Role of 4-Hydroxybutyrate-CoA Synthetase in the CO2 Fixation Cycle in Thermoacidophilic Archaea

Hawkins, Aaron S.; Han, Young-Tak; Bennett, R. Kyle; Adams, Michael W. W.; Kelly, Robert M.

doi:10.1074/jbc.m112.413195

Cited by 31 publications

(41 citation statements)

References 44 publications

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“…Cell extract measurements revealed that the two CoA ligases acting on 3-hydroxypropionate and 4-hydroxybutyrate were ADP-forming ( Fig. 1 and Table 1), whereas aerobic Crenarchaeota possess AMP-forming ligases (19,30,31). Because this issue is important for evaluating the energy efficiency of the cycle, we studied these enzymes in greater detail.…”

Section: Characterization Of Previously Unidentified Enzymes Involvedmentioning

confidence: 99%

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO ₂ fixation

Könneke

Schubert

Brown

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

408

342

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Archaea of the phylum Thaumarchaeota are among the most abundant prokaryotes on Earth and are widely distributed in marine, terrestrial, and geothermal environments. All studied Thaumarchaeota couple the oxidation of ammonia at extremely low concentrations with carbon fixation. As the predominant nitrifiers in the ocean and in various soils, ammonia-oxidizing archaea contribute significantly to the global nitrogen and carbon cycles. Here we provide biochemical evidence that thaumarchaeal ammonia oxidizers assimilate inorganic carbon via a modified version of the autotrophic hydroxypropionate/hydroxybutyrate cycle of Crenarchaeota that is far more energy efficient than any other aerobic autotrophic pathway. The identified genes of this cycle were found in the genomes of all sequenced representatives of the phylum Thaumarchaeota, indicating the environmental significance of this efficient CO 2 -fixation pathway. Comparative phylogenetic analysis of proteins of this pathway suggests that the hydroxypropionate/hydroxybutyrate cycle emerged independently in Crenarchaeota and Thaumarchaeota, thus supporting the hypothesis of an early evolutionary separation of both archaeal phyla. We conclude that high efficiency of anabolism exemplified by this autotrophic cycle perfectly suits the lifestyle of ammonia-oxidizing archaea, which thrive at a constantly low energy supply, thus offering a biochemical explanation for their ecological success in nutrient-limited environments.Nitrosopumilus maritimus | autotrophy

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Section: Characterization Of Previously Unidentified Enzymes Involvedmentioning

confidence: 99%

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO ₂ fixation

Könneke

Schubert

Brown

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

408

342

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“…The Sulfolobales-specific training set included the HHC pathway genes that were significantly upregulated under autotrophic conditions in the transcriptomic analyses of M. sedula (7,14) (see Table S1 in the supplemental material). For the Thermoproteales group, the training set included the DHC pathway genes from the comparative proteome and enzyme activity studies of autotrophically and heterotrophically grown cells of T. neutrophilus (15), including Tneu_0418 to Tneu_0422, Tneu_1797 to Tneu_1795, and Tneu_1204.…”

Section: Bioinformatics Tools and Databasesmentioning

confidence: 99%

“…Indeed, microarray transcriptional response analysis of M. sedula showed significant upregulation of the characteristic HHC enzymes under au-totrophic versus heterotrophic conditions (7,14). However, the mechanism of transcriptional regulation of the HHC pathway in the Sulfolobales is currently unknown.…”

mentioning

confidence: 99%

“…Members of both groups can grow under autotrophic conditions by using carbon dioxide as a carbon source (1,2). Studies of model organisms revealed the presence of two distinct autotrophic carbon dioxide fixation pathways in these crenarchaeal lineages (3)(4)(5)(6)(7)(8)(9)(10)(11)(12). Thermoproteus neutrophilus and other Thermoproteales possess the dicarboxylate/4-hydroxybutyrate cycle (DHC), whereas Metallosphaera sedula and related Sulfolobales use the 3-hydroxypropionate/ 4-hydroxybutyrate cycle (HHC).…”

mentioning

confidence: 99%

“…For functional protein annotations, distant homology to characterized proteins was determined using BLAST against the Swiss-Prot database. Autotrophic pathway enzymes were annotated using a compilation of recent publications (3)(4)(5)(6)(7)(8)(9). Protein domain families were determined by sequence similarity search tools implemented in the Pfam database (25).…”

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confidence: 99%

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Novel Transcriptional Regulons for Autotrophic Cycle Genes in Crenarchaeota

Leyn

Rodionova

et al. 2015

J Bacteriol

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Autotrophic microorganisms are able to utilize carbon dioxide as their only carbon source, or, alternatively, many of them can grow heterotrophically on organics. Different variants of autotrophic pathways have been identified in various lineages of the phylum Crenarchaeota. Aerobic members of the order Sulfolobales utilize the hydroxypropionate-hydroxybutyrate cycle (HHC) to fix inorganic carbon, whereas anaerobic Thermoproteales use the dicarboxylate-hydroxybutyrate cycle (DHC). Knowledge of transcriptional regulation of autotrophic pathways in Archaea is limited. We applied a comparative genomics approach to predict novel autotrophic regulons in the Crenarchaeota. We report identification of two novel DNA motifs associated with the autotrophic pathway genes in the Sulfolobales (HHC box) and Thermoproteales (DHC box). Based on genome context evidence, the HHC box regulon was attributed to a novel transcription factor from the TrmB family named HhcR. Orthologs of HhcR are present in all Sulfolobales genomes but were not found in other lineages. A predicted HHC box regulatory motif was confirmed by in vitro binding assays with the recombinant HhcR protein from Metallosphaera yellowstonensis. For the DHC box regulon, we assigned a different potential regulator, named DhcR, which is restricted to the order Thermoproteales. DhcR in Thermoproteus neutrophilus (Tneu_0751) was previously identified as a DNA-binding protein with high affinity for the promoter regions of two autotrophic operons. The global HhcR and DhcR regulons reconstructed by comparative genomics were reconciled with available omics data in Metallosphaera and Thermoproteus spp. The identified regulons constitute two novel mechanisms for transcriptional control of autotrophic pathways in the Crenarchaeota. IMPORTANCELittle is known about transcriptional regulation of carbon dioxide fixation pathways in Archaea. We previously applied the comparative genomics approach for reconstruction of DtxR family regulons in diverse lineages of Archaea. Here, we utilize similar computational approaches to identify novel regulatory motifs for genes that are autotrophically induced in microorganisms from two lineages of Crenarchaeota and to reconstruct the respective regulons. The predicted novel regulons in archaeal genomes control the majority of autotrophic pathway genes and also other carbon and energy metabolism genes. The HhcR regulon was experimentally validated by DNA-binding assays in Metallosphaera spp. Novel regulons described for the first time in this work provide a basis for understanding the mechanisms of transcriptional regulation of autotrophic pathways in Archaea. The Thermoproteales and Sulfolobales are two groups of thermophilic archaea from the phylum Crenarchaeota. Members of both groups can grow under autotrophic conditions by using carbon dioxide as a carbon source (1, 2). Studies of model organisms revealed the presence of two distinct autotrophic carbon dioxide fixation pathways in these crenarchaeal lineages (3-12). Thermoproteus ne...

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Physiological, metabolic and biotechnological features of extremely thermophilic microorganisms

Counts

Zeldes

Lee

et al. 2017

WIREs Mechanisms of Disease

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The current upper thermal limit for life as we know it is approximately 120°C. Microorganisms that grow optimally at temperatures of 75°C and above are usually referred to as ‘extreme thermophiles’ and include both bacteria and archaea. For over a century, there has been great scientific curiosity in the basic tenets that support life in thermal biotopes on earth and potentially on other solar bodies. Extreme thermophiles can be aerobes, anaerobes, autotrophs, heterotrophs, or chemolithotrophs, and are found in diverse environments including shallow marine fissures, deep sea hydrothermal vents, terrestrial hot springs – basically, anywhere there is hot water. Initial efforts to study extreme thermophiles faced challenges with their isolation from difficult to access locales, problems with their cultivation in laboratories, and lack of molecular tools. Fortunately, because of their relatively small genomes, many extreme thermophiles were among the first organisms to be sequenced, thereby opening up the application of systems biology-based methods to probe their unique physiological, metabolic and biotechnological features. The bacterial genera Caldicellulosiruptor, Thermotoga and Thermus, and the archaea belonging to the orders Thermococcales and Sulfolobales, are among the most studied extreme thermophiles to date. The recent emergence of genetic tools for many of these organisms provides the opportunity to move beyond basic discovery and manipulation to biotechnologically relevant applications of metabolic engineering.

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Role of 4-Hydroxybutyrate-CoA Synthetase in the CO2 Fixation Cycle in Thermoacidophilic Archaea

Cited by 31 publications

References 44 publications

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO ₂ fixation

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO ₂ fixation

Novel Transcriptional Regulons for Autotrophic Cycle Genes in Crenarchaeota

Physiological, metabolic and biotechnological features of extremely thermophilic microorganisms

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Role of 4-Hydroxybutyrate-CoA Synthetase in the CO2 Fixation Cycle in Thermoacidophilic Archaea

Cited by 31 publications

References 44 publications

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO 2 fixation

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO 2 fixation

Novel Transcriptional Regulons for Autotrophic Cycle Genes in Crenarchaeota

Physiological, metabolic and biotechnological features of extremely thermophilic microorganisms

Contact Info

Product

Resources

About

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO ₂ fixation

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO ₂ fixation