Abstract
The study of electrically conductive protein nanowires in Geobacter sulfurreducens has led to new concepts for long-range extracellular electron transport, as well as for the development of sustainable conductive materials and electronic devices with novel functions. Until recently, electrically conductive pili (e-pili), assembled from the PilA pilin monomer, were the only known Geobacter protein nanowires. However, filaments comprised of the multi-heme c-type cytochrome, OmcS, are present in some preparations of G. sulfurreducens outer-surface proteins. The purpose of this review is to evaluate the available evidence on the in vivo expression of e-pili and OmcS filaments and their biological function. Abundant literature demonstrates that G. sulfurreducens expresses e-pili, which are required for long-range electron transport to Fe (III) oxides and through conductive biofilms. In contrast, there is no definitive evidence yet that wild-type G. sulfurreducens express long filaments of OmcS extending from the cells, and deleting the gene for OmcS actually increases biofilm conductivity. The literature does not support the concern that many previous studies on e-pili were mistakenly studying OmcS filaments. For example, heterologous expression of the aromatic-rich pilin monomer of Geobacter metallireducens in G. sulfurreducens increases the conductivity of individual nanowires more than 5,000-fold, whereas expression of an aromatic-poor pilin reduced conductivity more than 1,000-fold. This more than million-fold range in nanowire conductivity was achieved while maintaining the 3-nm diameter characteristic of e-pili. Purification methods that eliminate all traces of OmcS yield highly conductive e-pili, as does heterologous expression of the e-pilin monomer in microbes that do not produce OmcS or any other outer-surface cytochromes. Future studies of G. sulfurreducens expression of protein nanowires need to be cognizant of the importance of maintaining environmentally relevant growth conditions because artificial laboratory culture conditions can rapidly select against e-pili expression. Principles derived from the study of e-pili have enabled identification of non-cytochrome protein nanowires in diverse bacteria and archaea. A similar search for cytochrome appendages is warranted. Both e-pili and OmcS filaments offer design options for the synthesis of protein-based “green” electronics, which may be the primary driving force for the study of these structures in the near future.
Highlights
The concept of long-range electron transport through microbially produced protein filaments with nanometer diameters (Reguera et al, 2005) has provided new insights into microbial physiology and ecology (Lovley, 2017b,c,d)
Oxidation of organic compounds by Geobacter species coupled to direct interspecies electron transfer (DIET) to methanogens is an important aspect of carbon and electron flux in some methanogenic soils (Holmes et al, 2017) and anaerobic digesters converting organic wastes to methane (Morita et al, 2011; Rotaru et al, 2014)
The strains expressing the peptide-tagged pili produced current densities comparable to wild-type, confirming that the capacity for longrange electron transport had been maintained (Ueki et al, 2019). These results demonstrate that G. sulfurreducens produces electrically conductive pili from the PilA pilin monomer with no evidence of OmcS filaments emanating from the cells
Summary
The concept of long-range electron transport through microbially produced protein filaments with nanometer diameters (Reguera et al, 2005) has provided new insights into microbial physiology and ecology (Lovley, 2017b,c,d). Enhancing the expression of protein nanowires is a strategy for increasing biofilm conductivity and current production in bioelectrochemical devices (Lovley, 2017b). A wide diversity of microorganisms appear to produce protein nanowires (Reguera et al, 2005; Holmes et al, 2016; Sure et al, 2016; Tan et al, 2017; Walker et al, 2018a,b, 2019), but in most instances, their structure or function have not yet been intensively investigated. Oxidation of organic compounds by Geobacter species coupled to direct interspecies electron transfer (DIET) to methanogens is an important aspect of carbon and electron flux in some methanogenic soils (Holmes et al, 2017) and anaerobic digesters converting organic wastes to methane (Morita et al, 2011; Rotaru et al, 2014). Stimulating Geobacter-enabled DIET with the addition of conductive materials is an effective strategy for accelerating and stabilizing anaerobic digestion (Lovley, 2017c, 2017d; Martins et al, 2018)
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