Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms

Justice, Nicholas B.; Norman, Anders; Brown, Christopher T.; Singh, Anil K.; Thomas, Brian C.; Banfield, Jillian F.

doi:10.1186/1471-2164-15-1107

Cited by 71 publications

(84 citation statements)

References 143 publications

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“…Sulfobacillus spp. are known as mixotrophic acidophiles that are capable of assimilating organic and inorganic carbon (30,34,42,51). Similar to the published Sulfobacillus genomes (30, 31), a full suite of genes involved in the Calvin-Benson-Bassham cycle were predicted in all strains ( Fig.…”

Section: Figsupporting

confidence: 69%

“…Sulfobacillus spp., known as a cohort of mildly thermophilic or thermotolerant acidophiles, are frequently found in various acidic settings worldwide. They are facultative anaerobes that utilize energy and electrons derived from aerobic oxidation of iron and a wide range of inorganic sulfur compounds for the assimilation of organic and/or inorganic carbon, as well as other anabolic metabolisms (30,37,38). According to the annotation results of the KEGG Automatic Annotation Server (50), the metabolic potentials of Sulfobacillus strains were reconstructed and compared with each other to investigate shared metabolic and species-and/or strain-specific pathways (Table S3).…”

Section: Figmentioning

confidence: 99%

“…To adapt to short-term or longstanding environmental stresses, microbes may have undergone frequent gene turnover. Sulfobacillus spp., which are Gram-positive sporeforming bacteria, are taxonomically affiliated with the order Clostridiales (30). Despite their poorly characterized low abundance compared to the dominant iron-oxidizing Leptospirillum spp.…”

mentioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

“…To date, the genomic features of two S. acidophilus strains (34,41) and three S. thermosulfidooxidans strains (31, 42) have been investigated. Furthermore, the draft genomes of several Sulfobacillus strains have been assembled from metagenomic data (30), including a strain of S. benefaciens, a strain of S. thermosulfidooxidans, and three strains with no cultured representatives. Comparative genomics have yielded valuable insights into the physiological diversity, ecological roles, and genome evolution of environmental microorganisms (9,43,44).…”

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confidence: 99%

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

Zhang

Liu

Liang

et al. 2017

Appl Environ Microbiol

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Recent phylogenomic analysis has suggested that three strains isolated from different copper mine tailings around the world were taxonomically affiliated with Sulfobacillus thermosulfidooxidans. 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.

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Section: Figsupporting

confidence: 69%

Section: Figmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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

Zhang

Liu

Liang

et al. 2017

Appl Environ Microbiol

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A cascade of sulfur transferases delivers sulfur to the sulfur‐oxidizing heterodisulfide reductase‐like complex

Tanabe,

Bach,

D'Ermo

et al. 2024

Protein Science

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A heterodisulfide reductase‐like complex (sHdr) and novel lipoate‐binding proteins (LbpAs) are central players of a wide‐spread pathway of dissimilatory sulfur oxidation. Bioinformatic analysis demonstrate that the cytoplasmic sHdr–LbpA systems are always accompanied by sets of sulfur transferases (DsrE proteins, TusA, and rhodaneses). The exact composition of these sets may vary depending on the organism and sHdr system type. To enable generalizations, we studied model sulfur oxidizers from distant bacterial phyla, that is, Aquificota and Pseudomonadota. DsrE3C of the chemoorganotrophic Alphaproteobacterium Hyphomicrobium denitrificans and DsrE3B from the Gammaproteobacteria Thioalkalivibrio sp. K90mix, an obligate chemolithotroph, and Thiorhodospira sibirica, an obligate photolithotroph, are homotrimers that donate sulfur to TusA. Additionally, the hyphomicrobial rhodanese‐like protein Rhd442 exchanges sulfur with both TusA and DsrE3C. The latter is essential for sulfur oxidation in Hm. denitrificans. TusA from Aquifex aeolicus (AqTusA) interacts physiologically with AqDsrE, AqLbpA, and AqsHdr proteins. This is particularly significant as it establishes a direct link between sulfur transferases and the sHdr–LbpA complex that oxidizes sulfane sulfur to sulfite. In vivo, it is unlikely that there is a strict unidirectional transfer between the sulfur‐binding enzymes studied. Rather, the sulfur transferases form a network, each with a pool of bound sulfur. Sulfur flux can then be shifted in one direction or the other depending on metabolic requirements. A single pair of sulfur‐binding proteins with a preferred transfer direction, such as a DsrE3‐type protein towards TusA, may be sufficient to push sulfur into the sink where it is further metabolized or needed.

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Microbial Approach for Valorization of Mining Wastes and Tailings: An Overview

Costa

Lima

Brito

et al. 2021

Bio-Valorization of Waste

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Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms

Cited by 71 publications

References 143 publications

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

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

A cascade of sulfur transferases delivers sulfur to the sulfur‐oxidizing heterodisulfide reductase‐like complex

Microbial Approach for Valorization of Mining Wastes and Tailings: An Overview

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