Abstract

The porin-cytochrome (Pcc) protein complex is responsible for trans-outer membrane electron transfer during extracellular reduction of Fe(III) by the dissimilatory metal-reducing bacterium Geobacter sulfurreducens PCA. The identified and characterized Pcc complex of G. sulfurreducens PCA consists of a porin-like outer-membrane protein, a periplasmic 8-heme c-type cytochrome (c-Cyt) and an outer-membrane 12-heme c-Cyt, and the genes encoding the Pcc proteins are clustered in the same regions of genome (i.e., the pcc gene clusters) of G. sulfurreducens PCA. A survey of additionally microbial genomes has identified the pcc gene clusters in all sequenced Geobacter spp. and other bacteria from six different phyla, including Anaeromyxobacter dehalogenans 2CP-1, A. dehalogenans 2CP-C, Anaeromyxobacter sp. K, Candidatus Kuenenia stuttgartiensis, Denitrovibrio acetiphilus DSM 12809, Desulfurispirillum indicum S5, Desulfurivibrio alkaliphilus AHT2, Desulfurobacterium thermolithotrophum DSM 11699, Desulfuromonas acetoxidans DSM 684, Ignavibacterium album JCM 16511, and Thermovibrio ammonificans HB-1. The numbers of genes in the pcc gene clusters vary, ranging from two to nine. Similar to the metal-reducing (Mtr) gene clusters of other Fe(III)-reducing bacteria, such as Shewanella spp., additional genes that encode putative c-Cyts with predicted cellular localizations at the cytoplasmic membrane, periplasm and outer membrane often associate with the pcc gene clusters. This suggests that the Pcc-associated c-Cyts may be part of the pathways for extracellular electron transfer reactions. The presence of pcc gene clusters in the microorganisms that do not reduce solid-phase Fe(III) and Mn(IV) oxides, such as D. alkaliphilus AHT2 and I. album JCM 16511, also suggests that some of the pcc gene clusters may be involved in extracellular electron transfer reactions with the substrates other than Fe(III) and Mn(IV) oxides.

Highlights

  • Geobacter spp. are a group of Gram-negative bacteria whose hallmark feature is transfer of metabolically-derived electrons to appropriate electron-accepting substrates external to the bacterial cells, such as oxidized metals, electrodes and even other microorganisms (Lovley et al, 2004, 2011; Summers et al, 2010)

  • Numbers of the pcc gene clusters found in Geobacter genomes varied, ranging from one in G. bemidjiensis Bem and Geobacter sp

  • Analyses of the amino acid sequences of the Pcc-associated c-type cytochrome (c-Cyt) suggest that they may be involved in redox cycling of quinone/quinol pool in the cytoplasmic membrane and electron transfer across the periplasm and outer membrane

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Summary

Introduction

Geobacter spp. are a group of Gram-negative bacteria whose hallmark feature is transfer of metabolically-derived electrons to appropriate electron-accepting substrates external to the bacterial cells, such as oxidized metals, electrodes and even other microorganisms (Lovley et al, 2004, 2011; Summers et al, 2010). We identified and characterized a trans-outer membrane porin-cytochrome (Pcc) protein complex for transferring electrons across the outer membrane during extracellular reduction of Fe(III) by G. sulfurreducens PCA.

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