China

³ Department of Medical Laboratory Sciences, Masinde Muliro University of Science and Technology, 190-50100, Kakamega, Kenya

* Corresponding Author(E-mail) : yang_sunny@yahoo.com

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Abstract

Microbial cells (bacteria, fungi, and algae) and viruses are important part of life; which besides their harmful effects, perform several useful functions owing to their unique cell surface properties. The unique structures present on their surfaces serve as barriers between the cell and its environment and bestow them with unique functional properties. The current review describes strategies to decorate microbial cells by using different materials. It details various strategies such as layer by layer (LbL) decoration, mineralization, encapsulation, and genetic engineering among others to modify the surfaces of different microbial cells for potential applications such as environmental biotechnology, toxicology, medical microbiology, and nano-biotechnology, etc. Besides, it discusses the effects of various materials on cell viability, physiology, and functionality used for surface engineering.  This review provides fundamentals to the novice readers and insights to the seasoned researchers to pave way for their future research in the area.

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Table of Content

The current review describes strategies to decorate microbial cells by using different materials.

 

 

 

Keywords

Microbial cell         Surface properties         Cell surface modification         Applications

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1. Introduction

Biomineralization is a biological process used for the formation of protective structures around different microscopic single-cell organisms like diatoms algae and foraminifers. These microorganisms possess inorganic shells on their surfaces which are made of calcium carbonate and silica and potentially serve as a boundary between the cell and its environment. However, most of the microorganisms lack such structures that necessitates the introduction of artificial biomimetic shells on their surfaces.¹ The process of introducing minerals or macromolecules helps in the modification of microbial cell surface thereby imparting specialized functions to them. This is achieved by using two main biological strategies: functional integration and biomimetic approach for modification of living cells.² Entrapping  live cells inside a polymer layer at a micrometer scale where the polymer coating restricts the cell movement within the microsphere and offer protection against the varying microenvironment (pH, temperature, ionic strength, etc.) is a strategy that has been broadly applied in recent years.^3,4 The pores, present in most cases in the encapsulating layer, allow the diffusion of nutrients, oxygen, wastes, and electrolytes to move across the barrier, thus, maintaining cell growth.⁵ Cells can also be coated with magnetic nanoparticles that allow effective spatial manipulation by application of magnetic fields. This property helps to improve control over size distribution, cell distribution and geometry within multicellular constructs, thus, giving way in tissue engineering which is a potential application in advanced regenerative medicine and many other fields.⁶ Polymer and nanoparticle coating of cells have been done on cells from different origin ¹. The mostly studied eukaryotic organism is the yeast cell because of its cell wall characteristics that provide cell resistance.⁷ Bacterial cells have also been decorated with polymers and magnetic nanoparticles to obtain functionalized cells.^8–10 Viruses on their surface lack the negative charge so they have been engineered with different minerals and nanoparticles.¹¹

To date, a variety of strategies have been developed for the surface modification of microbial cells such as layer by layer (LbL) decoration,¹² mineralization,¹³ encapsulation¹⁴ and genetic engineering¹⁵ among others. For example, the LbL strategy is used to achieve magnetized functionalized cells by depositing magnetic (Fe₃O₄) nanoparticles onto the cell surface using different polymers as mediators for the immobilization of colloidal nanoparticles. The simplicity and versatility of the LbL assembly technique paves the way for extensive applications due to the production of hybrid nanostructures with promising collective and improved functional properties.¹⁶ However, the different techniques used for surface modification of microbial cells differ in their degree of biocompatibility, sensitivity, types of materials, and effect on the viability of target microorganisms. Thus, there is an extensive need for developing more compatible strategies to deposit a variety of materials for the fabrication of broad-spectrum functionalized microbial cells.¹⁷ To date, materials of different nature such as natural and synthetic polymers, organic, inorganic, and magnetic nanoparticles, polyelectrolytes, gene and DNA, etc. have been used for the surface modification of microbial cells. The polymer and nanoparticles–based fabrication of microbial cells has been achieved for a variety of microbial cells owing to their potential applications in different fields such as biotechnology and biomedicine.¹

Despite the greater potential of microbial cells to be surface-modified and availability of various materials used for their modification, the coating of living cells with certain types of nanoparticles, polymeric– and non-polymeric, and polyelectrolytes tend to have toxic effects towards their viability. Therefore, any microencapsulation strategy used for surface modification should ensure the viability of coated cells against any harmful effects of the materials used as well as environmental factors such as varying pH, ionic strength, temperature, metabolites, and osmotic stress, etc. Further, it should enhance the storage stability of the encapsulated cells. In line with cell viability, important considerations include the integrity of cell membrane, cell division, and intracellular enzymes of the functionalized cell.¹⁸ Recent interests of cell-surface modification by using various polymer nanofilms, hydrogels, minerals, and sol-gel shells, etc. have resulted in developments in several fields such as their applications in whole-cell biosensors^19,20 toxicity microscreening devices¹⁷ and catalysts,²¹ tissue engineering,²² and bioanalytical chemistry.²³

The use of inorganic micro-shells of different varieties for biomimetic encapsulation of microbial cells has been the recent area of research whose target is mainly yeast, human normal and cancerous cell lines, and bacteria, etc. for diverse applications.¹⁸ Biofabrication of microbes has provided an insight for wide range of applications such as micro devices, bio-nanomaterials and micro/nanorobots due to their different shapes and sizes.²⁴ Therefore, this review is aimed to overview the current progress of surface engineering of a variety of microbial cells through different strategies for various applications. Emphasis has been laid on several microbes that can be potentially modified by using compatible materials. Further, various strategies employed to encapsulate different types of live microbial cells by creating an artificial shell around them have been described along with their potential merits and limitations. In addition, it addresses the effect of microbial encapsulation towards the viability of target cells to pave the way to future developments of the cell surface engineering strategies. Several important applications of surface modified microbial cells in different fields such as biomedical, pharmaceutics, environment, and industry, etc have been enumerated in detailed. Besides, this review provides a base for the development of new modification strategies, selection of appropriate materials and microbial cell types, and development of novel materials which can find potential applications in different fields.

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2.  Surface modification strategies 

2.1 Layer by layer technique  

Layer by layer (LbL) is the most commonly used technique for encapsulation of microbial cells and is illustrated in Fig. 1. It involves multilayer coatings formation by exposing the cells to polyelectrolytes by alternating the charges existing of an acidic and basic component. The living cells are mainly used as functional elements of polyelectrolyte such as attachment of multilayers to the surface of the cells and the incorporation of polyelectrolyte into multilayers.¹² This strategy involves formation of thin films and has received immense consideration owing to its wide choice of materials that can be used for coating particulate substrates and due to its ability to modulate nanometer control over film thickness. This fabrication technique has led to rise of functional and responsive thin films which have found potential applications in a various fields such as but not limited to bioelectronics, energy storage and conversion, drug delivery, and catalysis, etc..¹⁶

The LbL technique is a low-cost, simple, and possesses wall properties, such as texture or thickness and permeability. These properties can be controlled to a nanometer scale during the layer by modulating the ionic strength, pH or counteracting ions.²⁵ Briefly, the first layer deposited onto the cell is composed of a polycation (cells mainly possess the negative charge in water), the second layer deposited is comprised of a polyanion. This layer is repeated until the required bilayers are obtained. Washing is done after every layer has been deposited so as to remove the traces of polymers used and finally centrifugation is carried out.¹⁸ Several studies have reported about the application of LbL strategy to encapsulate microbial cells. For instance, Fakhrullin and Minullina demonstrated the LbL to encapsulate yeast cells into artificial inorganic shells of calcium carbonate (CaCO₃). Capsules of CaCO₃ were formed because of precipitation of Ca²⁺ and CO₃^2- ions onto the cell surfaces in aqueous solutions for several minutes. The resulting two component hybrid structures of cells and inorganic shells are formed, referred to as “core shell particles,” where the inorganic layer is 1–2 µm thick.²⁶

Fig. 1 Illustration of (A) layer by layer strategy and (B) single layer step of polycation stabilized with nanoparticles on the surface bacterial cell.

2.2 Genetic engineering

As stated earlier, viral engineering methods like genetic recombination, PEGylation, and covalent modulations have become disadvantageous owing to their irreversibility that can easily affect several processes like viral production, infection, and the transduction processes.^27,28 Fabrication strategies such as genetic engineering are more advantageous compared to the previously reported strategies. Genetic engineering involves the transformation of coat proteins by inserting amino acids which act as ligation handles for introducing peptide-based affinity tags, bio-conjugation, and to insert peptides as epitopes or targeting ligands in order to provoke the immune response.²⁹ The changes lead to the insertion or exchange of individual amino acids to introduce side chains that allow functionalization, terminal extensions (adding sequences to C-terminus or N-terminus of each coat protein), or insertion of sequences that form surface loops^30,31 or to alter the overall physicochemical properties of VNP.³² Examples of modifications include the introduction of targeting sequences that allow VNP to target-specific receptors, introduction of immunodetection tags/purification, and introduction of epitope sequences for functioning of VNP as a vaccine.^33,34 The genetic material is located in the single-stranded or double-stranded fragments or in the interior of the capsid as circular. Enveloped viruses consists of a bi-lipid layer on the exterior which provides targeting specificity to the virus.³⁵ The addition of unnatural amino acids as unique handles for subsequent chemical reactions is also possible using similar recombinant expression techniques.³⁶

2.3 Encapsulation

Virus coat proteins self-assemble around the nucleic acids under physiological conditions, and this property, shared by the viral nanoparticles (VNPs), can be exploited to reassemble and disassemble them into more desirable structures around other cargo molecules.¹⁴ At present, two different strategies are used to trigger the cargo encapsulation; (a) unique binding interactions that occur during self-assembly, and (b) electrostatic interactions and surface charge. For efficient encapsulation process of the foreign cargo, self-assembly of viral coat proteins around a negatively charged nucleic acid is warrant.¹⁴ In viral encapsulation, the size of the cargo is the main key factor due to different sizes and its radius of curvature, which could lead to the morphological and physical characteristics of the capsid to be altered.³⁷

2.4  Biomineralization

The deposition process of minerals around and in the cells and tissues of living organisms to accumulate and assemble is known as biomineralization. In viral nanoparticles (VNPs), this process involves the capability of virus coat proteins to nucleate mineralization or assemble around a mineral core.¹³ The biotemplate, that is a VNP, is exposed to other inorganic precursors or metallic, resulting in the nucleation of material on the internal or external surface due to the capsid amino acids interactions.¹³

A study by Pouget and Grelet described a novel mineralization process of a filamentous virus by stabilizing the virus surface with polyethylene glycol (PEG) covalently, followed by mineralization on the surface by use of silica and with titanium dioxide (TiO₂) to achieve high quantity of the mineralized rods. The results showed aggregation of 1-2 nm nanoparticles on the virus surface forming an incomplete non-homogeneous mineral layer. However, the mean thickness of coated mineral layer was constant on the whole length surface of the virus ¹¹. These three startegies have been summarized in Fig. 2.

Fig. 2 Illustration of techniques used for surface modification of different types of viruses.

3. Surface modification of microbial cells

The variability of live microbial cells in their sizes, morphologies, physiological properties, and biochemical activities give the possible ways to use them as objects to deposit different functional nanomaterials onto the their surface.¹ Several living microorganisms of different kinds, including magnetotatic bacteria, yeast, and viruses hardly makes their own shells, and hence been widely utilized by various researchers in nano modification by biomineralization which demonstrate their suitability by retaining their viability.² The following sections describe the surface modification of various types of microbial cells by different strategies:

3.1  Yeast

Yeast, Saccharomyces cerevisiae, is an important microorganism for understanding eukaryotic biology at the cellular and molecular levels. Its cell wall is composed of chemical compounds, including weak negatively charged polysaccharides, N-acetyl glucosamine, and mannose and rarely contains any minerals on its surface which limits its surface modification.⁷ Therefore, the deposition of positively charged polyelectrolytes on its surface will enable its biomineralization. This deposition of positively charged groups on surface of yeast cell wall serves as a link between the cell and deposited polyelectrolytes. For example, Yang et al. encapsulated the living yeast cells by forming silica shells in the presence of poly (diallyldimethylammonium chloride) (PDADMAC) and poly (styrene sulfonate) (PSS). This strategy was based on the preliminary modification of the cell surface by use of the LbL technique to form a multilayered film of PDADMAC/PSS and make the surface of the cell to act as a positive potential. The surface-modified cells were then placed in silicic acid which triggered the formation of a 50 nm thick layer of silica shell on the cell surface.³⁸ A similar technique was used by Wang et al. to form calcium phosphate micro shells by depositing PDADMAC/PSS/CaCl₂/Na₂HPO₄ on the surface of yeast cell wall.³⁹

Fig. 3 Schematic representation of (A) the process of coating the microbial cell surface with the hydrogel, (B) biomimetic mineralization technique, and (C) testing of magnetic properties of the modified microbial cells. The figure has been modified from ²¹. Copyright@2016, John Wiley and Sons.

Table 1. Microbial cell encapsulation and overview of the technique, coating substances used and general description of characteristics information obtained.

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4. Effects of microbial surface modification

5.1 Cell delivery

5.1.1 Hypocholesterolaemic effect

Two probiotic strains of Lactobacillus plantarum, Lp91 and Lp21, which produce bile salt hydrolase (Bsh), were evaluated on in Sprague–Dawley rats for high plasma cholesterol level that is the real cause of hypercholesterolaemia in humans. The probiotic bacterial cells were microencapsulated in sodium alginate matrix. Hypercholesterolaemic diet (HD) with L. plantarumLp91 (HD91), a HD with microencapsulated L. plantarum Lp91 (HDCap91) and a HD with L. plantarum Lp21 (HD21) were tested for cholesterol reduction effect. The total cholesterol reduction after 21 days was 23.26, 15.71, and 15.01%, and taurodeoxycholic acid (TGA) reduction was 21.09, 18.77, and 18·17 % and finally 38.13, 23.22, and 21.42 % reduction in LDL-cholesterol. The study showed that Bsh active L. plantarum strains have the potential to be used in treatment of hypercholesterolaemia in patients since it was able to demonstrate reduction in plasma total cholesterol and LDL-cholesterol in rats fed with a diet high in cholesterol.⁷⁴

5.1.2  Uremic therapy

A study by Lin et al., 2008 used Escherichia coli DH5α, a genetically modified strain encoded with urease gene, as a model for in vivo and in vitro studies to assess the alginate-chitosan-alginate (ACA) microcapsules as a potential functionalized cell for oral therapy of uremia. In the ACA microcapsules containing E. coli, the urea concentration in the simulated culture medium was significantly reduced from 429.20 mg/L to 37.06 mg/L in 2 h, and was undetectable after 4 h. The urea removal was accomplished better by free cells compared to bacteria encapsulated within the ACA or alginate-polylysine-alginate (APA) shells, which may be attributed to the easy diffusion of the urea molecule through the cell compared to the immobilized cells. It was concluded that the ACA microcapsule membrane possesses superior mechanical and chemical stability in the simulated gastrointestinal conditions. In vivo experiments demonstrated that the ACA microcapsule is more stable than the APA microcapsule, because of increased resistance to gastrointestinal (GIT) enzymatic degradation. Therefore, it is anticipated that ACA microcapsules could allow safer and more effective oral delivery of live bacterial cell for various clinical applications.⁷⁵

5.1.3  Renal failure treatment

Prakash et al. were the first to study the microencapsulated yeast cells, Saccharomyces cerevisiae in renal failure. Live yeast cells were encapsulated in alginate-polylysine-alginate (APA) microcapsules and orally administered to uremic rat model. It was found that microencapsulated yeast cells were retained in the microcapsules through gastro-intestinal tract transit, however, it allowed urea to diffuse through the semi-permeable membrane of the microcapsule and were acted upon by yeast urease. There was 18% decrease of the urea levels during 8 week treatment period, thus, demonstrated to be a therapeutic method for eliminating the elevated levels of metabolites in renal failure. Plasma urea level rapidly returned to uremic level when administration of APA encapsulated yeast was terminated. They, therefore, concluded that the encapsulated yeast cells did not remain in the intestinal tract rather it was removed in the stool.⁴⁷

5.1.4  Colon Diseases treatment

Recently, microencapsulation of probiotic cells has been vastly studied and being identified for the treatment of various gastrointestinal and other health condition. Their delivery has been enhanced by microencapsulation which offers protection against harsh conditions of the upper gastro intestinal tract (GIT).⁷³ The effect of the probiotic microencapsulation on therapy of neonatal calf-under field conditions was investigated using Enterobacterial Repetitive Intergenic Consensus-Polymerase Chain Reaction (ERIC-PCR) methods. The analysis of ERIC-PCR fingerprints showed that the administration of microencapsulated Lactobacillus brevis had a strong beneficial effect on the replacement of the intestinal microflora of diarrhea calves. ERIC-PCR profiles of fecal samples from the diarrhea calves were different from that of control health calves. Diarrhea calves who were administered with probiotic capsules showed ERIC-PCR profiles similar to that of healthy calves. These findings demonstrated a positive signal for using probiotics capsules to treat neonatal calf diarrhea ⁷⁶.  Several other studies have investigated the ability of APA microencapsulated L. acidophilus to suppress intestinal inflammation in mice, hence becoming one of the potential application in chronic inflammatory gut diseases such as inflammatory bowel syndrome and inflammatory bowel disease. A study showed that the cytokine level were lowered when microencapsulated cells were administered which enhanced the markers linked to colonic epithelial cell survival.⁷⁷

5.1.5  Drug delivery vehicles (Viral Nanoparticles)

The invention of Viral Nanoparticles (VPNs) targeting specific cell types by loading toxic substances through encapsulation, infusion, and/or conjugation to eliminate them enhanced the removal of diseased cells or cancer cells without any effect on the non-targeted cell. The toxic cargos are always loaded into the VNP cavity to preserve them from chemical and enzymatic degradation and to prevent them from interacting with the healthy cells.⁸³ It is presumed that up to 300 doxorubicin molecules can be conjugated to the capsid surface of cowpea mosaic virus (CPMV).⁵⁷ Some studies have reported the designing of VNPs for in vitro toxicity for drug delivery and the clinical trials demonstrated the in vivo efficacy reduced cardio toxicity of a doxorubicin-loaded VNPs; specifically the cucumber mosaic virus (CMV) modified with folic acid to target the ovarian cancer.⁵⁶

5.2  Pharmaceutical industry

5.2.1 Toxicology screening

The use of magnetically modified yeast cells in microfluidic biosensor systems have been studied as the most cost effective method for industrial scale application for screening toxicity of various substances. A short communication study by Alonso et al. exposed the magnetically-PAH stabilized GFP reporter yeast to a genotoxic chemical (methyl methane sulfonate) and monitor the genotoxicity of the chemical to the cells within a microfluidic device. Gradient mixing was done to ensure simultaneous exposure of functionalized yeast to a various concentrations of toxins in order to measure effectively the emitted fluorescence from GFP. The magnetic modification on the cells ensured that the yeast cells were retained within the device. The rapid toxicity screening of a various range of chemicals and convenience was enhanced by their facile subsequent reloading and removal.^17,71

5.3  Industry Applications

5.3.1 Food industry

In food industry, microbial cell or enzyme immobilization is mostly carried out through entrapment or encapsulation.^3,4 The process entails entrapping or coating the living cells inside a polymeric substance in order to obtain beads which are able to permit gases, metabolites, and nutrients within the cell to maintain cell viability.^52,84 This encapsulation strategy leads to the entrapment of the cells within a micro (within size range of 1–1000 µm) and macro (within size range of a few millimeters to a few centimeters) polymeric beads.^52,85 High rate of fermentation for beer production was observed when brewing yeast was encapsulated in alginate/chitosan polymers in matrix with a liquid core as compared to when it was done in free cell system. The high rate of ethanol production and yeast growth was attributed to the encapsulation technique protecting the cells from product and substrate inhibition.⁷⁸ Use of encapsulated S. cerevisiae AXAZ-1 cells in a multi-stage fixed bed tower bioreactor that has a capacity of 5000–10,000 L for wine production, lead to good operation stability even at a wide range of temperature. Time to complete fermentation with the immobilized yeast ranged from 290 h at 5 °C and 120 h at 40 °C to 25 h at 33 °C. The daily ethanol productivity reached maximum (88.6 g/l) and minimum (5.6 g/l) levels at 33 °C and 5 °C, respectively. Free cells were unable to ferment at temperatures greater than 35 °C, in contrast to immobilized yeast.⁷⁹

5.4 Environmental microbiology

5.4.1 Biodegradation

Phenol is one of the commonly used chemicals in various industries although it is hazardous to human health when released directly to the environment. Hence, there is a need to develop a method to reduce its concentration to safe levels and release the wastewater that has low phenol from industries to stream water. Several researchers have developed physical, chemical, and biological treatment methods to remove phenol from industrial water.^86–89 Immobilization of cells and cell suspension are two commonly used strategies for biological treatment of water.²⁷

For instance, in a study, the bacterium P. putida was immobilized in sodium alginate beads in order to evaluate the degradation of phenol of different concentrations.⁸⁰  A low phenol concentration between 50–500 mgL^-1 leads to higher biodegradation by both immobilized and suspended cells. However, an increased concentration above 500 mgL^-1 leads to decreased biodegradation of phenol by the suspended cells as compared to immobilized cells which showed to smaller extent decrease in biodegradation rate. In conclusion, the TiO₂ immobilized cells showed a higher rate of biodegradation.

5.4.2 Bioremediation

Bioremediation uses biological organisms to assist in the removal of hazardous substances from polluted area. When compared to the planktonic bacteria, the immobilized bacteria also shield perturbations of environmental conditions, like the toxic compounds.⁹⁰ Zhang et al. used three strains chromosomally encoded bioreporters of Acinetobacter baylyi ADP1 to obtain magnetic function by stabilizing the cells with poly (allylamine hydrochloride) and magnetic nanoparticles (PAAH-MNPs). Genetic engineering was done to the cells in order to produce bioluminescence in the presence of toluene/xylene, alkanes and salicylate. The Acinetobacter bioreporters cells were reported to have higher efficiency of magnetic nanoparticles functionalization of about 99.96 ± 0.01%.  Moreover, the magnetic modified bioreporters were able to detect salicylate when applied to garden soils and sediments which were detected by measuring the bioluminescence and they were able to be recovered by use of a permanent magnet, thus, serving as a promising tool for cleaning of contaminated soil.⁹

5.4.3  Biosorbents and catalysts

Microorganisms, either unicellular or multicellular, can interact with a variety of nanoparticles without interference of their viability to provide several potential applications.^91,92 For example, the magnetic modified microbial cells can find potential applications as cell biocatalysts and adsorbents of several types of organic and inorganic xenobiotics.^93,94 Ethylenediaminetetraacetic dianhydride (EDTAD) with magnetic nanoparticles (Fe₃O₄) was used to modify baker's yeast biomass to form a functionalized S. cerevisiae. The functionalized yeast cell obtained acted as a biosorbent for removal of heavy metals such as Cadmium (Cd ²⁺) and Lead (Pb²⁺). A higher adsorption rate of 40.72 mg/g for Cd²⁺and 88.16 mg/g Pb²⁺ was observed at pH 6.0 and 5.5, respectively.⁸¹ Similarly, biomass yeast cell was modified with ethylenediamine and doped with magnetic chitosan microparticles for the adsorption application of lead metal ions. Increase in pH leads to higher adsorption of lead ions and the highest adsorption rate was observed at pH 4.0-6.0.⁸²

6. Conclusion and future prospects

Surface engineering of microbial cells is a promising fabrication technique in industry, pharmaceutical, biomedical, and environmental sectors with promising applications. It is a simple, efficient, and cost-effective process that offers modification of a wide range of microbes for a wide range of applications. Recently, the surface modification processes have resulted in increased viability of microbes by the use of nontoxic polymers to encapsulate the cells, thus the development of different varieties of surface engineered organisms for different purposes. However, the selection of appropriate technique, polymers, and human beneficial microbial cells could help to extend the applications of this engineering process to other fields like advanced delivery of beneficial components to the human body. It is conceivable that this field with further advancements, will find major breakthroughs in the near future.

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Conflict of interest

The authors declare that they have no conflict of interest.

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Acknowledgement

This work was supported by National Natural Science Foundation of China (21574050, 21774039, 51603079), China Postdoctoral Science Foundation (2016M602291), Fundamental Research Funds for the Central Universities, Open Research Fund of State Key Laboratory of Polymer Physics and Chemistry, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences.

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