Review Article
Electrically conductive pili: Biological function and potential applications in electronics

https://doi.org/10.1016/j.coelec.2017.08.015Get rights and content

Highlights

  • •

    e-Pili enable unprecedented long-range biological electron transfer.

  • •

    e-Pili are electrical connectors for interspecies electron transfer and Fe(III) oxide reduction.

  • •

    Aromatic amino acids are key components in electron transport along e-pili.

  • •

    Synthetic e-pili with novel properties can be expressed with genetic manipulation.

  • •

    The properties of e-pili suggest applications as ‘green’ components in electronic devices.

Electrically conductive pili (e-pili) enable long-range electron exchange between microorganisms and their extracellular environment and show promise as a ‘green’ electronic material. Most studies have focused on the e-pili of G. sulfurreducens, which play a role in Fe(III) oxide reduction and interspecies electron transfer, and confer conductivity to current-producing biofilms. However, a diversity of other microorganisms have recently been found to possess e-pili, including e-pili with unique structures. Aromatic amino acids are key elements in electron transport along the length of e-pili and the conductivity of synthetic e-pili can be tuned by manipulating aromatic content. e-Pili are attractive as an electronic material because they can be produced from renewable feedstocks and are biodegradable, yet they are also highly robust for device fabrication. Basic information on the structure of e-pili, mechanisms for electron transport, and other electronic properties is required in order to better understand their biological function and to guide the design of synthetic e-pili for applications as electronic components.

Introduction

Electrically conductive pili (e-pili) enable electron transport over unprecedented distances for a biological protein and confer unique properties to microorganisms of biogeochemical and practical significance [1]. Furthermore, e-pili are a sustainable ‘green’ electronic material with diverse potential applications [2]. Following the initial discovery of e-pili in Geobacter sulfurreducens [3], highly divergent hypotheses were put forth on e-pili function within microbial communities and the mechanisms of electron transport along e-pili [1]. However, recent experimental evidence has culled some of these early concepts and has provided a foundation for further hypothesis development. The purpose of this review is to summarize these recent studies, focusing on publications within the last two years, with the exception that key earlier papers are mentioned when required for context. Current concepts on mechanisms for electron transfer along e-pili are discussed, as well as the possible biological functions of e-pili, and emerging technologies based on e-pili (Figure 1).

Section snippets

What is an e-pilus and who has them?

An e-pilus is any pilus that is sufficiently electrically conductive along its length to promote long-range electron exchange between the microbe expressing e-pili and the external environment. Conductivity data for e-pili under physiologically relevant conditions is limited (Box 1). The specific threshold conductivity required to satisfy the definition of an e-pilus is dependent on its function. Rough guidelines for the e-pili conductivity necessary for electron transport to extracellular

Mechanisms for electron transport along e-pili

Electron transport mechanisms for e-pili have primarily been investigated with e-pili from G. sulfurreducens and related proteins. Individual e-pili that are free of other proteins or metals have substantial conductivities (50 mS/cm–1 kS/cm) 4.●, 5., 6., 20., 21.●●. Propagation of charge along cytochrome-free regions of G. sulfurreducens e-pili was also documented with electrostatic force microscopy [22]. These direct experimental measurements negate multiple previous theoretical models which

Natural roles for e-Pili: direct interspecies electron transfer and Fe(III) reduction

A full understanding of the mechanisms for e-pili conductivity is not necessary to appreciate the remarkable biological capabilities that long-range electron transport along e-pili can provide to microorganisms. e-Pili permit cells to make direct electrical connections with insoluble electron acceptors multiple cell lengths from the cell surface 1., 31., 32., 33.. For example, direct interspecies electron transfer (DIET) with Geobacter species as the electron donating partner has been shown to

Role of e-Pili in conductive biofilms

The evolution of some Geobacter species to participate in DIET is a likely explanation for their effectiveness in growing thick conductive biofilms on the anodes of bioelectrochemical devices [39]. This conclusion is in accordance with the studies which first suggested that e-pili networks conferred conductivity to G. sulfurreducens biofilms, permitting cells at distance from the anode to contribute to current production by transferring electrons to the conductive e-pili network 23., 40.. Many

e-Pili as sustainable electronic materials

As the biological role of e-pili has become clearer, some research focus has shifted to investigating the possibility that e-pili might serve as a renewable electronic material. e-Pili have many attractive material properties [2]. For example, e-pili can readily be mass produced from renewable feedstocks, contain no toxic components, and can be recycled as a degradable organic material. They are thinner than many other nanowire materials of similar conductivity [21●●]. e-Pili properties such as

Conclusions

Significant advances in e-pili research can be expected in the near future. Elucidating the structure of an e-pilus will be a major breakthrough, providing a better understanding of the mechanisms for electron transport along e-pili and serving as a guide for the design of synthetic e-pili with novel properties. Continued prospecting through the microbial world for additional e-pili 12.●●, 13.●● will improve understanding of their biological role and provide a broader range of electronic

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • Paper of special interest.

  • •• Paper of outstanding interest.

Acknowledgment

Research in my laboratory on e-pili is supported by supported by Office of Naval Research Grants N000141310549 and N000141612526.

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