The Ion-Translocating NrfD-Like Subunit of Energy-Transducing Membrane Complexes.

Filipa Calisto,Manuela M Pereira

doi:10.3389/fchem.2021.663706

Filipa Calisto, Manuela M Pereira

Open Access

https://doi.org/10.3389/fchem.2021.663706

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Abstract

Several energy-transducing microbial enzymes have their peripheral subunits connected to the membrane through an integral membrane protein, that interacts with quinones but does not have redox cofactors, the so-called NrfD-like subunit. The periplasmic nitrite reductase (NrfABCD) was the first complex recognized to have a membrane subunit with these characteristics and consequently provided the family's name: NrfD. Sequence analyses indicate that NrfD homologs are present in many diverse enzymes, such as polysulfide reductase (PsrABC), respiratory alternative complex III (ACIII), dimethyl sulfoxide (DMSO) reductase (DmsABC), tetrathionate reductase (TtrABC), sulfur reductase complex (SreABC), sulfite dehydrogenase (SoeABC), quinone reductase complex (QrcABCD), nine-heme cytochrome complex (NhcABCD), group-2 [NiFe] hydrogenase (Hyd-2), dissimilatory sulfite-reductase complex (DsrMKJOP), arsenate reductase (ArrC) and multiheme cytochrome c sulfite reductase (MccACD). The molecular structure of ACIII subunit C (ActC) and Psr subunit C (PsrC), NrfD-like subunits, revealed the existence of ion-conducting pathways. We performed thorough primary structural analyses and built structural models of the NrfD-like subunits. We observed that all these subunits are constituted by two structural repeats composed of four-helix bundles, possibly harboring ion-conducting pathways and containing a quinone/quinol binding site. NrfD-like subunits may be the ion-pumping module of several enzymes. Our data impact on the discussion of functional implications of the NrfD-like subunit-containing complexes, namely in their ability to transduce energy.

Highlights

All living organisms need energy to fuel life processes
ArrAB complex was described as a periplasmic complex, which is associated with the transmembrane arsenate reductase (ArrC) subunit only in few microorganisms (Duval et al, 2008)
We identified nine genes coding for ArrC subunit, distributed in Gammaproteobacteria, Betaproteobacteria and Euryarchaeota species (Figure 5, ArrC)

Summary

INTRODUCTION

All living organisms need energy to fuel life processes. External energy sources, light or chemical compounds, are converted to biologically usable forms of energy, such as adenosine triphosphate (ATP) or electrochemical gradients. The NrfD-like subunits are present in many and diverse membrane complexes, widespread in Bacteria and Archaea, that can take part in oxygen, nitrogen, sulfur, arsenate or hydrogen metabolism (Figure 1, Table 1) (Rothery et al, 2008; Refojo et al, 2010, 2019; Marreiros et al, 2016). In this work we thoroughly analyze the primary structures of the members of the NrfD family and predicted the respective tertiary structures, the data provided allowed a deep and broad discussion on the presence of ion-conducting pathways and quinone/quinol-binding sites, which impacts on the function of the several complexes, namely in their ability to transduce energy. HybO (1x [3Fe-4S]1+/0, 2x [4Fe-4S]2+/1+) HybA (4x [4Fe-4S]2+/1+) DmsB (4x [4Fe-4S]2+/1+)

RESULTS AND DISCUSSION

MATERIALS AND METHODS

DATA AVAILABILITY STATEMENT