Nanobiohybrids: Materials approaches for bioaugmentation

Abstract

Nanobiohybrids, synthesized by integrating functional nanomaterials with living systems, have emerged as an exciting branch of research at the interface of materials engineering and biological science. Nanobiohybrids use synthetic nanomaterials to impart organisms with emergent properties outside their scope of evolution. Consequently, they endow new or augmented properties that are either innate or exogenous, such as enhanced tolerance against stress, programmed metabolism and proliferation, artificial photosynthesis, or conductivity. Advances in new materials design and processing technologies made it possible to tailor the physicochemical properties of the nanomaterials coupled with the biological systems. To date, many different types of nanomaterials have been integrated with various biological systems from simple biomolecules to complex multicellular organisms. Here, we provide a critical overview of recent developments of nanobiohybrids that enable new or augmented biological functions that show promise in high-tech applications across many disciplines, including energy harvesting, biocatalysis, biosensing, medicine, and robotics.

Fig. 1. Interfacing functional nanomaterials with biological systems for enabling new biological functions or augmenting existing biological functions.

Fig. 2. Materials and synthetic strategies and for biohybrid systems.

(A) Silica coating on cyanobacteria through LbL deposition of PDADMAC and PSS (22). (B) Illustration of single-walled CNT (SWCNT) augmentation (86). (C) SWCNT transport through the chloroplast double membrane envelope (39). (D) Schematics showing different strategies of LbL self-assembly for cell encapsulation (44). (E) Illustration of basic plant physiology and their analogy to electronics (48). (F) Poly(3,4-ethylenedioxythiophene) (PEDOT) infusion into leaves by a syringe (48). (G) Schematic illustration of the biomimetic EV-MOF protein nanoparticles and the intracellular delivery of proteins (78). (H) Schematic illustration of biomimetic crystallization of cytoprotective MOF coatings on living yeast cells (11). (I) Schematic illustration of the MOF monolayer wrapped M. thermoacetica and decomposing of reactive oxygen species (80). (J) Schematic illustration of the MPN shell on individual yeast cells (62). (K) Illustration of MOF formation inside of living plants (15). Reproduced with permissions from the Royal Society of Chemistry (22), American Chemical Society (78, 86) Springer Nature (39), Wiley-VCH (11, 15, 44, 62), National Academy of Sciences (80), and American Association for the Advancement of Science (48).

Fig. 3. Materials approaches and applications for bioaugmentation.

Fig. 4. Synthesis and performance of biomacromolecule-based nanobiohybrids.

(A) Schematic of CaP coating on the mutant viral protein and in vitro tests of virus thermostability. Thermal inactivation kinetics were determined at 26° and 37°C (91). PFU, plaque-forming units. (B) catalase (CAT) and superoxide dismutase (SOD) insertion into FNPCN-333 and the relative enzymatic activities of several SOD formulations. The fluorescence cell images showing the internalized FNPCN-333 particles in living cells. (C) Schematic diagram showing the new coordination bond formed between the carboxylate groups from catalase and Zn in ZIF-L. Retention of the biocatalytic efficiency of catalase@ZIF-L with different treatments (74). (D) Illustration of intracellular delivery of single-stranded DNA (ssDNA) with and without MOF as vectors. Comparison of the intracellular delivery efficiency of ssDNA with and without MOFs using MCF-7 human breast cancer cells (93). cDNA, complementary DNA; DAPI, 4′,6-diamidino-2-phenylindole; FAM, 6-carboxyfluorescein. (E) Schematic of reversible MOF coating on antibody-functionalized DNA nanoparticles. Graph shows the retained recognition capability of MOF-coated biosensors on glass substrates stored at room temperature (RT), 40°, and 60°C for different durations and the retained recognition capability of the MOF-coated biosensor stored at room temperature for 3 days (94). (F) Microscopy images showing the stability of a bare proteinosome and MPN-protected proteinosome (14). (G) Schematic representation of the microfluidic device used to encapsulate individual exosomes. A generic term, EV, was used for all secreted vesicles including exosomes and microvesicles (97). (H) Schematic of the approach for wrapping a virus in a metal-organic molecular net with two-step preparation and evaporation of water that leaves the virus partially hydrated for further analysis in vacuum or air (98). Reproduced with permissions from the National Academy of Sciences (91), Springer Nature (87, 93), Elsevier (74), Wiley-VCH (94, 97), and the Royal Society of Chemistry (14, 98).

Fig. 5. Synthesis and performance of cell-based nanobiohybrids.

(A) Schematic of polydopamine encapsulation and surface functionalization of individual yeast cells and the transmission electron microscopy micrograph of microtome-sliced hybrid cells. Reproduced with permission (9). (B) Schematic of modification of the cell surface using chain-transfer agent (CTA) lipids and subsequent cell surface–initiated polymerization and the cell viability after polymerization. Reproduced with permission (18). (C) Schematic of coating scheme for aminated beads and islet cell clusters and the multisliced projection confocal images of coated islets 48 hours after coating (12). Cluster diameter is of order 150 μm. NHS, N-hydroxysuccinimide. (D) Schematic showing the preparation of zona pellucida–like nanobiohybrid stem cells for implantation in the uterus wall (104). Reproduced with permissions from the American Chemical Society (9), Springer Nature (18, 104), and Wiley-VCH (12).

Fig. 6. Synthesis and performance of advanced nanobionics.

(A) Schematic illustration of the construction of bionic cells by interfacing bioactive MOF coatings with yeast cells. Reproduced with permission (79). (B) Schematic illustration of the artificial jellyfish construction and 2D muscle architecture (111). (C) Schematic illustration of the injectable photoreceptor-binding upconversion nanoparticles (UCNPs) in mouse (114). (D) Schematic illustration of nanoparticles in a leaf and an image of the light-emitting plants (13). (E) Illustration of the synthesis procedure of morph-TiO₂ from green leaf biotemplates (115). (F) Comparison of natural and artificial leaves from their structures and functions (116). Reproduced with permissions from Wiley-VCH (79, 115, 116), Springer Nature (111), Elsevier (114), and American Chemical Society (13).