An electrogenic redox loop in sulfate reduction reveals a likely widespread mechanism of energy conservation

Américo G Duarte,Teresa Catarino,Diana Lousa,Thomas A Clarke,Cláudio M Soares,Sinje Neukirchen,Inês A C Pereira,Gaye F White,Filipa L Sousa

doi:10.1038/s41467-018-07839-x

Abstract

The bioenergetics of anaerobic metabolism frequently relies on redox loops performed by membrane complexes with substrate- and quinone-binding sites on opposite sides of the membrane. However, in sulfate respiration (a key process in the biogeochemical sulfur cycle), the substrate- and quinone-binding sites of the QrcABCD complex are periplasmic, and their role in energy conservation has not been elucidated. Here we show that the QrcABCD complex of Desulfovibrio vulgaris is electrogenic, as protons and electrons required for quinone reduction are extracted from opposite sides of the membrane, with a H+/e− ratio of 1. Although the complex does not act as a H+-pump, QrcD may include a conserved proton channel leading from the N-side to the P-side menaquinone pocket. Our work provides evidence of how energy is conserved during dissimilatory sulfate reduction, and suggests mechanisms behind the functions of related bacterial respiratory complexes in other bioenergetic contexts.

Highlights

The bioenergetics of anaerobic metabolism frequently relies on redox loops performed by membrane complexes with substrate- and quinone-binding sites on opposite sides of the membrane
The QrcABCD membrane complex was reconstituted in liposomes (Supplementary Fig. 2), in the presence or absence of menaquinone-4 (MK4), according to the onset method[36]
The charge separation is achieved as the result of electron transfer from the positive (P) to the negative (N) side of the membrane accompanied with scalar proton uptake on the N side and release on the P side

Summary

Introduction

The bioenergetics of anaerobic metabolism frequently relies on redox loops performed by membrane complexes with substrate- and quinone-binding sites on opposite sides of the membrane. In sulfate respiration (a key process in the biogeochemical sulfur cycle), the substrate- and quinone-binding sites of the QrcABCD complex are periplasmic, and their role in energy conservation has not been elucidated. The dissimilatory reduction of sulfate is one of the most important processes of microbial respiration in anoxic environments, where it plays a major role in both the sulfur and carbon biogeochemical cycles[1,2]. The QrcABC proteins are on the periplasmic side of the cytoplasmic membrane and this complex links periplasmic hydrogen and formate oxidation to the MK pool[7,8] It is present in the large family of Deltaproteobacteria sulfate reducers, which are characterized by an abundance of multiheme cytochromes c (namely TpIc3), and hydrogenases or formate dehydrogenases that lack a membrane subunit for direct quinone reduction[6]. Desulfovibrio alaskensis G20, the Qrc complex was shown to be essential for growth on H2 or formate and sulfate[8] and it has been implicated in syntrophic growth[18,19]

Methods

Results

Conclusion