Cytoprotection of Probiotic Lactobacillus acidophilus with Artificial Nanoshells of Nature-Derived Eggshell Membrane Hydrolysates and Coffee Melanoidins in Single-Cell Nanoencapsulation

One-step fabrication method for thin films and shells is developed with nature-derived eggshell membrane hydrolysates (ESMHs) and coffee melanoidins (CMs) that have been discarded as food waste. The nature-derived polymeric materials, ESMHs and CMs, prove highly biocompatible with living cells, and the one-step method enables cytocompatible construction of cell-in-shell nanobiohybrid structures. Nanometric ESMH-CM shells are formed on individual probiotic Lactobacillus acidophilus, without any noticeable decrease in viability, and the ESMH-CM shells effectively protected L. acidophilus in the simulated gastric fluid (SGF). The cytoprotection power is further enhanced by Fe3+-mediated shell augmentation. For example, after 2 h of incubation in SGF, the viability of native L. acidophilus is 30%, whereas nanoencapsulated L. acidophilus, armed with the Fe3+-fortified ESMH-CM shells, show 79% in viability. The simple, time-efficient, and easy-to-process method developed in this work would contribute to many technological developments, including microbial biotherapeutics, as well as waste upcycling.

[1]  S. Li,et al.  Validation of Layer-By-Layer Coating as a Procedure to Enhance Lactobacillus plantarum Survival during In Vitro Digestion, Storage, and Fermentation. , 2023, Journal of agricultural and food chemistry.

[2]  G. Mauriello,et al.  Microencapsulation of Probiotics for Food Functionalization: An Update on Literature Reviews , 2022, Microorganisms.

[3]  J. Sheng,et al.  Enhanced Stability and Function of Probiotic Streptococcus thermophilus with Self-Encapsulation by Increasing the Biosynthesis of Hyaluronan. , 2022, ACS applied materials & interfaces.

[4]  D. Mcclements,et al.  Encapsulation of multiple probiotics, synbiotics, or nutrabiotics for improved health effects: A review. , 2022, Advances in colloid and interface science.

[5]  Juncai Hou,et al.  Novel nano-encapsulated probiotic agents: Encapsulate materials, delivery, and encapsulation systems. , 2022, Journal of controlled release : official journal of the Controlled Release Society.

[6]  G. Mauriello,et al.  Layer-by-Layer Coating of Single-Cell Lacticaseibacillus rhamnosus to Increase Viability Under Simulated Gastrointestinal Conditions and Use in Film Formation , 2022, Frontiers in Microbiology.

[7]  Neel S. Joshi,et al.  A single-cell nanocoating of probiotics for enhanced amelioration of antibiotic-associated diarrhea , 2022, Nature Communications.

[8]  K. Kalantar-zadeh,et al.  Cell‐Mediated Biointerfacial Phenolic Assembly for Probiotic Nano Encapsulation , 2022, Advanced Functional Materials.

[9]  T. K. Goswami,et al.  A Review on Probiotic Microencapsulation and Recent Advances of their Application in Bakery Products , 2022, Food and Bioprocess Technology.

[10]  J. Marchesi,et al.  The potential utility of fecal (or intestinal) microbiota transplantation in controlling infectious diseases , 2022, Gut microbes.

[11]  Hsiu-Wen Chien,et al.  Green sustainable photothermal materials by spent coffee grounds , 2022, Journal of the Taiwan Institute of Chemical Engineers.

[12]  Hsiu-Wen Chien,et al.  Spent coffee grounds as potential green photothermal materials for biofilm elimination , 2022, Journal of Environmental Chemical Engineering.

[13]  Ji Hun Park,et al.  Hydrogen Bonding‐Based Layer‐by‐Layer Assembly of Nature‐Derived Eggshell Membrane Hydrolysates and Coffee Melanoidins in Single‐Cell Nanoencapsulation , 2022, ChemNanoMat.

[14]  Ariel L. Furst,et al.  Protection of Anaerobic Microbes from Processing Stressors Using Metal-Phenolic Networks. , 2021, Journal of the American Chemical Society.

[15]  A. Basit,et al.  Nanoencapsulation for Probiotic Delivery. , 2021, ACS nano.

[16]  I. Choi,et al.  Enzyme-Mediated Kinetic Control of Fe3+-Tannic Acid Complexation for Interface Engineering. , 2021, ACS applied materials & interfaces.

[17]  M. D. del Castillo,et al.  Interest of Coffee Melanoidins as Sustainable Healthier Food Ingredients , 2021, Frontiers in Nutrition.

[18]  H. C. van der Mei,et al.  Interfacial interactions between protective, surface-engineered shells and encapsulated bacteria with different cell surface composition. , 2021, Nanoscale.

[19]  H. C. van der Mei,et al.  Escherichia coli Colonization of Intestinal Epithelial Layers In Vitro in the Presence of Encapsulated Bifidobacterium breve for Its Protection against Gastrointestinal Fluids and Antibiotics , 2021, ACS applied materials & interfaces.

[20]  M. Hoorfar,et al.  Nanomaterial-based encapsulation for controlled gastrointestinal delivery of viable probiotic bacteria , 2021, Nanoscale advances.

[21]  I. Choi,et al.  Iron Gall Ink Revisited: A Surfactant-Free Emulsion Technology for Black Hair-Dyeing Formulation , 2021, Cosmetics.

[22]  Ping Guo,et al.  Synthesis of a Removable Cytoprotective Exoskeleton by Tea Polyphenol Complexes for Living Cell Encapsulation. , 2021, ACS biomaterials science & engineering.

[23]  I. Choi,et al.  Reversed Anionic Hofmeister Effect in Metal-Phenolic-Based Film Formation. , 2020, Langmuir.

[24]  Ji Hun Park,et al.  Single‐Cell Nanoencapsulation of Saccharomyces cerevisiae by Cytocompatible Layer‐by‐Layer Assembly of Eggshell Membrane Hydrolysate and Tannic Acid , 2020, Advanced NanoBiomed Research.

[25]  Juha Song,et al.  Bioinspired cell-in-shell systems in biomedical engineering and beyond: Comparative overview and prospects. , 2020, Biomaterials.

[26]  I. Choi,et al.  Ascorbic acid-mediated reductive disassembly of Fe3+-tannic acid shells in degradable single-cell nanoencapsulation. , 2020, Chemical communications.

[27]  F. Caruso,et al.  Dynamic Electrophoretic Assembly of Metal–Phenolic Films: Accelerated Formation and Cytocompatible Detachment , 2020 .

[28]  Yan Long,et al.  Optimization of staining with SYTO 9/propidium iodide: interplay, kinetics and impact on Brevibacillus brevis. , 2020, BioTechniques.

[29]  I. Choi,et al.  Single‐Cell Nanoencapsulation: From Passive to Active Shells , 2020, Advanced materials.

[30]  Ji Hun Park,et al.  Coffee Melanoidin‐Based Multipurpose Film Formation: Application to Single‐Cell Nanoencapsulation , 2020 .

[31]  Lanjuan Li,et al.  Progress in microencapsulation of probiotics: A review. , 2020, Comprehensive reviews in food science and food safety.

[32]  N. Tzortzakis,et al.  The use of spent coffee grounds in growing media for the production of Brassica seedlings in nurseries , 2020, Environmental Science and Pollution Research.

[33]  Joseph J. Richardson,et al.  The Biomolecular Corona in 2D and Reverse: Patterning Metal–Phenolic Networks on Proteins, Lipids, Nucleic Acids, Polysaccharides, and Fingerprints , 2019, Advanced Functional Materials.

[34]  Ji Hun Park,et al.  Thickness-Tunable Eggshell Membrane Hydrolysate Nanocoating with Enhanced Cytocompatibility and Neurite Outgrowth. , 2019, Langmuir : the ACS journal of surfaces and colloids.

[35]  Hao Wu,et al.  Enhanced viability of layer-by-layer encapsulated Lactobacillus pentosus using chitosan and sodium phytate. , 2019, Food chemistry.

[36]  I. Choi,et al.  Iron Gall Ink Revisited: Natural Formulation for Black Hair-Dyeing , 2019, Cosmetics.

[37]  Joseph J. Richardson,et al.  Tuning the Mechanical Behavior of Metal-Phenolic Networks through Building Block Composition. , 2019, ACS applied materials & interfaces.

[38]  C. McGoverin,et al.  Rapid and cost-effective evaluation of bacterial viability using fluorescence spectroscopy , 2019, Analytical and Bioanalytical Chemistry.

[39]  Bingyun Li,et al.  Biomedical Applications of Layer‐by‐Layer Self‐Assembly for Cell Encapsulation: Current Status and Future Perspectives , 2018, Advanced healthcare materials.

[40]  I. Choi,et al.  Iron Gall Ink Revisited: In Situ Oxidation of Fe(II)–Tannin Complex for Fluidic‐Interface Engineering , 2018, Advanced materials.

[41]  S. Dhara,et al.  Surface Modification of Eggshell Membrane with Electrospun Chitosan/Polycaprolactone Nanofibers for Enhanced Dermal Wound Healing. , 2018, ACS applied bio materials.

[42]  Joseph J. Richardson,et al.  Self-Assembly of Nano- to Macroscopic Metal–Phenolic Materials , 2018, Chemistry of Materials.

[43]  Ji Hun Park,et al.  Strategic Advances in Formation of Cell‐in‐Shell Structures: From Syntheses to Applications , 2018, Advanced materials.

[44]  I. Choi,et al.  Biphasic Supramolecular Self‐Assembly of Ferric Ions and Tannic Acid across Interfaces for Nanofilm Formation , 2017, Advanced materials.

[45]  Jiwei Cui,et al.  Innovation in Layer-by-Layer Assembly. , 2016, Chemical reviews.

[46]  Robert Langer,et al.  Layer‐by‐Layer Encapsulation of Probiotics for Delivery to the Microbiome , 2016, Advanced materials.

[47]  N. Boon,et al.  Reevaluating multicolor flow cytometry to assess microbial viability , 2016, Applied Microbiology and Biotechnology.

[48]  João F Mano,et al.  Coating Strategies Using Layer-by-layer Deposition for Cell Encapsulation. , 2016, Chemistry, an Asian journal.

[49]  Ji Hun Park,et al.  Cell-in-Shell Hybrids: Chemical Nanoencapsulation of Individual Cells. , 2016, Accounts of chemical research.

[50]  Ji Hun Park,et al.  Chemical sporulation and germination: cytoprotective nanocoating of individual mammalian cells with a degradable tannic acid-FeIII complex. , 2015, Nanoscale.

[51]  B. Dave Oomah,et al.  Spent coffee grounds: A review on current research and future prospects , 2015 .

[52]  Ji Hun Park,et al.  A cytoprotective and degradable metal-polyphenol nanoshell for single-cell encapsulation. , 2014, Angewandte Chemie.

[53]  M. Baláž.  Eggshell membrane biomaterial as a platform for applications in materials science. , 2014, Acta biomaterialia.

[54]  Ji Hun Park,et al.  Nanocoating of Single Cells: From Maintenance of Cell Viability to Manipulation of Cellular Activities , 2014, Advanced materials.

[55]  Maneesh K. Gupta,et al.  Biomimetic Coatings to Control Cellular Function through Cell Surface Engineering , 2013 .

[56]  Haeshin Lee,et al.  Chemical control of yeast cell division by cross-linked shells of catechol-grafted polyelectrolyte multilayers. , 2013, Macromolecular rapid communications.

[57]  I. Choi,et al.  Artificial spores: cytoprotective nanoencapsulation of living cells. , 2013, Trends in biotechnology.

[58]  I. Choi,et al.  Artificial spores: cytocompatible encapsulation of individual living cells within thin, tough artificial shells. , 2013, Small.

[59]  M. Coimbra,et al.  Coffee melanoidins: structures, mechanisms of formation and potential health impacts. , 2012, Food & function.

[60]  Y. Lvov,et al.  "Face-lifting" and "make-up" for microorganisms: layer-by-layer polyelectrolyte nanocoating. , 2012, ACS nano.

[61]  A. Raichur,et al.  Enhanced survival of probiotic Lactobacillus acidophilus by encapsulation with nanostructured polyelectrolyte layers through layer-by-layer approach. , 2011, Journal of agricultural and food chemistry.

[62]  Svetlana V. Harbaugh,et al.  Hydrogen-bonded LbL shells for living cell surface engineering , 2011 .

[63]  G. Reid,et al.  Vaginal Microbiota and the Use of Probiotics , 2009, Interdisciplinary perspectives on infectious diseases.

[64]  J. Yang,et al.  Characterization and adsorption properties of eggshells and eggshell membrane. , 2006, Bioresource technology.

[65]  I. Choi,et al.  Cell Surface Engineering , 2014 .