Bacterial extracellular electron transfer: a powerful route to the green biosynthesis of inorganic nanomaterials for multifunctional applications

Abstract

Synthesis of inorganic nanomaterials such as metal nanoparticles (MNPs) using various biological entities as smart nanofactories has emerged as one of the foremost scientific endeavors in recent years. The biosynthesis process is environmentally friendly, cost-effective and easy to be scaled up, and can also bring neat features to products such as high dispersity and biocompatibility. However, the biomanufacturing of inorganic nanomaterials is still at the trial-and-error stage due to the lack of understanding for underlying mechanism. Dissimilatory metal reduction bacteria, especially Shewanella and Geobacter species, possess peculiar extracellular electron transfer (EET) features, through which the bacteria can pump electrons out of their cells to drive extracellular reduction reactions, and have thus exhibited distinct advantages in controllable and tailorable fabrication of inorganic nanomaterials including MNPs and graphene. Our aim is to present a critical review of recent state-of-the-art advances in inorganic biosynthesis methodologies based on bacterial EET using Shewanella and Geobacter species as typical strains. We begin with a brief introduction about bacterial EET mechanism, followed by reviewing key examples from literatures that exemplify the powerful activities of EET-enabled biosynthesis routes towards the production of a series of inorganic nanomaterials and place a special emphasis on rationally tailoring the structures and properties of products through the fine control of EET pathways. The application prospects of biogenic nanomaterials are then highlighted in multiple fields of (bio-) energy conversion, remediation of organic pollutants and toxic metals, and biomedicine. A summary and outlook are given with discussion on challenges of bio-manufacturing with well-defined controllability.

Electrogenic Bacteria Promise New Opportunities for Powering, Sensing, and Synthesizing

“…Many bacterial species are capable of biosynthesizing nanoparticles by reducing metal ions through their enzyme and protein components. [149,150] This activity can be essential for their fundamental metabolism or survival in toxic metallic environments. Compared to conventional chemical synthetic methods, biosynthetic routes using microorganisms have emerged as an environmental-friendly, simple, biocompatible, and cost-effective "Green Chemistry."…”

“…[143,144,149,150] The biosynthesized nanoparticles do not require additional stabilizing and capping agents to improve stability and biocompatibility because biological envelops are naturally formed on the surface of the nanoparticles during the process. [149] Among various biological entities as biofactories, electrogenic bacteria have received notable attention because they can synthesize the nanoparticles outside cells or on the surface of the cell membrane via the EET-driven reduction process. [149,150] Clearly, the extracellularly formed nanoparticles can be readily extracted by simple centrifugation in a cost-effective and ecofriendly manner.…”

“…[149] Among various biological entities as biofactories, electrogenic bacteria have received notable attention because they can synthesize the nanoparticles outside cells or on the surface of the cell membrane via the EET-driven reduction process. [149,150] Clearly, the extracellularly formed nanoparticles can be readily extracted by simple centrifugation in a cost-effective and ecofriendly manner. Although extracellular biosynthesis can be beneficial to industrial-scale production, the technique is in its infancy and considerable advancements are required for practical implementation.…”

“…[155][156][157][158] Because most nanoparticles are in situ biosynthesized in the microbial electron transport pathways, they dramatically facilitate bacterial EET as a conductive conduit through the insulating cell membranes, thus improving power performance. [149,150,159] Furthermore, the bottom-up self-assembly process provides the most innovative but realistic solution toward the future fabrication of next-generation MFC devices. Wu et al reported a pioneering study on palladium nanoparticle biosynthesis in bacterial EET, exploring the microbial electrochemistry and the role of biosynthesized metals (Figure 8a).…”

Gentle Patterning Approaches toward Compatibility with Bio‐Organic Materials and Their Environmental Aspects

“…[72] 2.2.2. Biological nanowires Protein and protein-lipid nanowire structures, [73,74] in which electron transfer is observed over significant distances (in terms of biological dimensions), also lack the developed methodological base of patterning. Indeed, being a convenient natural nanostructure, these objects require a design of reliable electrical contacts, which might imply deposition of non-metallic delicate conductors with a nanometer precision.…”