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Understanding Stress Response to High-Arsenic Gold-Bearing Sulfide Concentrate in Extremely Metal-Resistant Acidophile Sulfobacillus thermotolerans.

ABSTRACT: Biooxidation of gold-bearing arsenopyrite concentrates, using acidophilic microbial communities, is among the largest commercial biohydrometallurgical processes. However, molecular mechanisms of microbial responses to sulfide raw materials have not been widely studied. The goal of this research was to gain insight into the defense strategies of the acidophilic bacterium Sulfobacillus thermotolerans, which dominates microbial communities functioning in industrial biooxidation processes at >35 °C, against the toxic effect of the high-arsenic gold-bearing sulfide concentrate. In addition to extreme metal resistance, this acidophile proved to be one of the most As-tolerant microorganisms. Comparative proteomic analysis indicated that 30 out of 33 differentially expressed proteins were upregulated in response to the ore concentrate, while the synthesis level of the functional proteins required for cell survival was not negatively affected. Despite a high level of cellular metal(loid) accumulation, no specific metal(loid)-resistant systems were regulated. Instead, several proteins involved in the metabolic pathways and stress response, including MBL fold metallo-hydrolase, sulfide:quinone oxidoreductase, and GroEL chaperonin, may play crucial roles in resistance to the sulfide ore concentrate and arsenic, in particular. This study provides the first data on the microbial responses to sulfide ore concentrates and advances our understanding of defense mechanisms against toxic compounds in acidophiles.

SUBMITTER: Panyushkina A

PROVIDER: S-EPMC7409299 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Understanding Stress Response to High-Arsenic Gold-Bearing Sulfide Concentrate in Extremely Metal-Resistant Acidophile <i>Sulfobacillus thermotolerans</i>.

Panyushkina Anna A Matyushkina Daria D Pobeguts Olga O

Microorganisms 20200719 7

Biooxidation of gold-bearing arsenopyrite concentrates, using acidophilic microbial communities, is among the largest commercial biohydrometallurgical processes. However, molecular mechanisms of microbial responses to sulfide raw materials have not been widely studied. The goal of this research was to gain insight into the defense strategies of the acidophilic bacterium <i>Sulfobacillus thermotolerans</i>, which dominates microbial communities functioning in industrial biooxidation processes at ...[more]

PMID: 32707712

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Project description:Recent phylogenomic analysis has suggested that three strains isolated from different copper mine tailings around the world were taxonomically affiliated with Sulfobacillusthermosulfidooxidans Here, we present a detailed investigation of their genomic features, particularly with respect to metabolic potentials and stress tolerance mechanisms. Comprehensive analysis of the Sulfobacillus genomes identified a core set of essential genes with specialized biological functions in the survival of acidophiles in their habitats, despite differences in their metabolic pathways. The Sulfobacillus strains also showed evidence for stress management, thereby enabling them to efficiently respond to harsh environments. Further analysis of metabolic profiles provided novel insights into the presence of genomic streamlining, highlighting the importance of gene loss as a main mechanism that potentially contributes to cellular economization. Another important evolutionary force, especially in larger genomes, is gene acquisition via horizontal gene transfer (HGT), which might play a crucial role in the recruitment of novel functionalities. Also, a successful integration of genes acquired from archaeal donors appears to be an effective way of enhancing the adaptive capacity to cope with environmental changes. Taken together, the findings of this study significantly expand the spectrum of HGT and genome reduction in shaping the evolutionary history of Sulfobacillus strains.IMPORTANCE Horizontal gene transfer (HGT) and gene loss are recognized as major driving forces that contribute to the adaptive evolution of microbial genomes, although their relative importance remains elusive. The findings of this study suggest that highly frequent gene turnovers within microorganisms via HGT were necessary to incur additional novel functionalities to increase the capacity of acidophiles to adapt to changing environments. Evidence also reveals a fascinating phenomenon of potential cross-kingdom HGT. Furthermore, genome streamlining may be a critical force in driving the evolution of microbial genomes. Taken together, this study provides insights into the importance of both HGT and gene loss in the evolution and diversification of bacterial genomes.

Project description:β-Hydroxy-α-amino acids are useful compounds for pharmaceutical development. Enzymatic synthesis of β-hydroxy-α-amino acids has attracted considerable interest as a selective, sustainable, and environmentally benign process. In this study, we identified a novel amino acid hydroxylase, AEP14369, from Sulfobacillus thermotolerans Y0017, which is included in a previously constructed CAS-like superfamily protein library, to widen the variety of amino acid hydroxylases. The detailed structures determined by nuclear magnetic resonance and X-ray crystallography analysis of the enzymatically produced compounds revealed that AEP14369 catalyzed threo-β-selective hydroxylation of l-His and l-Gln in a 2-oxoglutarate-dependent manner. Furthermore, the production of l-threo-β-hydroxy-His and l-threo-β-hydroxy-Gln was achieved using Escherichia coli expressing the gene encoding AEP14369 as a whole-cell biocatalyst. Under optimized reaction conditions, 137 mM (23.4 g liter-1) l-threo-β-hydroxy-His and 150 mM l-threo-β-hydroxy-Gln (24.3 g liter-1) were obtained, indicating that the enzyme is applicable for preparative-scale production. AEP14369, an l-His/l-Gln threo-β-hydroxylase, increases the availability of 2-oxoglutarate-dependent hydroxylase and opens the way for the practical production of β-hydroxy-α-amino acids in the future. The amino acids produced in this study would also contribute to the structural diversification of pharmaceuticals that affect important bioactivities. IMPORTANCE Owing to an increasing concern for sustainability, enzymatic approaches for producing industrially useful compounds have attracted considerable attention as a powerful complement to chemical synthesis for environment-friendly synthesis. In this study, we developed a bioproduction method for β-hydroxy-α-amino acid synthesis using a newly discovered enzyme. AEP14369 from the moderate thermophilic bacterium Sulfobacillus thermotolerans Y0017 catalyzed the hydroxylation of l-His and l-Gln in a regioselective and stereoselective fashion. Furthermore, we biotechnologically synthesized both l-threo-β-hydroxy-His and l-threo-β-hydroxy-Gln with a titer of over 20 g liter-1 through whole-cell bioconversion using recombinant Escherichia coli cells. As β-hydroxy-α-amino acids are important compounds for pharmaceutical development, this achievement would facilitate future sustainable and economical industrial applications.

Dataset Information

Understanding Stress Response to High-Arsenic Gold-Bearing Sulfide Concentrate in Extremely Metal-Resistant Acidophile Sulfobacillus thermotolerans.

Publications

Understanding Stress Response to High-Arsenic Gold-Bearing Sulfide Concentrate in Extremely Metal-Resistant Acidophile <i>Sulfobacillus thermotolerans</i>.

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