Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense

Nunoura, Takuro; Sako, Yoshihiko; Wakagi, Takayoshi; Uchida, Aritsune

doi:10.1099/mic.0.26000-0

Cited by 17 publications

(15 citation statements)

References 89 publications

(62 reference statements)

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“…The opposing expression pattern of the two homologous cytochrome oxidase complexes in P. aerophilum corroborates the expression patterns observed in P. oguniense and provides support for the distinct functions proposed by Nunoura and colleagues (45). In the current study, P. aerophilum SoxB complex genes were upregulated under suboxic conditions, consistent with encoding an oxygen scavenger or sensor (Fig.…”

Section: Resultssupporting

confidence: 75%

“…The regulation of two cytochrome oxidases in the facultative aerobe Pyrobaculum oguniense (45) suggests an analogous specialization in the Pyrobaculum genus: the P. oguniense SoxM-type oxidase was induced under aerobic conditions, whereas the SoxB-type oxidase was induced under anaerobic, thiosulfate-respiring conditions (45). This suggested that the terminal reductase for aerobic growth is the SoxM complex and that the SoxB complex functions in oxygen scavenging with a possible regulatory role.…”

Section: Resultsmentioning

confidence: 91%

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Transcriptional Map of Respiratory Versatility in the Hyperthermophilic Crenarchaeon Pyrobaculum aerophilum

et al. 2009

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Hyperthermophilic crenarchaea in the genus Pyrobaculum are notable for respiratory versatility, but relatively little is known about the genetics or regulation of crenarchaeal respiratory pathways. We measured global gene expression in Pyrobaculum aerophilum cultured with oxygen, nitrate, arsenate and ferric iron as terminal electron acceptors to identify transcriptional patterns that differentiate these pathways. We also compared genome sequences for four closely related species with diverse respiratory characteristics (Pyrobaculum arsenaticum, Pyrobaculum calidifontis, Pyrobaculum islandicum, and Thermoproteus neutrophilus) to identify genes associated with different respiratory capabilities. Specific patterns of gene expression in P. aerophilum were associated with aerobic respiration, nitrate respiration, arsenate respiration, and anoxia. Functional predictions based on these patterns include separate cytochrome oxidases for aerobic growth and oxygen scavenging, a nitric oxide-responsive transcriptional regulator, a multicopper oxidase involved in denitrification, and an archaeal arsenate respiratory reductase. We were unable to identify specific genes for iron respiration, but P. aerophilum exhibited repressive transcriptional responses to iron remarkably similar to those controlled by the ferric uptake regulator in bacteria. Together, these analyses present a genome-scale view of crenarchaeal respiratory flexibility and support a large number of functional and regulatory predictions for further investigation. The complete gene expression data set can be viewed in genomic context with the Archaeal Genome Browser at archaea.ucsc.edu.With the exception of the euryarchaeal halophiles, many archaeal model organisms are either obligate aerobes (e.g., Sulfolobus spp.) or obligate anaerobes (e.g., the Thermococcales), with limited respiratory flexibility. As a consequence, relatively little is known about the genetics, regulation, and enzymology of archaeal respiratory pathways compared to those of bacteria. Species in the genus Pyrobaculum are notable both for respiratory versatility, exemplified by Pyrobaculum aerophilum, and for diversity in respiratory capabilities between closely related species (6,28,29,31,65), presenting a potential model system for investigating respiratory pathways in the crenarchaea.Pyrobaculum species grow optimally at 90 to 100°C and are common constituents of microbial communities in neutral pH geothermal springs and shallow marine hydrothermal vents (39,42,61). Pyrobaculum aerophilum is a facultative chemoautotroph that can use oxygen, nitrate, nitrite, arsenate, selenate, selenite, soluble ferric iron citrate, and insoluble ferric iron oxide as respiratory electron acceptors. The complete genome sequence of P. aerophilum was published in 2002 (23). The genome sequences of four additional Pyrobaculum species (P. arsenaticum, P. calidifontis, P. islandicum, and Thermoproteus neutrophilus [to be reclassified as a true Pyrobaculum]) have recently been completed (T. M. Lowe et al., unpub...

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Section: Resultssupporting

confidence: 75%

Section: Resultsmentioning

confidence: 91%

Transcriptional Map of Respiratory Versatility in the Hyperthermophilic Crenarchaeon Pyrobaculum aerophilum

et al. 2009

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“…Interestingly, the cbaABD genes were markedly up-regulated (fivefold) under anaerobic conditions, suggesting an unusual requirement of this cytochrome oxidase under anoxic conditions (see Discussion). The cox and cyd genes as well as other genes encoding for respiratory enzymes (e.g., equivalents to mitochondrial complex I, II, and III) were not significantly differentially expressed, indicating constitutive regulation as in Pyrobaculum oguniense (21) and/or their requirement during TMAO respiration (e.g., complex I and II equivalents). The transcript levels of genes involved in the citrate cycle were also not significantly differentially expressed; however, the pyruvate:ferredoxin oxidoreductase-encoding porAB genes, channeling carbon and electrons into the citrate cycle, were down-regulated (2.3-fold) during TMAO respiration.…”

Section: Fig 3 Rt-pcr Analysis Of the Dms Operon Inmentioning

confidence: 95%

Genomic Analysis of Anaerobic Respiration in the ArchaeonHalobacteriumsp. Strain NRC-1: Dimethyl Sulfoxide and TrimethylamineN-Oxide as Terminal Electron Acceptors

2005

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We have investigated anaerobic respiration of the archaeal model organism Halobacterium sp. strain NRC-1 by using phenotypic and genetic analysis, bioinformatics, and transcriptome analysis. NRC-1 was found to grow on either dimethyl sulfoxide (DMSO) or trimethylamine N-oxide (TMAO) as the sole terminal electron acceptor, with a doubling time of 1 day. An operon, dmsREABCD, encoding a putative regulatory protein, DmsR, a molybdopterin oxidoreductase of the DMSO reductase family (DmsEABC), and a molecular chaperone (DmsD) was identified by bioinformatics and confirmed as a transcriptional unit by reverse transcriptase PCR analysis. dmsR, dmsA, and dmsD in-frame deletion mutants were individually constructed. Phenotypic analysis demonstrated that dmsR, dmsA, and dmsD are required for anaerobic respiration on DMSO and TMAO. The requirement for dmsR, whose predicted product contains a DNA-binding domain similar to that of the Bat family of activators (COG3413), indicated that it functions as an activator. A cysteine-rich domain was found in the dmsR gene, which may be involved in oxygen sensing. Microarray analysis using a wholegenome 60-mer oligonucleotide array showed that the dms operon is induced during anaerobic respiration. Comparison of dmsR؉ and ⌬dmsR strains by use of microarrays showed that the induction of the dmsEABCD operon is dependent on a functional dmsR gene, consistent with its action as a transcriptional activator. Our results clearly establish the genes required for anaerobic respiration using DMSO and TMAO in an archaeon for the first time.Extremely halophilic archaea (haloarchaea) generally grow heterotrophically under aerobic conditions in hypersaline environments, although they possess facultative anaerobic capabilities (9). These anaerobic capabilities are important since the high salt concentrations and elevated temperatures the organisms encounter, together with high cell densities promoted by aerobic growth and flotation, reduce the availability of molecular oxygen. Although haloarchaeal microorganisms frequently encounter microaerobic or even anoxic conditions, detailed knowledge regarding the extent of haloarchaeal anaerobic growth is still only beginning to emerge. Some species of haloarchaea can carry out primary energy conservation in the absence of molecular oxygen via photophosphorylation (13), substrate-level phosphorylation (13), and anaerobic respiration using nitrate (references 9 and 42 and references therein). In addition, two previous reports described the ability to use dimethyl sulfoxide (DMSO) and trimethylamine-N-oxide (TMAO) (23), and to some extent fumarate (22), as alternative electron acceptors for growth enhancement for some haloarchaea.The molecular basis of the DMSO and TMAO respiratory systems has not been described for any member of the domain Archaea. By contrast, in various bacterial model organisms, DMSO reductases and the related TMAO reductases are well characterized as membrane-bound or periplasmic terminal reductases forming dimethyl sulfide or trimethyla...

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“…Aerobic Pyrobaculum spp. do not contain cyd genes but have heme-Cu oxidase complexes (10)(11)(12). Genes involved in the reduction of oxygen radicals, including superoxide dismutase, peroxiredoxin, and thioredoxin, were identified in P. yellowstonensis strain WP30 (see Table S3 in the supplemental material), indicating tolerance toward reactive oxygen species.…”

Section: Growth Characteristicsmentioning

confidence: 99%

Pyrobaculum yellowstonensis Strain WP30 Respires on Elemental Sulfur and/or Arsenate in Circumneutral Sulfidic Geothermal Sediments of Yellowstone National Park

Jay

Beam

Dohnálková

et al. 2015

Appl Environ Microbiol

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d Thermoproteales (phylum Crenarchaeota) populations are abundant in high-temperature (>70°C) environments of Yellowstone National Park (YNP) and are important in mediating the biogeochemical cycles of sulfur, arsenic, and carbon. The objectives of this study were to determine the specific physiological attributes of the isolate Pyrobaculum yellowstonensis strain WP30, which was obtained from an elemental sulfur sediment (Joseph's Coat Hot Spring [JCHS], 80°C, pH 6.1, 135 M As) and relate this organism to geochemical processes occurring in situ. Strain WP30 is a chemoorganoheterotroph and requires elemental sulfur and/or arsenate as an electron acceptor. Growth in the presence of elemental sulfur and arsenate resulted in the formation of thioarsenates and polysulfides. The complete genome of this organism was sequenced (1.99 Mb, 58% G؉C content), revealing numerous metabolic pathways for the degradation of carbohydrates, amino acids, and lipids. Multiple dimethyl sulfoxide-molybdopterin (DMSO-MPT) oxidoreductase genes, which are implicated in the reduction of sulfur and arsenic, were identified. Pathways for the de novo synthesis of nearly all required cofactors and metabolites were identified. The comparative genomics of P. yellowstonensis and the assembled metagenome sequence from JCHS showed that this organism is highly related (ϳ95% average nucleotide sequence identity) to in situ populations. The physiological attributes and metabolic capabilities of P. yellowstonensis provide an important foundation for developing an understanding of the distribution and function of these populations in YNP.

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Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense

Cited by 17 publications

References 89 publications

Transcriptional Map of Respiratory Versatility in the Hyperthermophilic Crenarchaeon Pyrobaculum aerophilum

Transcriptional Map of Respiratory Versatility in the Hyperthermophilic Crenarchaeon Pyrobaculum aerophilum

Genomic Analysis of Anaerobic Respiration in the ArchaeonHalobacteriumsp. Strain NRC-1: Dimethyl Sulfoxide and TrimethylamineN-Oxide as Terminal Electron Acceptors

Pyrobaculum yellowstonensis Strain WP30 Respires on Elemental Sulfur and/or Arsenate in Circumneutral Sulfidic Geothermal Sediments of Yellowstone National Park

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