Professor Robert Poole
School of Biosciences
Emeritus Professor of Microbiology
+44 114 222 4447
Full contact details
School of Biosciences
Firth Court
Western Bank
91Ö±²¥
S10 2TN
- Profile
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Career history
- 1996 - 2020: West Riding Chair of Microbiology, 91Ö±²¥
- 1997 - 2008: Director of Research, Biological Sciences, 91Ö±²¥
- 1994: Fulbright Scholar, Cornell University
- 1993: Visiting Fellow, Australian National University, Canberra
- 1990 -1991: Royal Society-Leverhulme Trust Senior Research Fellow (KCL)
- 1988 -1996: Personal Chair of Microbiology (KCL)
- 1988: Head of Department, Queen Elizabeth College
- 1986-1988: Reader in Microbiology, University of London
- 1984-1985: Royal Society Anglo-Australian Fellow, Australian National University, Canberra
- 1980-1981: Nuffield Foundation Science Research Fellow, Queen Elizabeth College, London
- 1984: DSc, University of Wales
- 1975 -1985: Lecturer, Department of Microbiology, Queen Elizabeth College, London (now King’s College London, KCL)
- 1973 -1974: Personal SRC Post-doctoral Research Fellowship, Department of Biochemistry, Medical Sciences Institute, The University, Dundee
- 1967 -1973: BSc (First Class Hons.), Department of Microbiology, University College Cardiff; PhD, Department of Microbiology, University College Cardiff
- Qualifications
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Honours and distinctions
- 2008 - present: Editorial Board, Journal of Biological Chemistry
- 2007: FRSC, Fellow of the Royal Society of Chemistry
- 1994 - present: Sole Editor Advances in Microbial Physiology
- 1994: Fulbright Scholar, Cornell University, USA
- 1993: Visiting Fellow, Australian National University, Canberra
- 1990 - 1991: Royal Society-Leverhulme Trust Senior Research Fellow (KCL)
- 1985: FRSB, Fellow of the Royal Society of Biology
- Research interests
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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.
- Publications
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Journal articles
- . Veterinary Microbiology, 284, 109819-109819.
- . Antioxidants, 10(6).
- . Antioxidants & Redox Signaling, 34(16), 1280-1318.
- . Chemical Reviews, 120(24), 13273-13311.
- . Metallomics, 12(10), 1563-1575.
- . Biotechnology for Biofuels, 13(1).
- . Frontiers in Microbiology, 10.
- . Research in Microbiology, 170(8), 407-416.
- . ACS Nano, 13(5), 5133-5146.
- . Journal of Biomedical Optics, 24(05).
- . Biochemical Society transactions.
- . Redox Biology, 18, 114-123.
- . ChemPlusChem, 83(7), 643-650.
- . Dalton Transactions, 47(7), 2422-2434.
- . Nitric Oxide, 73, 39-51.
- . Environmental Microbiology, 19(10), 4326-4348.
- . Microbiology.
- . Antioxidants & Redox Signaling.
- . Infection and Immunity, 85(11).
- . Advances in Microbial Physiology.
- . Advances in microbial physiology, 70, XI-XII.
- . Scientific Reports, 6, 35285-35285.
- . Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1857, e13-e14.
- . Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1857, e85-e86.
- . Antioxidants & Redox Signaling, 24(17), 1013-1028.
- . Molecular Microbiology, 100(5), 877-892.
- . Antioxidants & Redox Signaling, 24(14), 765-780.
- . PLOS ONE, 11(5), e0155186-e0155186.
- . Science, 352(6285), 518-519.
- . Scientific Reports, 6.
- . Biochemical Journal, 473(6), 693-701.
- . Genomics Data, 5, 231-234.
- . Journal of Biological Chemistry, 290(31), 18999-19007.
- . Environmental Microbiology, 17(7), 2477-2491.
- . Antioxidants & Redox Signaling, 23(2), 148-162.
- , 1-53.
- . Journal of Biological Chemistry, 289(43), 29471-29482.
- . J Biol Chem, 289(33), 23177-23188.
- . Microbiology, 160(12), 2771-2779.
- . Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1837, e96-e96.
- . Microbiology, 160(Pt 9), 2045-2052.
- . DALTON TRANSACTIONS, 43(26), 9986-9997.
- . Front Microbiol, 5, 124.
- . PLoS One, 9(4), e95617.
- . Adv Microb Physiol, 64, 65-114.
- . PLoS Comput Biol, 10(4), e1003595.
- . F1000Prime Rep, 5, 28.
- . Nitric Oxide, 34, 65-75.
- . Biochim Biophys Acta, 1834(9), 1693-1703.
- . Biochim Biophys Acta, 1834(9), 1789-1800.
- . Antioxid Redox Signal, 19(17), 1999-2012.
- . Biochim Biophys Acta, 1834(9), 1923-1931.
- , 63, 391-446.
- . Antioxid Redox Signal, 19(5), 497-509.
- . Antioxid Redox Signal, 18(4), 424-431.
- . Antioxid Redox Signal, 18(3), 309-322.
- . Curr Pharm Biotechnol, 13(6), 760-768.
- . Open Biol, 2(7), 120091.
- . Anal Biochem, 427(1), 36-40.
- Electron transport and oxidative stress in Zymomonas mobilis respiratory mutants. Archives of Microbiology, 1-11.
- . Microbiology, 158(Pt 1), 284-292.
- . PLoS ONE, 6(9).
- . IUBMB Life, 63(5), 363-371.
- . J Biol Chem, 286(12), 10147-10154.
- . Nitric Oxide - Biology and Chemistry, 25(2), 229-233.
- . Biochemistry, 50(19), 3946-3956.
- . Adv Microb Physiol, 59, 135-219.
- . Nitric Oxide, 25(2), 234-241.
- . Environ Microbiol, 13(1), 48-61.
- . Microbiology, 156(Pt 12), 3556-3565.
- . J Biol Chem, 285(27), 20724-20731.
- . J Biol Chem, 285(17), 12747-12754.
- . FEBS Lett, 584(8), 1628-1632.
- . J Biol Chem, 285(24), 18464-18472.
- . Microbial Pathogenesis, 49(3), 59-66.
- . FASEB J, 24(1), 286-295.
- , 56, 85-167.
- . J Microbiol Methods, 79(3), 329-335.
- . J Biol Chem, 284(27), 18377-18389.
- . FASEB J, 23(4), 1023-1031.
- . J Biol Chem, 284(7), 4516-4524.
- . 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.
- . FEMS Microbiol Lett, 289(2), 219-224.
- . J Biol Chem, 283(42), 28413-28425.
- . J Biol Chem, 283(17), 11146-11154.
- . Microbiology, 154(Pt 2), 608-618.
- . Microbiology, 154(3), 989-994.
- , 437, 255-286.
- . Journal of the American Chemical Society, 130(15), 5231-5244.
- . Methods Enzymol, 437, 499-519.
- . Methods Enzymol, 436, 289-302.
- . Methods Enzymol, 436, 169-186.
- . Gene, 398(1-2), 62-68.
- . Microbes Infect, 9(8), 981-987.
- . Microbiology, 153(Pt 6), 1756-1771.
- . Biochemistry, 46(17), 5030-5037.
- . Microbiology, 153(Pt 5), 1499-1509.
- . J Biol Chem, 282(15), 11230-11237.
- . J Bacteriol, 189(5), 1845-1855.
- . J Bacteriol, 189(5), 1604-1615.
- . Journal of Biological Chemistry, 282(18), 13627-13636.
- . Archives of Microbiology, 187(1), 67-77.
- . Journal of Biological Chemistry, 282(35), 25917-25928.
- . Mol Microbiol, 63(2), 575-590.
- . J Biol Chem, 281(38), 27806-27815.
- . Biochemistry, 45(19), 6003-6011.
- . FEBS Letters, 580(21), 5084-5088.
- . Microbiology, 151(Pt 12), 4079-4091.
- . J Biol Chem, 280(37), 32254-32261.
- . J Biol Chem, 280(11), 10065-10072.
- . J Bacteriol, 187(3), 1124-1134.
- . Biochem Soc Trans, 33(Pt 1), 176-180.
- . Molecular Microbiology, 57(3), 735-750.
- . Plant Journal, 43(2), 226-237.
- . Arch Microbiol, 182(2-3), 193-203.
- . 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.
- . Electrophoresis, 25(15), 2469-2477.
- . FEBS Letters, 576(1-2), 201-204.
- . Journal of Bacteriology, 186(16), 5332-5341.
- . J Biol Chem, 278(34), 31584-31592.
- . J BIOL CHEM, 278(32), 29478-29486.
- . Anal Biochem, 318(1), 30-38.
- . World Journal of Microbiology and Biotechnology, 19(2), 117-121.
- . Journal of Biological Chemistry, 278(37), 34975-34982.
- . Microbiology, 149(7), 1739-1744.
- . Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 84(2), 99-107.
- . Adv Microb Physiol, 47, 255-310.
- . J Biol Chem, 277(51), 49841-49849.
- . Arch Microbiol, 178(5), 358-369.
- . Infect Immun, 70(8), 4399-4405.
- . FEMS Microbiol Lett, 213(1), 121-126.
- . EMBO J, 21(13), 3235-3244.
- Structure and function relationships in bacterial hemoglobins. JOURNAL OF INORGANIC BIOCHEMISTRY, 86(1), 487-487.
- . J Biol Chem, 276(25), 22095-22099.
- . J Bacteriol, 183(10), 3050-3054.
- . MOLECULAR AND BIOCHEMICAL PARASITOLOGY, 114(1), 103-109.
- . BIOMETALS, 14(1), 59-66.
- . Biochemical Journal, 353(2), 207-213.
- . Biochem J, 353(Pt 2), 207-213.
- . FEMS Microbiol Lett, 194(2), 215-220.
- . FEMS Microbiology Letters, 194(2), 215-220.
- Resonance Raman studies of the catalytic site of flavohemoglobin. BIOPHYSICAL JOURNAL, 80(1), 290A-290A.
- . Journal of Biological Chemistry, 276(10), 7272-7277.
- . J Biol Chem, 275(46), 35868-35875.
- . FEBS Lett, 473(1), 67-70.
- . Mol Microbiol, 36(4), 775-783.
- . Microbiology, 146 ( Pt 4), 787-796.
- . FEMS Microbiol Lett, 185(1), 71-77.
- . J Bacteriol, 182(5), 1442-1447.
- . J Biol Chem, 275(7), 4679-4686.
- . Microbiology, 146 ( Pt 2), 527-536.
- . FEMS Microbiology Letters, 184(2), 231-235.
- . Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 78(1), 23-31.
- . Microbiology, 146(6), 1259-1266.
- . Adv Microb Physiol, 43, 165-224.
- . Microbiology, 145 ( Pt 8), 1817-1830.
- . FEBS Lett, 445(2-3), 389-394.
- . J Biol Chem, 274(2), 748-754.
- . Microbiology, 145(7), 1563-1573.
- Bacterial response to pH. Introduction.. Novartis Found Symp, 221, 1-3.
- . J Bacteriol, 181(2), 501-507.
- . Microbiology, 144 ( Pt 12), 3297-3308.
- . FEMS Microbiol Lett, 166(2), 219-223.
- . Mol Microbiol, 29(4), 1101-1112.
- . Biochemical Society Transactions, 26(3), S216-S216.
- . Microbiology, 144(2), 361-373.
- . Journal of Bacteriology, 180(1), 128-135.
- . Microbiology, 144(8), 2271-2280.
- . Molecular Microbiology, 28(1), 205-216.
- . FEMS Microbiology Letters, 168(1), 91-97.
- . Biochemical Journal, 332(2), 413-419.
- . FEMS Microbiol Lett, 155(2), 179-184.
- . J Bacteriol, 179(20), 6525-6530.
- . FEBS Lett, 414(2), 373-376.
- . Microbiology, 143 ( Pt 7), 2197-2207.
- . Biosci Rep, 17(3), 303-317.
- . Mol Gen Genet, 254(5), 599-603.
- . Microbiology, 143 ( Pt 5), 1557-1565.
- . J Bacteriol, 179(10), 3164-3170.
- . Molecular Microbiology, 25(5), 883-891.
- . Microbiology, 143(1), 231-237.
- Metal-microbe interactions: Contemporary approaches. Advances in Microbial Physiology, 38, 231-243.
- Metal-microbe interactions: Contemporary approaches. ADV MICROB PHYSIOL, 38, 177-243.
- . Microbiology, 142(12), 3381-3388.
- . Journal of Bacteriology, 178(18), 5487-5492.
- . Molecular Microbiology.
- . Antioxidants, 11(7), 1222-1222.
- . Biochemical Journal.
- . F1000Research, 9, 7-7.
- . Dalton Transactions, 48(38), 14505-14515.
- . Metallomics, 11(12), 2033-2042.
- . PLOS ONE, 12(10), e0186359-e0186359.
- . F1000Research, 4, 22-22.
- . F1000Research, 4, 5-5.
- . F1000Research, 4, 22-22.
- . Integr. Biol., 4(1), 53-64.
Chapters
- , Advances in Microbial Physiology (pp. xiii-xiii). Elsevier
- , Advances in Microbial Physiology (pp. xi-xi). Elsevier
- , Advances in Microbial Physiology (pp. xiii-xiii). Elsevier
- (pp. xiii). Elsevier
- Advances in Microbial Physiology Preface, ADVANCES IN MICROBIAL PHYSIOLOGY, VOL 78 (pp. XI-XI).
- Advances in Microbial Physiology PREFACE, ADVANCES IN MICROBIAL PHYSIOLOGY, VOL 74 (pp. XIII-XIII).
- , Encyclopedia of Biophysics (pp. 1-6). Springer Berlin Heidelberg
- , Encyclopedia of Biophysics (pp. 1-7). Springer Berlin Heidelberg
- , Advances in Bacterial Electron Transport Systems and Their Regulation (pp. xiii-xiii). Elsevier
- , Encyclopedia of Biophysics (pp. 156-160). Springer Berlin Heidelberg
- , Encyclopedia of Biophysics (pp. 172-177). Springer Berlin Heidelberg
- , Methods in Enzymology (pp. xxiii-xxiv). Elsevier
- , Globins and Other Nitric Oxide-Reactive Proteins, Part B (pp. xxvii-xxviii). Elsevier
- , Dioxygen Binding and Sensing Proteins (pp. 241-257). Springer Milan
- , Biological Nitrogen Fixation for the 21st Century (pp. 87-92). Springer Netherlands
- , Novartis Foundation Symposium 221 - Bacterial Responses to pH (pp. 251-255). John Wiley & Sons, Ltd.
- , Helicobacter pylori (pp. 111-124). ASM Press
Conference proceedings papers
- . Free Radical Biology and Medicine, Vol. 120 (pp S163-S164)
- . Free Radical Biology and Medicine, Vol. 96 (pp S43-S44)
- . Nitric Oxide, Vol. 27 (pp S44-S45)
- . NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 27 (pp S10-S10)
- . NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S78-S78)
- . NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S22-S22)
- . NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S77-S77)
- . NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S91-S91)
- . NITRIC OXIDE-BIOLOGY AND CHEMISTRY, Vol. 22 (pp S78-S78)
- . 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)