Deletion Strains Reveal Metabolic Roles for Key Elemental Sulfur-Responsive Proteins in Pyrococcus furiosus

Bridger, Stephanie L.; Clarkson, Sonya M.; Stirrett, Karen; DeBarry, Megan B.; Lipscomb, Gina L.; Schut, Gerrit J.; Westpheling, Janet; Scott, Robert A.; Adams, Michael W. W.

doi:10.1128/jb.05445-11

Cited by 56 publications

(77 citation statements)

References 29 publications

(48 reference statements)

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“…Another member of the MTH1175 subfamily, sulfur-induced protein A (sipA), was recently found to be expressed in response to elemental sulfur addition in Pyrococcus furiosus (52,53). However, sipA does not appear to be required for growth on elemental sulfur in P. furiosus (54). The CT1277 gene product contains a conserved domain of the helix-turn-helix xenobiotic response element family-like protein superfamily (cl15258).…”

Section: Resultsmentioning

confidence: 99%

Chlorobaculum tepidum TLS Displays a Complex Transcriptional Response to Sulfide Addition

Eddie

Hanson

2013

J Bacteriol

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Chlorobaculum tepidum is a green sulfur bacterium (GSB) that is a model system for phototrophic sulfur oxidation. Despite over 2 decades of research, conspicuous gaps exist in our understanding of its electron donor metabolism and regulation. RNA sequencing (RNA-seq) was used to provide a global picture of the C. tepidum transcriptome during growth on thiosulfate as the sole electron donor and at time points following the addition of sulfide to such a culture. Following sulfide addition, 121 to 150 protein-coding genes displayed significant changes in expression depending upon the time point. These changes included a rapid decrease in expression of thiosulfate and elemental sulfur oxidation genes. Genes and gene loci with increased expression included CT1087, encoding a sulfide:quinone oxidoreductase required for growth in high sulfide concentrations; a polysulfide reductase-like complex operon, psrABC (CT0496 to CT0494); and, surprisingly, a large cluster of genes involved in iron acquisition. Finally, two genes that are conserved as a cassette in anaerobic bacteria and archaea, CT1276 and CT1277, displayed a strong increase in expression. The CT1277 gene product contains a DNA-binding domain, suggesting a role for it in sulfide-dependent gene expression changes.

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Section: Resultsmentioning

confidence: 99%

Chlorobaculum tepidum TLS Displays a Complex Transcriptional Response to Sulfide Addition

Eddie

Hanson

2013

J Bacteriol

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“…kodakarensis and Pyr. furiosus (458,459). It is proposed that Mbx catalyzes the transfer of electrons from reduced ferredoxin to NADP ϩ and, in conjunction with the cytoplasmic coenzyme A (CoASH)-dependent NADPH elemental sulfur reductase (Nsr), catalyzes sulfur reduction.…”

Section: Thermococcales (Pyrococcus Furiosus and Thermococcus Kodakarmentioning

confidence: 99%

Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation

Bräsen

Esser

Rauch

et al. 2014

Microbiol Mol Biol Rev

271

294

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SUMMARY The metabolism of Archaea , the third domain of life, resembles in its complexity those of Bacteria and lower Eukarya . However, this metabolic complexity in Archaea is accompanied by the absence of many “classical” pathways, particularly in central carbohydrate metabolism. Instead, Archaea are characterized by the presence of unique, modified variants of classical pathways such as the Embden-Meyerhof-Parnas (EMP) pathway and the Entner-Doudoroff (ED) pathway. The pentose phosphate pathway is only partly present (if at all), and pentose degradation also significantly differs from that known for bacterial model organisms. These modifications are accompanied by the invention of “new,” unusual enzymes which cause fundamental consequences for the underlying regulatory principles, and classical allosteric regulation sites well established in Bacteria and Eukarya are lost. The aim of this review is to present the current understanding of central carbohydrate metabolic pathways and their regulation in Archaea . In order to give an overview of their complexity, pathway modifications are discussed with respect to unusual archaeal biocatalysts, their structural and mechanistic characteristics, and their regulatory properties in comparison to their classic counterparts from Bacteria and Eukarya . Furthermore, an overview focusing on hexose metabolic, i.e., glycolytic as well as gluconeogenic, pathways identified in archaeal model organisms is given. Their energy gain is discussed, and new insights into different levels of regulation that have been observed so far, including the transcript and protein levels (e.g., gene regulation, known transcription regulators, and posttranslational modification via reversible protein phosphorylation), are presented.

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“…S5 in the supplemental material), and their function is currently unknown. Without the requisite Mbx complex, or a putative elemen-tal sulfur response regulator, SurA (83,84), the role of NSR proteins in sulfur reduction is unclear at this time. Genes similar to either the large subunits of sulfide dehydrogenase (sudA) or glutamate synthase (gltD) were also identified in the four Acidilobus populations (43% amino acid identity to both SudA and GltD characterized in S. marinus [16] and 35% amino acid identity to SudA of Pyrococcus furiosus [85]).…”

Section: Metabolic Potential Of Acidilobus-like Populations From Ynpmentioning

confidence: 99%

Predominant Acidilobus-Like Populations from Geothermal Environments in Yellowstone National Park Exhibit Similar Metabolic Potential in Different Hypoxic Microbial Communities

Jay

Rusch

Tringe

et al. 2014

Appl Environ Microbiol

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c High-temperature (>70°C) ecosystems in Yellowstone National Park (YNP) provide an unparalleled opportunity to study chemotrophic archaea and their role in microbial community structure and function under highly constrained geochemical conditions. Acidilobus spp. (order Desulfurococcales) comprise one of the dominant phylotypes in hypoxic geothermal sulfur sediment and Fe(III)-oxide environments along with members of the Thermoproteales and Sulfolobales. Consequently, the primary goals of the current study were to analyze and compare replicate de novo sequence assemblies of Acidilobus-like populations from four different mildly acidic (pH 3.3 to 6.1) high-temperature (72°C to 82°C) environments and to identify metabolic pathways and/or protein-encoding genes that provide a detailed foundation of the potential functional role of these populations in situ. De novo assemblies of the highly similar Acidilobus-like populations (>99% 16S rRNA gene identity) represent near-complete consensus genomes based on an inventory of single-copy genes, deduced metabolic potential, and assembly statistics generated across sites. Functional analysis of coding sequences and confirmation of gene transcription by Acidilobus-like populations provide evidence that they are primarily chemoorganoheterotrophs, generating acetyl coenzyme A (acetyl-CoA) via the degradation of carbohydrates, lipids, and proteins, and auxotrophic with respect to several external vitamins, cofactors, and metabolites. No obvious pathways or protein-encoding genes responsible for the dissimilatory reduction of sulfur were identified. The presence of a formate dehydrogenase (Fdh) and other protein-encoding genes involved in mixed-acid fermentation supports the hypothesis that Acidilobus spp. function as degraders of complex organic constituents in high-temperature, mildly acidic, hypoxic geothermal systems. Microbial communities in high-temperature geothermal environments provide unique opportunities for determining the physiology of specific populations and for studying geobiological interactions central to a comprehensive functional and evolutionary understanding of thermophilic microorganisms. Acidic, hyperthermal (Ͼ70°C) systems from Yellowstone National Park (YNP) contain significant concentrations of reduced constituents such as H 2 , H 2 S, elemental sulfur, As(III) (e.g., H 3 AsO 3 ), Fe(II), and organic carbon (1, 2), which are often used as electron donors for different chemotrophic microorganisms (3). The oxidation of reduced compounds is coupled with the reduction of terminal electron acceptors, including O 2 , Fe(III), and different sulfur species, generating energy for cellular processes (3, 4). Thermophilic organisms catalyze reactions of geochemical significance (e.g., oxidation-reduction, biomineralization, acidification, and mineral dissolution) that are often orders of magnitude faster than the corresponding abiotic mechanisms (4-7).High-temperature acidic geothermal systems contain several predominant archaeal populations within the phylum Cr...

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Deletion Strains Reveal Metabolic Roles for Key Elemental Sulfur-Responsive Proteins in Pyrococcus furiosus

Cited by 56 publications

References 29 publications

Chlorobaculum tepidum TLS Displays a Complex Transcriptional Response to Sulfide Addition

Chlorobaculum tepidum TLS Displays a Complex Transcriptional Response to Sulfide Addition

Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation

Predominant Acidilobus-Like Populations from Geothermal Environments in Yellowstone National Park Exhibit Similar Metabolic Potential in Different Hypoxic Microbial Communities

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