Solid-State NMR Investigations of Extracellular Matrixes and Cell Walls of Algae, Bacteria, Fungi, and Plants

Abstract

Extracellular matrixes (ECMs), such as the cell walls and biofilms, are important for supporting cell integrity and function and regulating intercellular communication. These biomaterials are also of significant interest to the production of biofuels and the development of antimicrobial treatment. Solid-state nuclear magnetic resonance (ssNMR) and magic-angle spinning-dynamic nuclear polarization (MAS-DNP) are uniquely powerful for understanding the conformational structure, dynamical characteristics, and supramolecular assemblies of carbohydrates and other biomolecules in ECMs. This review highlights the recent high-resolution investigations of intact ECMs and native cells in many organisms spanning across plants, bacteria, fungi, and algae. We spotlight the structural principles identified in ECMs, discuss the current technical limitation and underexplored biochemical topics, and point out the promising opportunities enabled by the recent advances of the rapidly evolving ssNMR technology.

Modern Biophysics Redefines Our Understanding of Fungal Cell Wall Structure, Complexity, and Dynamics

“…The advantage of the ssNMR approach is that the cell wall is analyzed without any chemical perturbation; therefore, the physical and structural status of the cell wall is in its native configuration ( 19 ). ssNMR enables the detection of rigid and mobile molecules as defined by their native dynamics in the cell wall with no dependence on covalent linkage patterns or their susceptibility to chemical extraction.…”

Solid-state NMR analysis of unlabeled fungal cell walls from Aspergillus and Candida species

“…Solid-state NMR (ss NMR) spectroscopy is a non-destructive and high-resolution method for elucidating the structure of fungal biopolymers ( Ghassemi, 2022 ). This method has been extensively employed to track melanization in Cryptococcus neoformans and other fungi ( Zhong et al, 2008 , Chatterjee et al, 2015 , Chrissian, 2020 ).…”

Structure of In Vitro-Synthesized Cellulose Fibrils Viewed by Cryo-Electron Tomography and 13C Natural-Abundance Dynamic Nuclear Polarization Solid-State NMR

“…Recently, multidimensional solid-state NMR techniques have shown their capability of revealing the molecular structure of cellulose and its interactions with other biopolymers (such as hemicellulose, pectin, and lignin) in native plant cell walls and carbohydrate-based materials. − By coupling 13 C labeling of samples and high-field NMR, seven types of glucose units were consistently identified in the CMFs across the cell walls of a variety of plant genera, including Arabidopsis, Brachypodium, maize, rice, switchgrass, poplar, eucalyptus, and spruce. − None of these glucose units follow the 13 C chemical shifts of the bulk allomorphs, Iα and Iβ structures, revealing a substantially deviated structure of cellulose when placed in the native context. However, the expected signals of Iα and Iβ allomorphs have been recently observed in cotton, indicating that model crystal structures are only possible in highly crystalline cellulose with large crystallites .…”