Structural Basis for Metallic-Like Conductivity in Microbial Nanowires

ABSTRACT Direct measurement of multiple physical properties of Geobacter sulfurreducens pili have demonstrated that they possess metallic-like conductivity, but several studies have suggested that metallic-like conductivity is unlikely based on the structures of the G. sulfurreducens pilus predicted...

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Autores principales:	Nikhil S. Malvankar, Madeline Vargas, Kelly Nevin, Pier-Luc Tremblay, Kenneth Evans-Lutterodt, Dmytro Nykypanchuk, Eric Martz, Mark T. Tuominen, Derek R. Lovley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/64c2358021474adb8b40345f74e76c54
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spelling	oai:doaj.org-article:64c2358021474adb8b40345f74e76c542021-11-15T15:41:34ZStructural Basis for Metallic-Like Conductivity in Microbial Nanowires10.1128/mBio.00084-152150-7511https://doaj.org/article/64c2358021474adb8b40345f74e76c542015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00084-15https://doaj.org/toc/2150-7511ABSTRACT Direct measurement of multiple physical properties of Geobacter sulfurreducens pili have demonstrated that they possess metallic-like conductivity, but several studies have suggested that metallic-like conductivity is unlikely based on the structures of the G. sulfurreducens pilus predicted from homology models. In order to further evaluate this discrepancy, pili were examined with synchrotron X-ray microdiffraction and rocking-curve X-ray diffraction. Both techniques revealed a periodic 3.2-Å spacing in conductive, wild-type G. sulfurreducens pili that was missing in the nonconductive pili of strain Aro5, which lack key aromatic acids required for conductivity. The intensity of the 3.2-Å peak increased 100-fold when the pH was shifted from 10.5 to 2, corresponding with a previously reported 100-fold increase in pilus conductivity with this pH change. These results suggest a clear structure-function correlation for metallic-like conductivity that can be attributed to overlapping π-orbitals of aromatic amino acids. A homology model of the G. sulfurreducens pilus was constructed with a Pseudomonas aeruginosa pilus model as a template as an alternative to previous models, which were based on a Neisseria gonorrhoeae pilus structure. This alternative model predicted that aromatic amino acids in G. sulfurreducens pili are packed within 3 to 4 Å, consistent with the experimental results. Thus, the predictions of homology modeling are highly sensitive to assumptions inherent in the model construction. The experimental results reported here further support the concept that the pili of G. sulfurreducens represent a novel class of electronically functional proteins in which aromatic amino acids promote long-distance electron transport. IMPORTANCE The mechanism for long-range electron transport along the conductive pili of Geobacter sulfurreducens is of interest because these “microbial nanowires” are important in biogeochemical cycling as well as applications in bioenergy and bioelectronics. Although proteins are typically insulators, G. sulfurreducens pilus proteins possess metallic-like conductivity. The studies reported here provide important structural insights into the mechanism of the metallic-like conductivity of G. sulfurreducens pili. This information is expected to be useful in the design of novel bioelectronic materials.Nikhil S. MalvankarMadeline VargasKelly NevinPier-Luc TremblayKenneth Evans-LutterodtDmytro NykypanchukEric MartzMark T. TuominenDerek R. LovleyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Nikhil S. Malvankar Madeline Vargas Kelly Nevin Pier-Luc Tremblay Kenneth Evans-Lutterodt Dmytro Nykypanchuk Eric Martz Mark T. Tuominen Derek R. Lovley Structural Basis for Metallic-Like Conductivity in Microbial Nanowires
description	ABSTRACT Direct measurement of multiple physical properties of Geobacter sulfurreducens pili have demonstrated that they possess metallic-like conductivity, but several studies have suggested that metallic-like conductivity is unlikely based on the structures of the G. sulfurreducens pilus predicted from homology models. In order to further evaluate this discrepancy, pili were examined with synchrotron X-ray microdiffraction and rocking-curve X-ray diffraction. Both techniques revealed a periodic 3.2-Å spacing in conductive, wild-type G. sulfurreducens pili that was missing in the nonconductive pili of strain Aro5, which lack key aromatic acids required for conductivity. The intensity of the 3.2-Å peak increased 100-fold when the pH was shifted from 10.5 to 2, corresponding with a previously reported 100-fold increase in pilus conductivity with this pH change. These results suggest a clear structure-function correlation for metallic-like conductivity that can be attributed to overlapping π-orbitals of aromatic amino acids. A homology model of the G. sulfurreducens pilus was constructed with a Pseudomonas aeruginosa pilus model as a template as an alternative to previous models, which were based on a Neisseria gonorrhoeae pilus structure. This alternative model predicted that aromatic amino acids in G. sulfurreducens pili are packed within 3 to 4 Å, consistent with the experimental results. Thus, the predictions of homology modeling are highly sensitive to assumptions inherent in the model construction. The experimental results reported here further support the concept that the pili of G. sulfurreducens represent a novel class of electronically functional proteins in which aromatic amino acids promote long-distance electron transport. IMPORTANCE The mechanism for long-range electron transport along the conductive pili of Geobacter sulfurreducens is of interest because these “microbial nanowires” are important in biogeochemical cycling as well as applications in bioenergy and bioelectronics. Although proteins are typically insulators, G. sulfurreducens pilus proteins possess metallic-like conductivity. The studies reported here provide important structural insights into the mechanism of the metallic-like conductivity of G. sulfurreducens pili. This information is expected to be useful in the design of novel bioelectronic materials.
format	article
author	Nikhil S. Malvankar Madeline Vargas Kelly Nevin Pier-Luc Tremblay Kenneth Evans-Lutterodt Dmytro Nykypanchuk Eric Martz Mark T. Tuominen Derek R. Lovley
author_facet	Nikhil S. Malvankar Madeline Vargas Kelly Nevin Pier-Luc Tremblay Kenneth Evans-Lutterodt Dmytro Nykypanchuk Eric Martz Mark T. Tuominen Derek R. Lovley
author_sort	Nikhil S. Malvankar
title	Structural Basis for Metallic-Like Conductivity in Microbial Nanowires
title_short	Structural Basis for Metallic-Like Conductivity in Microbial Nanowires
title_full	Structural Basis for Metallic-Like Conductivity in Microbial Nanowires
title_fullStr	Structural Basis for Metallic-Like Conductivity in Microbial Nanowires
title_full_unstemmed	Structural Basis for Metallic-Like Conductivity in Microbial Nanowires
title_sort	structural basis for metallic-like conductivity in microbial nanowires
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/64c2358021474adb8b40345f74e76c54
work_keys_str_mv	AT nikhilsmalvankar structuralbasisformetalliclikeconductivityinmicrobialnanowires AT madelinevargas structuralbasisformetalliclikeconductivityinmicrobialnanowires AT kellynevin structuralbasisformetalliclikeconductivityinmicrobialnanowires AT pierluctremblay structuralbasisformetalliclikeconductivityinmicrobialnanowires AT kennethevanslutterodt structuralbasisformetalliclikeconductivityinmicrobialnanowires AT dmytronykypanchuk structuralbasisformetalliclikeconductivityinmicrobialnanowires AT ericmartz structuralbasisformetalliclikeconductivityinmicrobialnanowires AT markttuominen structuralbasisformetalliclikeconductivityinmicrobialnanowires AT derekrlovley structuralbasisformetalliclikeconductivityinmicrobialnanowires
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Structural Basis for Metallic-Like Conductivity in Microbial Nanowires

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