Abstract

The genomes of Thiohalobacter thiocyanaticus and Guyparkeria (formerly known as Halothiobacillus) sp. SCN-R1, two gammaproteobacterial halophilic sulfur-oxidizing bacteria (SOB) capable of thiocyanate oxidation via the “cyanate pathway”, have been analyzed with a particular focus on their thiocyanate-oxidizing potential and sulfur oxidation pathways. Both genomes encode homologs of the enzyme thiocyanate dehydrogenase (TcDH) that oxidizes thiocyanate via the “cyanate pathway” in members of the haloalkaliphilic SOB of the genus Thioalkalivibrio. However, despite the presence of conservative motives indicative of TcDH, the putative TcDH of the halophilic SOB have a low overall amino acid similarity to the Thioalkalivibrio enzyme, and also the surrounding genes in the TcDH locus were different. In particular, an alternative copper transport system Cus is present instead of Cop and a putative zero-valent sulfur acceptor protein gene appears just before TcDH. Moreover, in contrast to the thiocyanate-oxidizing Thioalkalivibrio species, both genomes of the halophilic SOB contained a gene encoding the enzyme cyanate hydratase. The sulfur-oxidizing pathway in the genome of Thiohalobacter includes a Fcc type of sulfide dehydrogenase, a rDsr complex/AprAB/Sat for oxidation of zero-valent sulfur to sulfate, and an incomplete Sox pathway, lacking SoxCD. The sulfur oxidation pathway reconstructed from the genome of Guyparkeria sp. SCN-R1 was more similar to that of members of the Thiomicrospira-Hydrogenovibrio group, including a Fcc type of sulfide dehydrogenase and a complete Sox complex. One of the outstanding properties of Thiohalobacter is the presence of a Na+-dependent ATP synthase, which is rarely found in aerobic Prokaryotes.Overall, the results showed that, despite an obvious difference in the general sulfur-oxidation pathways, halophilic and haloalkaliphilic SOB belonging to different genera within the Gammaproteobacteria developed a similar unique thiocyanate-degrading mechanism based on the direct oxidative attack on the sulfane atom of thiocyanate.

Highlights

  • Chemolithoautotrophic sulfur-oxidizing bacteria (SOB) play an important role in the global biogeochemical sulfur cycle by oxidizing various reduced sulfur compounds, such as sulfide, sulfur, thiosulfate and polythionates, to sulfate both in natural and industrial habitats (Janssen et al, 2009; Caia et al, 2017; Wasmund et al, 2017).Only a few of these SOB have the ability to use thiocyanate as an energy source

  • Primary degradation of the thiocyanate molecule is needed before the reduced sulfane atom could be utilized, which is not an easy task, since the molecule is chemically stable, which might be a reason for the scarcity of thiocyanate-utilizing SOB known in culture

  • The genome of Thiohalobacter thiocyanaticus HRh1T, which was sequenced with PaqBio and Illumina, consists of two scaffolds with a total size of 3.3 Mbp

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Summary

Introduction

Chemolithoautotrophic sulfur-oxidizing bacteria (SOB) play an important role in the global biogeochemical sulfur cycle by oxidizing various reduced sulfur compounds, such as sulfide, sulfur, thiosulfate and polythionates, to sulfate both in natural and industrial habitats (Janssen et al, 2009; Caia et al, 2017; Wasmund et al, 2017).Only a few of these SOB have the ability to use thiocyanate as an energy source. Thiocyanate can be regarded as an inorganic nitrile whereby its carbon atom is linked to a reduced sulfur atom (N≡C-S−) This reduced sulfur compound is forming at low concentrations in natural habitats by reaction of cyanide with inorganic sulfan atom donors, such as thiosulfate, tetrathionate or polysulfide (Kurashova et al, 2017). Thiocyanate is formed as a major waste product in metallurgy and precious metal mining with cyanide (Luque-Almagro et al, 2016). Since it has a reduced sulfane atom similar to sulfide, it can be used by some SOB as an electron donor. Primary degradation of the thiocyanate molecule is needed before the reduced sulfane atom could be utilized, which is not an easy task, since the molecule is chemically stable, which might be a reason for the scarcity of thiocyanate-utilizing SOB known in culture

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