Comparative Genome Analysis Reveals Metabolic Versatility and Environmental Adaptations of Sulfobacillus thermosulfidooxidans Strain ST

Abstract

The genus Sulfobacillus is a cohort of mildly thermophilic or thermotolerant acidophiles within the phylum Firmicutes and requires extremely acidic environments and hypersalinity for optimal growth. However, our understanding of them is still preliminary partly because few genome sequences are available. Here, the draft genome of Sulfobacillus thermosulfidooxidans strain ST was deciphered to obtain a comprehensive insight into the genetic content and to understand the cellular mechanisms necessary for its survival. Furthermore, the expressions of key genes related with iron and sulfur oxidation were verified by semi-quantitative RT-PCR analysis. The draft genome sequence of Sulfobacillus thermosulfidooxidans strain ST, which encodes 3225 predicted coding genes on a total length of 3,333,554 bp and a 48.35% G+C, revealed the high degree of heterogeneity with other Sulfobacillus species. The presence of numerous transposases, genomic islands and complete CRISPR/Cas defence systems testifies to its dynamic evolution consistent with the genome heterogeneity. As expected, S. thermosulfidooxidans encodes a suit of conserved enzymes required for the oxidation of inorganic sulfur compounds (ISCs). The model of sulfur oxidation in S. thermosulfidooxidans was proposed, which showed some different characteristics from the sulfur oxidation of Gram-negative A. ferrooxidans. Sulfur oxygenase reductase and heterodisulfide reductase were suggested to play important roles in the sulfur oxidation. Although the iron oxidation ability was observed, some key proteins cannot be identified in S. thermosulfidooxidans. Unexpectedly, a predicted sulfocyanin is proposed to transfer electrons in the iron oxidation. Furthermore, its carbon metabolism is rather flexible, can perform the transformation of pentose through the oxidative and non-oxidative pentose phosphate pathways and has the ability to take up small organic compounds. It encodes a multitude of heavy metal resistance systems to adapt the heavy metal-containing environments.

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

“…Unfortunately, the environmental attributes of the sampling sites in the Zambian copper mine at that time were not assessed. Strains were cultivated aerobically in 100 ml of liquid 9K basic medium [3.0 g/liter (NH 4 ) 2 SO 4 , 0.5 g/liter MgSO 4 ·7H 2 O, 0.1 g/liter KCl, 0.01 g/liter Ca(NO 3 ) 2 , and 0.5 g/liter K 2 HPO 4 (initial pH 1.6)] with 4.5% (wt/vol) ferrous sulfate (membrane filtered) and 0.02% yeast, as previously described (31). The temperature and shaking speed of the bacterial cultures were 45°C and 170 rpm, respectively.…”

“…Phylogenetic analysis of sulfur oxygenase reductase (a critical enzyme involved in the sulfur oxidation of many acidophiles) unraveled a close relationship between the Sulfobacillus genus and archaeal Ferroplasma acidarmanus (31). Accordingly, it is plausible that archaeal phyla acted as potential gene donors to Sulfobacillus strains.…”

“…Despite their poorly characterized low abundance compared to the dominant iron-oxidizing Leptospirillum spp. or certain members of the heterotrophic Thermoplasmatales, members of the genus Sulfobacillus are metal-tolerant, mildly thermophilic, or thermotolerant acidophiles that promote sulfide mineral dissolution and ubiquitously occur in various acidic habitats (30,31), such as acid mine drainage (32), acid thermal springs (33), hydrothermal vents (34), and industrial bioleaching operations (35). In the past several decades, a number of papers have discussed issues related to key metabolic features within several isolated Sulfobacillus species, namely, S. thermosulfidooxidans (36), S. acidophilus (33), S. thermotolerans (37), S. sibiricus (38), and S. benefaciens (39).…”

Carbon Material with High Specific Surface Area Improves Complex Copper Ores’ Bioleaching Efficiency by Mixed Moderate Thermophiles

“…Four moderately thermophilic strains (Leptospirillum ferriphilum DX, Acidithiobacillus caldus DX, Sulfobacillus thermosulfidooxidans ST and Ferroplasma thermophilum L1) used in this study were isolated from an acid mine drainage in China [19][20][21]. Each strain grew in basal salt media at 45 • C except that L. ferriphilum DX subcultured at 40 • C. L. ferriphilum DX grew at an initial pH of 1.6 and supplemented with FeSO 4 ·7H 2 O (44.7 g/L); A. caldus DX was maintained with an initial pH of 2.0 and added to S 0 (10 g/L); S. thermosulfidooxidans ST was at an initial pH of 1.6 and supplemented with FeSO 4 ·7H 2 O (44.7 g/L) and 0.02% (wt/vol) yeast extract; and F. thermophilum L1 grew in basal salt medium at an initial pH of 1.0 and added with FeSO 4 ·7H 2 O (44.7 g/L) and 0.01% (wt/vol) yeast extract.…”

A Sulfur Oxygenase from the Haloalkaliphilic Bacterium Thioalkalivibrio paradoxus with Atypically Low Reductase Activity

“…Dendrogram and alignment analyses show that the generally conserved SORs from different Gram-negative bacteria are split into distinguishable subgroups independent of phylogenetic relationship of the organisms. In addition, the SORs from the Gram-positive Sulfobacillus species group with archaeal enzymes of the Sulfolobales (Crenarchaeota) and Thermoplasmatales (Euryarchaeota) orders, probably reflecting horizontal gene transfer between microorganisms living in similar acidic environments (18).…”