Nano‐Biohybrids: In Vivo Synthesis of Metal–Organic Frameworks inside Living Plants

Abstract

Plants have a complex passive fluid transport system capable of internalizing small molecules from the environment, and this system offers an ideal route for augmenting plants with functional nanomaterials. Current plant augmentation techniques use pre-formed nanomaterials and permeabilizing agents or plant cuttings. A so far unexplored concept is the formation of the functional material, in situ, from precursors small enough to be passively internalized through the roots without harming the plants. Metal-organic frameworks are ideal for in situ synthesis as they are composed of metal ions coordinated with organic ligands and have recently been mineralized around single-celled organisms in mild aqueous conditions. Herein, the synthesis of two types of metal-organic frameworks, zinc(2-methylimidazole) and lanthanide (terephthalate) , are reported inside a variety of plants. In situ synchrotron experiments help elucidate the formation kinetics and crystal phases of the nano-biohybrid plants. Plants augmented with luminescent metal-organic frameworks are utilized for small molecule sensing, although other applications, such as pathogen sensing, proton conductive plants, improved CO capture, bacteria-free nitrogen fixation, drought and fungi-resistance, and enhanced photosynthesis and photocatalysis, are foreseeable. Overall, the generation of functional materials inside of fully intact plants could lead to more complex nano-biohybrid sensors and organisms augmented with superior performance characteristics.

Nanobiohybrids: Materials approaches for bioaugmentation

“…(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).…”

“…on July 4, 2020 http://advances.sciencemag.org/ Downloaded from was presynthesized and wrapped spontaneously around the newly grown cell surface through coordination bonds between the zirconium cluster and teichoic acid. In terms of multicellular-scale augmentation, Richardson and Liang reported the growth of ZIF-8 (and its derivative) and Eu and Tb 2 (bdc) 3 inside and outside living plants (15). Using intact plant and plant clippings, they showed that aqueous solutions containing the MOF precursors can be taken up into the xylem through the plant's active liquid uptake mechanism, where the rich polysaccharide-containing plant linings could induce the rapid MOF nucleation and growth in situ both inside and outside of the plants (15).…”

“…In terms of multicellular-scale augmentation, Richardson and Liang reported the growth of ZIF-8 (and its derivative) and Eu and Tb 2 (bdc) 3 inside and outside living plants (15). Using intact plant and plant clippings, they showed that aqueous solutions containing the MOF precursors can be taken up into the xylem through the plant's active liquid uptake mechanism, where the rich polysaccharide-containing plant linings could induce the rapid MOF nucleation and growth in situ both inside and outside of the plants (15). So far, only a few MOFs have been incorporated with living cells, which contrasts with the extensive work performed on traditional biomineralization routes such as calcium phosphate, calcium carbonate, silica, gold, or graphene coatings (29,37), and it is expected that new MOFs will be studied to greatly expand their integration with biological systems.…”

“…We recently showed that the in situ formation of MOFs inside living plants can be achieved without affecting the plant's viability, which turned the plant into a living chemical sensor ( Fig. 2K) (15). Taking advantage of the rapid liquid transport mechanism of living plants, aqueous solutions containing the metal ions and organic linkers could be easily transported inside the xylem from the root of the plant through the cohesive and adhesive forces.…”

“…Notable effort in the past decade has been devoted to the design of nanobiohybrid systems, which broadly encompasses composite materials that have both a biologically derived component and a synthetic component. The biological component can be anything from purified biomolecules (14) (e.g., DNA and proteins) to complex biological systems (11,15) (e.g., living cells, tissues, and organisms), while the synthetic component can be inorganic materials (16,17) (e.g., carbon materials, CaCO 3 , SiO 2 , Au, and iron oxide), organic materials (18,19) (e.g., polymers and lipids), or hybrid materials (14,20) [e.g., metal-organic frameworks (MOFs) and metal-phenolic networks (MPNs)]. In these nanobiohybrid systems, the choice of both biological and synthetic components has an impact on different aspects of the final biofunctionality ( Fig.…”