Whole-genome sequencing reveals novel insights into sulfur oxidation in the extremophile Acidithiobacillus thiooxidans

Abstract

BackgroundAcidithiobacillus thiooxidans (A. thiooxidans), a chemolithoautotrophic extremophile, is widely used in the industrial recovery of copper (bioleaching or biomining). The organism grows and survives by autotrophically utilizing energy derived from the oxidation of elemental sulfur and reduced inorganic sulfur compounds (RISCs). However, the lack of genetic manipulation systems has restricted our exploration of its physiology. With the development of high-throughput sequencing technology, the whole genome sequence analysis of A. thiooxidans has allowed preliminary models to be built for genes/enzymes involved in key energy pathways like sulfur oxidation.ResultsThe genome of A. thiooxidans A01 was sequenced and annotated. It contains key sulfur oxidation enzymes involved in the oxidation of elemental sulfur and RISCs, such as sulfur dioxygenase (SDO), sulfide quinone reductase (SQR), thiosulfate:quinone oxidoreductase (TQO), tetrathionate hydrolase (TetH), sulfur oxidizing protein (Sox) system and their associated electron transport components. Also, the sulfur oxygenase reductase (SOR) gene was detected in the draft genome sequence of A. thiooxidans A01, and multiple sequence alignment was performed to explore the function of groups of related protein sequences. In addition, another putative pathway was found in the cytoplasm of A. thiooxidans, which catalyzes sulfite to sulfate as the final product by phosphoadenosine phosphosulfate (PAPS) reductase and adenylylsulfate (APS) kinase. This differs from its closest relative Acidithiobacillus caldus, which is performed by sulfate adenylyltransferase (SAT). Furthermore, real-time quantitative PCR analysis showed that most of sulfur oxidation genes were more strongly expressed in the S0 medium than that in the Na2S2O3 medium at the mid-log phase.ConclusionSulfur oxidation model of A. thiooxidans A01 has been constructed based on previous studies from other sulfur oxidizing strains and its genome sequence analyses, providing insights into our understanding of its physiology and further analysis of potential functions of key sulfur oxidation genes.

Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

“…Sulfur oxygenase reductase (SOR) catalyzes the disproportionation reaction of linear polysulfide in the presence of molecular oxygen to generate hydrogen sulfide, sulfite, and thiosulfate (57,58). SOR was identified in all Sulfobacillus spp., with S. thermosulfidooxidans strains and Sulfobacillus sp.…”

“…An additional route for tetrathionate metabolism in S. acidophilus strains was predicted to be driven by tetrathionate reductase, which is a three-subunit enzyme that catalyzes the reduction of tetrathionate to produce thiosulfate (59). Another important enzyme complex associated with sulfur compound oxidation in Sulfobacillus strains is heterodisulfide reductase-like protein, which is also frequently observed in other acidophilic sulfur oxidizers, such as Acidithiobacillus (57,60,61). All Sulfobacillus strains exhibited the predicted sulfate reduction, although only the S. acidophilus strains harbored the sulfite reductase (ferredoxin) as an additional enzyme.…”

“…Other metabolic enzymes potentially involved in sulfur oxidation of Sulfobacillus strains include sulfide:quinone oxidoreductase, thiosulfate:quinone oxidoreductase that is encoded by doxDA, and thiosulfate sulfurtransferase. Sulfobacillus genomes were predicted to possess tetrathionate hydrolase, which directs the disproportionation of tetrathionate to generate sulfate, thiosulfate, and other sulfur compounds (57). An additional route for tetrathionate metabolism in S. acidophilus strains was predicted to be driven by tetrathionate reductase, which is a three-subunit enzyme that catalyzes the reduction of tetrathionate to produce thiosulfate (59).…”

Biological treatment of coal combustion wastes by Acidithiobacillus thiooxidans DSM 26636

“…During bioleaching, bio-oxidation of elemental sulfur by A. thiooxidans produce H + that causes the decrease of pH that is involved in the bioleaching process (Zhou et al, 2014). The metabolites, mainly sulfuric acid, play a major role during bioleaching of heavy metals and is typically related to copper mining operations (bioleaching) (Chang et al, 2008;Yin et al, 2014). Acidithiobacillus group has been used for dissolution of Cu, Zn, Fe and As from different ores and wastes.…”

Bioelectrochemical Changes during the Early Stages of Chalcopyrite Interaction with Acidithiobacillus Thiooxidans and Leptospirillum sp.

“…Currently, there is limited research on electron transfer between Fe 3+ and RSS. According to Rohwerder et al [25] and Yin et al [26], the activation of S 0 from cyclic to linear RSS proceeds via a nucleophilic attack of glutathione (GSH) and sulfonate (-SH) groups found in the outer-membrane protein of SOM. We hypothesize that Fe ions also favor such activation of the linear structures (Figure 5a), as the results of this and other works suggested, as well as the Hard-Soft Acid Base Theory studies on solid sulfur allotropes and sulfur oxidation [15,[26][27][28][29][30][31][32][33].…”