Going the Distance: Long-Range Conductivity in Protein and Peptide Bioelectronic Materials

Abstract

Bioelectronic materials interface biomolecules, cells, organs, or organisms with electronic devices, and they represent an active and growing field of materials research. Protein and peptide nanostructures are ideal bioelectronic materials. They possess many of the properties required for biocompatibility across scales from enzymatic to organismal interfaces, and recent examples of supramolecular protein and peptide nanostructures exhibit impressive electronic properties. The ability of such natural and synthetic protein and peptide materials to conduct electricity over micrometer to centimeter length scales, however, is not readily understood from a conventional view of their amino acid building blocks. Distinct in structure and properties from solid-state inorganic and synthetic organic metals and semiconductors, supramolecular conductive proteins and peptides require careful theoretical treatment and experimental characterization methods to understand their electronic structure. In this review, we discuss theory and experimental evidence from recent literature describing the long-range conduction of electronic charge in protein and peptide materials. Electron transfer across proteins has been studied extensively, but application of models for such short-range charge transport to longer distances relevant to bioelectronic materials are less well-understood. Implementation of electronic band structure and electron transfer formulations in extended biomolecular systems will be covered in the context of recent materials discoveries and efforts at characterization of electronic transport mechanisms.

The Archaellum ofMethanospirillum hungateiis Electrically Conductive

“…e-Pili enable unprecedented long-range (μm) electron conduction along the length of a protein filament, which not only has important biological implications, but also suggests diverse applications for these ‘protein nanowires’ as a sustainably produced electronic material 1,4–6 . There is substantial debate over the potential mechanisms of long-range electron transport in e-pili 1,5,6 , which is unresolved in large part because of the lack of a definitive e-pili structure. Although it has been possible to determine the structure of some pili with cryo-electron microscopy (cryo-EM) 7 , to date, the thin diameter (3 nm) and high flexibility of G. sulfurreducens e-pili have thwarted structural determination with the cryo-EM approach.…”

“…The cryo-EM structure of the M. hungatei e-archaellum 10 provides the first opportunity to directly evaluate possible routes for long-range electron transport along a biologically produced protein filament. Multiple lines of experimental evidence suggest that closely packed aromatic amino acids confer conductivity to G. sulfurreducens e-pili 1,5 Analysis of the distribution of aromatic amino acids in the M. hungatei e-archaellum revealed aromatic side chains organized in three distinct groups: a core, a middle sleeve, and an outer sleeve (Fig. 2a).…”

Geobacter protein nanowires

“…The focus is on biological function. Mechanistic details of the mechanisms for electron transport along the filaments will not be discussed in detail because: 1) this topic is a matter of debate, requiring further experimentation (Lovley, 2017b;Creasey et al, 2018;Ing et al, 2018;Ru et al, 2019); and 2) it is not necessary to know the fine-scale mechanistic details of electron transport along the filaments in order to identify the filaments or evaluate their biological function. The primary questions addressed are: 1) what is the evidence for epili and OmcS filaments in live cells?…”

Extracellular Electron Transfer: Respiratory or Nutrient Homeostasis?

“…G. sulfurreducens trans-fers electrons over large distances via conducting pili or filaments. The exact nature, composition, and conductivity of these pili and filaments are still actively debated (3)(4)(5). S. oneidensis transfers electrons extracellularly via outer membrane cytochromes, with the MtrCAB complex being the best characterized (6,7).…”