Professor Robert Poole
West Riding Chair in Microbiology
Tel: 0114 222 4447
Functions and biogenesis of bacterial terminal oxidases, their reactivity with small gaseous ligands and the first evidence that a specific oxidase contributes to nitric oxide tolerance and aerotolerant nitrogen fixation.
Poole’s laboratory was the first to identify correctly the nature of spectrally distinct forms of the alternative E. coli oxidase (cytochrome bd). He also showed the unique functional capabilities of this oxidase, including its remarkably high affinity for oxygen and its role in protecting E. coli from nitric oxide. In the aerobic diazotroph Azotobacter vinelandii, his group demonstrated the critical role of this oxidase in aerotolerant nitrogen fixation in the process known as respiratory protection. This advanced our understanding of the cytochrome bd-type oxidase by demonstrating that its assembly requires a membrane transport complex, CydDC, the first bacterial example of a heterodimeric ABC (ATP-Binding Cassette) transporter homologous to the cystic fibrosis chloride channel (CFTR). He subsequently demonstrated that it exports cysteine and glutathione to the bacterial periplasm and its importance for maintaining the redox environment required for cytochrome assembly in the periplasm.
Discovery of the first flavohaemoglobin gene in any organism, regulation by nitric oxide and pioneering studies of the roles of bacterial haemoglobins in resisting nitric oxide.
In 1991, Poole discovered the flavohaemoglobin gene (hmp) of Escherichia coli, the first to be identified. New understanding of the roles of bacterial haemoglobins was gained by the discovery that the hmp gene was up-regulated by nitric oxide (NO). His group showed that flavohaemoglobin expression represents an adaptive response to the toxic NO generated by macrophage NO synthase and described in detail the reaction of Hmp with oxygen and NO at a peroxidase-like active site. They demonstrated genetically and biochemically that Hmp is required for detoxification of NO both in vitro and within human macrophages. More recently, the flavohaemoglobins of E. coli and Salmonella (and the functionally analogous NO reductase of Neisseria meningitidis) were shown to diminish, via removal of NO, the NO-dependent formation of S-nitrosothiols in macrophages. This led to detailed investigations of transcriptional regulation, which revealed unexpected complexity and showed that the oxygen-sensing Fnr protein also senses NO, with important consequences for global gene regulation. The chemistries of S-nitrosoglutathione and NO suggest that they should exert distinct biological effects: only the former readily transnitrosates thiols, such as homocysteine. These distinctive metabolic consequences were probed using microarray analyses of chemostat-grown cells, which confirmed that S-nitrosoglutathione, but not NO, nitrosates cellular targets, whereas NO targets metalloproteins, including Fnr and other metal-containing transcription factors. We are currently interested in the interactions between NO, oxygen and antibiotics.
Comprehensive systems biology approaches to a new understanding of the energy metabolism of a model organism, Escherichia coli.
When oxygen is available, Escherichia coli switches to aerobic respiration to achieve redox balance and optimal energy conservation by proton translocation linked to electron transfer. The switch between fermentative and aerobic respiratory growth is driven by extensive changes in gene expression and protein synthesis, resulting in global changes in metabolic fluxes and metabolite concentrations. This oxygen response is determined by the interaction of global and local genetic regulatory mechanisms, as well as by enzymatic regulation. A systems-level understanding of the oxygen response of E. coli requires the integrated interpretation of experimental data that are pertinent to the multiple levels of organisation that mediate the response. In the pan-European venture Systems Biology of Microorganisms (SysMO) and specifically within the project Systems Understanding of Microbial Oxygen Metabolism (SUMO), regulator activities, gene expression, metabolite levels and metabolic flux datasets were obtained using a standardised and reproducible chemostat-based experimental system. These different types and qualities of data were integrated using mathematical models. We revealed a much more detailed picture of the aerobic-anaerobic response, especially for the environmentally critical microaerobic range that is located between unlimited oxygen availability and anaerobiosis.
Carbon monoxide binding to haem proteins to understand oxidases in vivo and the physiological, pathological and antibacterial consequences of bacterial exposure to carbon monoxide-releasing compounds.
In biology and medicine, carbon monoxide (CO) is now recognised as a second, vital signaling molecule (or ‘gasotransmitter’), implicated as a neurotransmitter and in diverse cytoprotective roles. The mode(s) of action of CO remains unclear, mainly due to the difficulty of delivering and manipulating CO in biological systems. The distribution of CO in therapy is difficult to tune, while application to localised sites, e.g. of microbial infection, is virtually impossible. Therefore, Poole’s group has started to evaluate CO-Releasing Molecules (CORMs, transition metal carbonyl complexes) as easy-to-handle molecular storage and carrier systems for CO. Its antibacterial activities are described in recent papers that show that CO generated from CORM-3 [Ru(CO)3Cl(glycinate)] is an effective antibacterial agent and exerts global effects on gene expression in E. coli. CORM-3 has been shown also to be an effective antibacterial agent against Pseudomonas aeruginosa and decreased bacterial counts in the spleen, increasing survival in immunocompetent and immunosuppressed mice following P. aeruginosa bacteraemia. Current work focuses on novel light-activated CORMs and ruthenium complexes with potential as antimicrobials
First evidence for the selective action of a gasotransmitter – hydrogen sulphide – on bacterial respiratory systems.
Hydrogen sulfide (H2S) impairs mitochondrial respiration by potently inhibiting cytochrome c oxidase. Since many prokaryotes, including Escherichia coli, generate H2S and encounter high H2S levels particularly in the human gut, we tested whether bacteria can sustain sulfide-resistant O2-dependent respiration. E. coli has three respiratory oxidases, the cyanide-sensitive heme-copper bo3 enzyme and two bd oxidases much less sensitive to cyanide. Working on the isolated enzymes, we found that, whereas the bo3 oxidase is potently inhibited by sulfide, both bd oxidases are insensitive to sulfide up to 58 μM. In E. coli respiratory mutants, both O2-consumption and aerobic growth proved to be severely impaired by sulfide when respiration was sustained by the bo3 oxidase alone, but unaffected by ≤ 200 μM sulfide when either bd enzyme acted as the only terminal oxidase. Accordingly, wild-type E. coli showed sulfide-insensitive respiration and growth under O2-limiting conditions favouring the expression of bd oxidases. Sulfide and cyanide affected bacterial cell respiration equally, causing either no effect or identical inhibition, depending on the tested strain and growth conditions. Thus cytochrome bd oxidases promote sulfide-resistant O2-consumption and growth in E. coli and possibly other bacteria.
Microbiology, physiology, respiration, oxidative and nitrosative stress, NO and CO, antimicrobial compounds and antibiotics
Level 3 Modules
MBB335 Bacterial Pathogenicity
Honours and Distinctions
- Using Nanoscopy To Probe the Biological Activity of Antimicrobial Leads That Display Potent Activity against Pathogenic, Multidrug Resistant, Gram-Negative Bacteria. ACS Nano, 13(5), 5133-5146. View this article in WRRO
- Temporal metabolic partitioning of the yeast and protist cellular networks: the cell is a global scale-invariant (fractal or self-similar) multioscillator. Journal of Biomedical Optics, 24(05). View this article in WRRO
- Do nitric oxide, carbon monoxide and hydrogen sulfide really qualify as 'gasotransmitters' in bacteria?. Biochemical Society transactions. View this article in WRRO
- A thiol-reactive Ru(II) ion, not CO release, underlies the potent antimicrobial and cytotoxic properties of CO-releasing molecule-3. Redox Biology, 18, 114-123. View this article in WRRO
- The Antimicrobial Activity of Mononuclear Ruthenium(II) Complexes Containing the dppz Ligand. ChemPlusChem, 83(7), 643-650. View this article in WRRO
- Synthesis, isomerisation and biological properties of mononuclear ruthenium complexes containing the bis[4(4′-methyl-2,2′-bipyridyl)]-1,7-heptane ligand. Dalton Transactions, 47(7), 2422-2434. View this article in WRRO
- Coexistence of multiple globin genes conferring protection against nitrosative stress to the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Nitric Oxide, 73, 39-51. View this article in WRRO
- Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability. Environmental Microbiology, 19(10), 4326-4348. View this article in WRRO
- A manganese photosensitive tricarbonyl molecule [Mn(CO)3(tpa-κ(3)N)]Br enhances antibiotic efficacy in a multi-drug-resistant Escherichia coli.. Microbiology. View this article in WRRO
- The Broad-Spectrum Antimicrobial Potential of [Mn(CO)4(S2CNMe(CH2CO2H))], a Water-Soluble CO-Releasing Molecule (CORM-401): Intracellular Accumulation, Transcriptomic and Statistical Analyses, and Membrane Polarization. Antioxidants & Redox Signaling. View this article in WRRO
- Listeria monocytogenes Has Both Cytochrome bd-Type and Cytochrome aa3-Type Terminal Oxidases, Which Allow Growth at Different Oxygen Levels, and Both Are Important in Infection. Infection and Immunity, 85(11). View this article in WRRO
- The Microbiology of Ruthenium Complexes. Advances in Microbial Physiology.
- Preface. Advances in microbial physiology, 70, XI-XII.
- The cytochrome bd-I respiratory oxidase augments survival of multidrug-resistant Escherichia coli during infection. Scientific Reports, 6, 35285-35285. View this article in WRRO
- Sulfide-resistant O 2 respiration: A new role for bacterial bd -type terminal oxidases. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1857, e85-e86.
- Sulfide-resistant O 2 respiration: A new role for bacterial bd -type terminal oxidases. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1857, e13-e14.
- Carbon Monoxide Gas Is Not Inert, but Global, in Its Consequences for Bacterial Gene Expression, Iron Acquisition, and Antibiotic Resistance. Antioxidants & Redox Signaling, 24(17), 1013-1028. View this article in WRRO
- The roles of the hybrid cluster protein, Hcp and its reductase, Hcr, in high affinity nitric oxide reduction that protects anaerobic cultures of Escherichia coli against nitrosative stress. Molecular Microbiology, 100(5), 877-892.
- Antimicrobial Activity of the Manganese Photoactivated Carbon Monoxide-Releasing Molecule [Mn(CO) 3 (tpa-κ 3 N )] + Against a Pathogenic Escherichia coli that Causes Urinary Infections. Antioxidants & Redox Signaling, 24(14), 765-780. View this article in WRRO
- Evidence for Fast Electron Transfer between the High-Spin Haems in Cytochrome bd-I from Escherichia coli. PLOS ONE, 11(5), e0155186-e0155186. View this article in WRRO
- A bacterial oxidase like no other?. Science, 352(6285), 518-519. View this article in WRRO
- The Terminal Oxidase Cytochrome bd Promotes Sulfide-resistant Bacterial Respiration and Growth. Scientific Reports, 6. View this article in WRRO
- CydDC-mediated reductant export in Escherichia coli controls the transcriptional wiring of energy metabolism and combats nitrosative stress. Biochemical Journal, 473(6), 693-701. View this article in WRRO
- Analysis of transcript changes in a heme-deficient mutant of Escherichia coli in response to CORM-3 [Ru(CO)3Cl(glycinate)]. Genomics Data, 5, 231-234.
- CO-releasing Metal Carbonyl Compounds as Antimicrobial Agents in the Post-antibiotic Era. Journal of Biological Chemistry, 290(31), 18999-19007. View this article in WRRO
- Adaptation of anaerobic cultures of Escherichia coliK-12 in response to environmental trimethylamine-N-oxide. Environmental Microbiology, 17(7), 2477-2491. View this article in WRRO
- CO-Releasing Molecules Have Nonheme Targets in Bacteria: Transcriptomic, Mathematical Modeling and Biochemical Analyses of CORM-3 [Ru(CO) 3 Cl(glycinate)] Actions on a Heme-Deficient Mutant of Escherichia coli. Antioxidants & Redox Signaling, 23(2), 148-162. View this article in WRRO
- The CydDC Family of Transporters and Their Roles in Oxidase Assembly and Homeostasis, 1-53.
- Carbon Monoxide-releasing Molecule-3 (CORM-3; Ru(CO)3Cl(Glycinate)) as a Tool to Study the Concerted Effects of Carbon Monoxide and Nitric Oxide on Bacterial Flavohemoglobin Hmp. Journal of Biological Chemistry, 289(43), 29471-29482.
- Structure and function of the bacterial heterodimeric ABC transporter CydDC: stimulation of ATPase activity by thiol and heme compounds.. J Biol Chem, 289(33), 23177-23188. View this article in WRRO
- Interaction of the carbon monoxide-releasing molecule Ru(CO)3Cl(glycinate) (CORM-3) with Salmonella enterica serovar Typhimurium: in situ measurements of carbon monoxide binding by integrating cavity dual-beam spectrophotometry. Microbiology, 160(12), 2771-2779.
- Fast electron transfer between hemes and binding of internal ligand to heme d upon photodissociation of CO from cytochrome bd oxidase. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1837, e96-e96.
- Structure of the Zymomonas mobilis respiratory chain: oxygen affinity of electron transport and the role of cytochrome c peroxidase.. Microbiology, 160(Pt 9), 2045-2052.
- Towards a systems level understanding of the oxygen response of Escherichia coli.. Adv Microb Physiol, 64, 65-114.
- Introducing [Mn(CO)(3)(tpa-kappa N-3)](+) as a novel photoactivatable CO-releasing molecule with well-defined iCORM intermediates - synthesis, spectroscopy, and antibacterial activity. DALTON TRANSACTIONS, 43(26), 9986-9997.
- A mathematical model of metabolism and regulation provides a systems-level view of how Escherichia coli responds to oxygen.. Front Microbiol, 5, 124. View this article in WRRO
- Microsecond time-resolved absorption spectroscopy used to study CO compounds of cytochrome bd from Escherichia coli.. PLoS One, 9(4), e95617. View this article in WRRO
- Agent-based modeling of oxygen-responsive transcription factors in Escherichia coli.. PLoS Comput Biol, 10(4), e1003595. View this article in WRRO
- Gasotransmitters, poisons, and antimicrobials: it's a gas, gas, gas!. F1000Prime Rep, 5, 28. View this article in WRRO
- Nitric oxide reactivities of the two globins of the foodborne pathogen Campylobacter jejuni: roles in protection from nitrosative stress and analysis of potential reductants.. Nitric Oxide, 34, 65-75.
- Cytochrome bd-I in Escherichia coli is less sensitive than cytochromes bd-II or bo'' to inhibition by the carbon monoxide-releasing molecule, CORM-3: N-acetylcysteine reduces CO-RM uptake and inhibition of respiration.. Biochim Biophys Acta, 1834(9), 1693-1703. View this article in WRRO
- Bacterial and archaeal globins - a revised perspective.. Biochim Biophys Acta, 1834(9), 1789-1800.
- Analysis of the bacterial response to Ru(CO)3Cl(Glycinate) (CORM-3) and the inactivated compound identifies the role played by the ruthenium compound and reveals sulfur-containing species as a major target of CORM-3 action.. Antioxid Redox Signal, 19(17), 1999-2012.
- Antarctic bacterial haemoglobin and its role in the protection against nitrogen reactive species.. Biochim Biophys Acta, 1834(9), 1923-1931.
- Microbial eukaryote globins, 63, 391-446.
- Ru(CO)3Cl(Glycinate) (CORM-3): a carbon monoxide-releasing molecule with broad-spectrum antimicrobial and photosensitive activities against respiration and cation transport in Escherichia coli.. Antioxid Redox Signal, 19(5), 497-509. View this article in WRRO
- Do globins in microaerophilic Campylobacter jejuni confer nitrosative stress tolerance under oxygen limitation?. Antioxid Redox Signal, 18(4), 424-431.
- Nitrosothiols in bacterial pathogens and pathogenesis.. Antioxid Redox Signal, 18(3), 309-322.
- Antibacterial effects of carbon monoxide.. Curr Pharm Biotechnol, 13(6), 760-768.
- Systems analysis of transcription factor activities in environments with stable and dynamic oxygen concentrations.. Open Biol, 2(7), 120091. View this article in WRRO
- Sulfite species enhance carbon monoxide release from CO-releasing molecules: implications for the deoxymyoglobin assay of activity.. Anal Biochem, 427(1), 36-40.
- Electron transport and oxidative stress in Zymomonas mobilis respiratory mutants. Archives of Microbiology, 1-11.
- Dynamics of a starvation-to-surfeit shift: a transcriptomic and modelling analysis of the bacterial response to zinc reveals transient behaviour of the Fur and SoxS regulators.. Microbiology, 158(Pt 1), 284-292.
- Reprogramming of escherichia coli K-12 metabolism during the initial phase of transition from an anaerobic to a micro-aerobic environment. PLoS ONE, 6(9). View this article in WRRO
- The carbon monoxide-releasing molecule, CORM-3 (RU(CO)(3) CL(glycinate)), targets respiration and oxidases in Campylobacter jejuni, generating hydrogen peroxide.. IUBMB Life, 63(5), 363-371.
- Transcript profiling and inference of Escherichia coli K-12 ArcA activity across the range of physiologically relevant oxygen concentrations.. J Biol Chem, 286(12), 10147-10154.
- Globin-mediated nitric oxide detoxification in the foodborne pathogenic bacterium Campylobacter jejuni proceeds via a dioxygenase or denitrosylase mechanism. Nitric Oxide - Biology and Chemistry, 25(2), 229-233.
- Role of the distal hydrogen-bonding network in regulating oxygen affinity in the truncated hemoglobin III from campylobacter jejuni. Biochemistry, 50(19), 3946-3956.
- The diversity of microbial responses to nitric oxide and agents of nitrosative stress close cousins but not identical twins.. Adv Microb Physiol, 59, 135-219.
- The NO-responsive hemoglobins of Campylobacter jejuni: concerted responses of two globins to NO and evidence in vitro for globin regulation by the transcription factor NssR.. Nitric Oxide, 25(2), 234-241.
- Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on L-lactate.. Environ Microbiol, 13(1), 48-61.
- Peroxynitrite stress is exacerbated by flavohaemoglobin-derived oxidative stress in Salmonella Typhimurium and is relieved by nitric oxide.. Microbiology, 156(Pt 12), 3556-3565.
- Peroxynitrite toxicity in Escherichia coli K12 elicits expression of oxidative stress responses and protein nitration and nitrosylation.. J Biol Chem, 285(27), 20724-20731.
- The single-domain globin from the pathogenic bacterium Campylobacter jejuni: novel D-helix conformation, proximal hydrogen bonding that influences ligand binding, and peroxidase-like redox properties.. J Biol Chem, 285(17), 12747-12754.
- KatG from Salmonella typhimurium is a peroxynitritase.. FEBS Lett, 584(8), 1628-1632.
- Compensations for diminished terminal oxidase activity in Escherichia coli: cytochrome bd-II-mediated respiration and glutamate metabolism.. J Biol Chem, 285(24), 18464-18472.
- Role of flavohemoglobin in combating nitrosative stress in uropathogenic Escherichia coli - Implications for urinary tract infection. Microbial Pathogenesis, 49(3), 59-66.
- Bacterial nitric oxide detoxification prevents host cell S-nitrosothiol formation: a novel mechanism of bacterial pathogenesis.. FASEB J, 24(1), 286-295.
- Carbon Monoxide in Biology and Microbiology: Surprising Roles for the "Detroit Perfume", 56, 85-167.
- A novel method for exploring elemental composition of microbial communities: laser ablation-inductively coupled plasma-mass spectrometry of intact bacterial colonies.. J Microbiol Methods, 79(3), 329-335.
- Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins.. J Biol Chem, 284(27), 18377-18389. View this article in WRRO
- A carbon monoxide-releasing molecule (CORM-3) exerts bactericidal activity against Pseudomonas aeruginosa and improves survival in an animal model of bacteraemia.. FASEB J, 23(4), 1023-1031.
- Carbon monoxide-releasing antibacterial molecules target respiration and global transcriptional regulators.. J Biol Chem, 284(7), 4516-4524. View this article in WRRO
- Cytochrome bd confers nitric oxide resistance to Escherichia coli. NAT CHEM BIOL, 5(2), 94-96.
- A Carbon Monoxide-Releasing Molecule (CORM-3) Exerts Bactericidal Activity Against Pseudomonas aeruginosa. AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE, 179.
- Expression of the PitA phosphate/metal transporter of Escherichia coli is responsive to zinc and inorganic phosphate levels.. FEMS Microbiol Lett, 289(2), 219-224.
- Oxygen- and NssR-dependent globin expression and enhanced iron acquisition in the response of campylobacter to nitrosative stress.. J Biol Chem, 283(42), 28413-28425.
- Nitric oxide homeostasis in Salmonella typhimurium: roles of respiratory nitrate reductase and flavohemoglobin.. J Biol Chem, 283(17), 11146-11154.
- Characterization of the Escherichia coli K-12 ydhYVWXUT operon: regulation by FNR, NarL and NarP.. Microbiology, 154(Pt 2), 608-618.
- Coherence spectroscopy investigations of the low-frequency vibrations of heme: Effects of protein-specific perturbations. Journal of the American Chemical Society, 130(15), 5231-5244.
- NADH dehydrogenase deficiency results in low respiration rate and improved aerobic growth of Zymomonas mobilis. Microbiology, 154(3), 989-994.
- Hemoglobins from Mycobacterium tuberculosis and Campylobacter jejuni: A Comparative Study with Resonance Raman Spectroscopy, 437, 255-286.
- Expression and purification of Cgb and Ctb, the NO-inducible globins of the foodborne bacterial pathogen C. jejuni.. Methods Enzymol, 436, 289-302.
- Microbial responses to nitric oxide and nitrosative stress: growth, "omic," and physiological methods.. Methods Enzymol, 437, 499-519.
- A survey of methods for the purification of microbial flavohemoglobins.. Methods Enzymol, 436, 169-186.
- The hmp gene encoding the NO-inducible flavohaemoglobin in Escherichia coli confers a protective advantage in resisting killing within macrophages, but not in vitro: links with swarming motility.. Gene, 398(1-2), 62-68.
- Metabolism of nitric oxide by Neisseria meningitidis modifies release of NO-regulated cytokines and chemokines by human macrophages.. Microbes Infect, 9(8), 981-987.
- NsrR: a key regulator circumventing Salmonella enterica serovar Typhimurium oxidative and nitrosative stress in vitro and in IFN-gamma-stimulated J774.2 macrophages.. Microbiology, 153(Pt 6), 1756-1771.
- The Escherichia coli yhjA gene, encoding a predicted cytochrome c peroxidase, is regulated by FNR and OxyR.. Microbiology, 153(Pt 5), 1499-1509.
- NikA binds heme: a new role for an Escherichia coli periplasmic nickel-binding protein.. Biochemistry, 46(17), 5030-5037.
- Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components.. J Biol Chem, 282(15), 11230-11237.
- Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S nitrosation.. J Bacteriol, 189(5), 1845-1855.
- Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type.. J Bacteriol, 189(5), 1604-1615.
- Structural and functional properties of a truncated hemoglobin from a food-borne pathogen Campylobacter jejuni. Journal of Biological Chemistry, 282(18), 13627-13636.
- Multiple regulators of the Flavohaemoglobin (hmp) gene of Salmonella enterica serovar Typhimurium include RamA, a transcriptional regulator conferring the multidrug resistance phenotype. Archives of Microbiology, 187(1), 67-77.
- Structural and functional properties of a single domain hemoglobin from the food-borne pathogen Campylobactor jejuni. Journal of Biological Chemistry, 282(35), 25917-25928.
- Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress.. Mol Microbiol, 63(2), 575-590.
- Escherichia coli transcriptome dynamics during the transition from anaerobic to aerobic conditions.. J Biol Chem, 281(38), 27806-27815.
- Purification and spectroscopic characterization of Ctb, a group III truncated hemoglobin implicated in oxygen metabolism in the food-borne pathogen Campylobacter jejuni.. Biochemistry, 45(19), 6003-6011.
- Respiratory behaviour of a Zymomonas mobilis adhB::kanr mutant supports the hypothesis of two alcohol dehydrogenase isoenzymes catalysing opposite reactions. FEBS Letters, 580(21), 5084-5088.
- A truncated haemoglobin implicated in oxygen metabolism by the microaerophilic food-borne pathogen Campylobacter jejuni.. Microbiology, 151(Pt 12), 4079-4091.
- A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm.. J Biol Chem, 280(37), 32254-32261.
- Transcriptional responses of Escherichia coli to S-nitrosoglutathione under defined chemostat conditions reveal major changes in methionine biosynthesis.. J Biol Chem, 280(11), 10065-10072.
- Nitric oxide and nitrosative stress tolerance in bacteria.. Biochem Soc Trans, 33(Pt 1), 176-180.
- Genome-wide transcriptional response of chemostat-cultured Escherichia coli to zinc.. J Bacteriol, 187(3), 1124-1134.
- Flavohaemoglobin HmpX from Erwinia chrysanthemi confers nitrosative stress tolerance and affects the plant hypersensitive reaction by intercepting nitric oxide produced by the host. Plant Journal, 43(2), 226-237.
- NssR, a member of the Crp-Fnr superfamily from Campylobacter jejuni, regulates a nitrosative stress-responsive regulon that includes both a single-domain and a truncated haemoglobin. Molecular Microbiology, 57(3), 735-750.
- Escherichia coli Hmp, an "oxygen-binding flavohaemoprotein", produces superoxide anion and self-destructs.. Arch Microbiol, 182(2-3), 193-203.
- Membrane topology and mutational analysis of Escherichia coli CydDC, an ABC-type cysteine exporter required for cytochrome assembly.. Microbiology, 150(Pt 10), 3415-3427.
- The bacterial terminal cytochrome bd oxidase and nitric oxide. COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY B-BIOCHEMISTRY & MOLECULAR BIOLOGY, 139(1), 145-146.
- Speciation of protein-bound trace elements by gel electrophoresis and atomic spectrometry.. Electrophoresis, 25(15), 2469-2477.
- Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide. FEBS Letters, 576(1-2), 201-204.
- Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli. Journal of Bacteriology, 186(16), 5332-5341.
- Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp.. J Biol Chem, 278(34), 31584-31592.
- Global iron-dependent gene regulation in Escherichia coli - A new mechanism for iron homeostasis. J BIOL CHEM, 278(32), 29478-29486.
- Detection and characterization of zinc- and cadmium-binding proteins in Escherichia coli by gel electrophoresis and laser ablation-inductively coupled plasma-mass spectrometry.. Anal Biochem, 318(1), 30-38.
- The paradoxical cyanide-stimulated respiration of Zymomonas mobilis: Cyanide sensitivity of alcohol dehydrogenase (ADH II). Microbiology, 149(7), 1739-1744.
- Copper biosorption by Pseudomonas cepacia and other strains. World Journal of Microbiology and Biotechnology, 19(2), 117-121.
- Differential pulse polarography: A method for the direct study of biosorption of metal ions by live bacteria from mixed metal solutions. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 84(2), 99-107.
- Flavohemoglobin Hmp, but not its individual domains, confers protection from respiratory inhibition by nitric oxide in Escherichia coli. Journal of Biological Chemistry, 278(37), 34975-34982.
- Microbial globins.. Adv Microb Physiol, 47, 255-310.
- Cysteine is exported from the Escherichia coli cytoplasm by CydDC, an ATP-binding cassette-type transporter required for cytochrome assembly.. J Biol Chem, 277(51), 49841-49849.
- A novel haem compound accumulated in Escherichia coli overexpressing the cydDC operon, encoding an ABC-type transporter required for cytochrome assembly.. Arch Microbiol, 178(5), 358-369.
- Flavohemoglobin Hmp protects Salmonella enterica serovar typhimurium from nitric oxide-related killing by human macrophages.. Infect Immun, 70(8), 4399-4405.
- Nitric oxide releases intracellular zinc from prokaryotic metallothionein in Escherichia coli.. FEMS Microbiol Lett, 213(1), 121-126.
- NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp.. EMBO J, 21(13), 3235-3244.
- Structure and function relationships in bacterial hemoglobins. JOURNAL OF INORGANIC BIOCHEMISTRY, 86(1), 487-487.
- Interaction of cytochrome bd with carbon monoxide at low and room temperatures: evidence that only a small fraction of heme b595 reacts with CO.. J Biol Chem, 276(25), 22095-22099.
- Enzymatic removal of nitric oxide catalyzed by cytochrome c' in Rhodobacter capsulatus.. J Bacteriol, 183(10), 3050-3054.
- Taenia crassiceps metacestodes have cytochrome oxidase aa(3) but not cytochrome o functioning as terminal oxidase. MOLECULAR AND BIOCHEMICAL PARASITOLOGY, 114(1), 103-109.
- Alleviation of aluminum toxicity to Rhizobium leguminosarum bv. viciae by the hydroxamate siderophore vicibactin. BIOMETALS, 14(1), 59-66.
- Escherichia coli flavohaemoglobin (Hmp) with equistoichiometric FAD and haem contents has a low affinity for dioxygen in the absence or presence of nitric oxide. Biochemical Journal, 353(2), 207-213.
- Escherichia coli flavohaemoglobin (Hmp) with equistoichiometric FAD and haem contents has a low affinity for dioxygen in the absence or presence of nitric oxide.. Biochem J, 353(Pt 2), 207-213.
- Biosynthesis of poly-beta-hydroxybutyrate (PHB) is controlled by CydR (Fnr) in the obligate aerobe Azotobacter vinelandii.. FEMS Microbiol Lett, 194(2), 215-220.
- Biosynthesis of poly-Î²-hydroxybutyrate (PHB) is controlled by CydR (Fnr) in the obligate aerobeAzotobacter vinelandii. FEMS Microbiology Letters, 194(2), 215-220.
- Resonance Raman studies of the catalytic site of flavohemoglobin. BIOPHYSICAL JOURNAL, 80(1), 290A-290A.
- Flavohemoglobin, a Globin with a Peroxidase-like Catalytic Site. Journal of Biological Chemistry, 276(10), 7272-7277.
- Escherichia coli flavohaemoglobin (Hmp) with equistoichiometric FAD and haem contents has a low affinity for dioxygen in the absence or presence of nitric oxide. Biochemical Journal, 353(2), 207-213.
- Flavohemoglobin Hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo' or bd, from nitric oxide.. J Biol Chem, 275(46), 35868-35875.
- Cd(II), Pb(II) and Zn(II) ions regulate expression of the metal-transporting P-type ATPase ZntA in Escherichia coli.. FEBS Lett, 473(1), 67-70.
- New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress.. Mol Microbiol, 36(4), 775-783.
- Mutation of cytochrome bd quinol oxidase results in reduced stationary phase survival, iron deprivation, metal toxicity and oxidative stress in Azotobacter vinelandii.. FEMS Microbiol Lett, 185(1), 71-77.
- Ubiquinone limits oxidative stress in Escherichia coli.. Microbiology, 146 ( Pt 4), 787-796.
- Cytochrome c' from Rhodobacter capsulatus confers increased resistance to nitric oxide.. J Bacteriol, 182(5), 1442-1447.
- Regulation of cytochrome bd expression in the obligate aerobe Azotobacter vinelandii by CydR (Fnr). Sensitivity to oxygen, reactive oxygen species, and nitric oxide.. J Biol Chem, 275(7), 4679-4686.
- Oxidase and periplasmic cytochrome assembly in Escherichia coli K-12: CydDC and CcmAB are not required for haem-membrane association.. Microbiology, 146 ( Pt 2), 527-536.
- Roles of respiratory oxidases in protecting Escherichia coli K12 from oxidative stress. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 78(1), 23-31.
- Cyanide inhibits respiration yet stimulates aerobic growth of Zymomonas mobilis. Microbiology, 146(6), 1259-1266.
- Evidence for the transport of zinc(II) ions via the Pit inorganic phosphate transport system in Escherichia coli. FEMS Microbiology Letters, 184(2), 231-235.
- Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation.. Adv Microb Physiol, 43, 165-224.
- Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management.. Microbiology, 145 ( Pt 8), 1817-1830.
- Anoxic function for the Escherichia coli flavohaemoglobin (Hmp): reversible binding of nitric oxide and reduction to nitrous oxide.. FEBS Lett, 445(2-3), 389-394.
- The flavohemoglobin of Escherichia coli confers resistance to a nitrosating agent, a "Nitric oxide Releaser," and paraquat and is essential for transcriptional responses to oxidative stress.. J Biol Chem, 274(2), 748-754.
- An unusual cytochrome o'-type cytochrome c oxidase in a Bacillus cereus cytochrome a
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- CtaA of Staphylococcus aureus is required for starvation survival, recovery, and cytochrome biosynthesis.. J Bacteriol, 181(2), 501-507.
- A factor produced by Escherichia coli K-12 inhibits the growth of E. coli mutants defective in the cytochrome bd quinol oxidase complex: enterochelin rediscovered.. Microbiology, 144 ( Pt 12), 3297-3308.
- Response of the NAD(P)H-oxidising flavohaemoglobin (Hmp) to prolonged oxidative stress and implications for its physiological role in Escherichia coli.. FEMS Microbiol Lett, 166(2), 219-223.
- A novel mechanism for upregulation of the Escherichia coli K-12 hmp (flavohaemoglobin) gene by the 'NO releaser', S-nitrosoglutathione: nitrosation of homocysteine and modulation of MetR binding to the glyA-hmp intergenic region.. Mol Microbiol, 29(4), 1101-1112.
- The nrfEFG gene products are required for the activity of the cytochrome c552 nitrite reductase from Escherichia coli. Biochemical Society Transactions, 26(3), S216-S216.
- Involvement of products of the nrfEFG genes in the covalent attachment of haem c to a novel cysteine-lysine motif in the cytochrome c
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- Requirement for ubiquinone downstream of cytochrome(s) b in the oxygen-terminated respiratory chains of Escherichia coli K-12 revealed using a null mutant allele of ubiCA. Microbiology, 144(2), 361-373.
- Identification and characterization of aarF, a locus required for production of ubiquinone in Providencia stuartii and Escherichia coli and for expression of 2'-N-acetyltransferase in P. stuartii. Journal of Bacteriology, 180(1), 128-135.
- Membrane D-lactate oxidase in Zymomonas mobilis: Evidence for a branched respiratory chain. FEMS Microbiology Letters, 168(1), 91-97.
- Redox poise and oxygenation of cytochrome bd in the diazotroph Azotobacter vinelandii assessed in vivo using diode-array reflectance spectrophotometry. Microbiology, 144(8), 2271-2280.
- Electron donation to the flavoprotein NifL, a redox-sensing transcriptional regulator. Biochemical Journal, 332(2), 413-419.
- Bacterial flavohaemoglobins: a consensus sequence and identification of a discrete enterobacterial group and of further bacterial globins.. FEMS Microbiol Lett, 155(2), 179-184.
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- Aerobic and anaerobic regulation of the ubiCA operon, encoding enzymes for the first two committed steps of ubiquinone biosynthesis in Escherichia coli.. FEBS Lett, 414(2), 373-376.
- The cydR gene product, required for regulation of cytochrome bd expression in the obligate aerobe Azotobacter vinelandii, is an Fnr-like protein.. Microbiology, 143 ( Pt 7), 2197-2207.
- Respiratory protection of nitrogenase activity in Azotobacter vinelandii--roles of the terminal oxidases.. Biosci Rep, 17(3), 303-317.
- Roles of RpoS (sigmaS), IHF and ppGpp in the expression of the hmp gene encoding the flavohemoglobin (Hmp) of Escherichia coli K-12.. Mol Gen Genet, 254(5), 599-603.
- Paraquat regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12 is SoxRS independent but modulated by sigma S.. J Bacteriol, 179(10), 3164-3170.
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- Zinc(II) tolerance in Escherichia coli K-12: Evidence that the zntA gene (o732) encodes a cation transport ATPase. Molecular Microbiology, 25(5), 883-891.
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- Metal-microbe interactions: Contemporary approaches. Advances in Microbial Physiology, 38, 231-243.
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- Bacterial Respiratory Chains, Encyclopedia of Biophysics (pp. 1-7). Springer Berlin Heidelberg
- Bacterial Globins, Encyclopedia of Biophysics (pp. 1-6). Springer Berlin Heidelberg
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- Bacterial Globins, Encyclopedia of Biophysics (pp. 156-160). Springer Berlin Heidelberg
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Conference proceedings papers
- Cytochrome bd and bacterial respiration in sulfide rich environments. Free Radical Biology and Medicine, Vol. 120 (pp S163-S164)
- Cytochrome bd oxidase sustains sulfide-resistant bacterial respiration and growth. Free Radical Biology and Medicine, Vol. 96 (pp S43-S44)
- Heterologous expression of the Campylobacter jejuni globins: Roles of CGB and CTB in the nitrosative stress resistance in Escherichia coli. Nitric Oxide, Vol. 27 (pp S44-S45)
- Bacterial haemoglobins and nitric oxide: Diversity and redundancy?. NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 27 (pp S10-S10)
- The nitric oxide-responsive haemoglobins of Campylobacter jejuni. NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S78-S78)
- Haemoglobin-mediated NO detoxification and S-nitrosothiol depletion by pathogenic bacteria. NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S22-S22)
- Peroxynitrite stress is exacerbated by increased Hmp levels in Salmonella Typhimurium. NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S78-S78)
- NO-detoxifying flavohaemoglobins of the fungal pathogens Magnaporthe grisea and Botrytis cinerea. NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S77-S77)
- The transcriptional response of Escherichia coli to peroxynitrite uncovers an enzyme with peroxynitrase activity. NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S91-S91)
- The Single Domain Hemoglobin From Campylobactor Jejuni: The Unique Structural Features Underlying Its NO Dioxygenase Activity. Biophysical Journal, Vol. 96(3) (pp 557a-557a)
- Ligand binding properties of hemoglobin cgb from the food-borne pathogen Campylobacter Jejuni. BIOPHYSICAL JOURNAL (pp 382A-382A)
- Nitric oxide-responsive and detoxifying mechanisms in bacteria. NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 11(1) (pp 37-37)
- Nitric oxide is an effector in bacterial gene expression mediated by FNR and FNR-like proteins. BIOLOGY OF NITRIC OXIDE, PT 7, Vol. 16 (pp 158-158)
- Bacterial responses to pH - Summary. BACTERIAL RESPONSE TO PH, Vol. 221 (pp 251-255)
- Symposium on Bacterial responses to pH, held at the Novartis Foundation, London 1-4 June 1998 - Introduction. BACTERIAL RESPONSE TO PH, Vol. 221 (pp 1-3)