Faculty of Health and Life Sciences

Dr Clive Butler

Dr Clive Butler

Associate Professor of Microbial Biochemistry

 C.S.Butler@exeter.ac.uk

 4675

 Geoffrey Pope 415

 

Geoffrey Pope Building, University of Exeter , Stocker Road, Exeter, EX4 4QD, UK

Overview

My research interests lie in the study of the microbiology and biochemistry of important mineral cycles, with specific focus on the microbial interaction with selenium and nitrogen. The main objective of my work is to characterize the biochemical reactions of these cycles in whole cells and cell fractions.  We study gene expression and protein synthesis in response to environmental change; investigate electron-transfer reactions between proteins involved in respiratory pathways; and purify and characterize proteins and enzymes to reveal their structure and function. We study a range of organisms including human pathogens, soil bacteria, archaea and algae, and use a combination of whole cell physiology, molecular genetics, enzymology, spectroscopy, imaging and structural biology. This work has implications for understanding how pathogens can survive and colonize within a host during infection, through to the synthetic exploitation of bacterial biomineralization for the environmentally friendly and cost efficient fabrication of novel nanomaterials.

Qualifications

2014 Senior Fellow of The Higher Education Academy
2001 Certificate in Learning and Teaching, Faculty of Education, University of Newcastle
1995 PhD Microbial Biochemistry, King's College, University of London
1991 BSc (Hons) Biotechnology, King's College, University of London

Career

2012 – present Associate Professor in Microbial Biochemistry, Biosciences, CLES, University of Exeter
2006-2012 Senior Lecturer in Biochemistry, School of Biosciences, University of Exeter
2000-2006 Lecturer in Biochemistry, Institute for Cell and Molecular Biosciences, University of Newcastle
1995-2000 Senior Research Associate, Centre for Metalloprotein Spectroscopy and Biology (CMSB). University of East Anglia, Norwich

Research group links

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Research

Research interests

My main research interest is in the general area of Microbial Biochemistry. Current work in the laboratory is focussed on four key projects.

Research projects

  • Characterization of enzyme complexes that participate in the microbial respiration of selenium and nitrogen oxyanions.
  • Understanding the role of anaerobic respiration in the survival and virulence of pathogenic bacteria.
  • Functional studies of microbial metalloproteins, with particular interest in molybdenum, tungsten, iron-sulphur, copper and haem biochemistry.
  • Synthetic biomineralization of metalloid nano-materials using bacterial peptides.

We use a range of model organisms (bacteria (pathogens and non-pathogens), archaea and algae) and use a combination of whole cell physiology (bioreactors/photo-reactors), molecular genetics, enzymology, spectroscopy and structural biology. The work is currently funded by both research council and industrial sponsors.

Research grants

2016 BBSRC Research Grant (with Titball and Wagley)
Uncovering the molecular basis of formation of viable but non-culturable cells

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Publications

Journal articles

Wagley S, Morcrette H, Kovacs-Simon A, Yang ZR, Power A, Tennant RK, Love J, Murray N, Titball RW, Butler CS, et al (2021). Bacterial dormancy: a subpopulation of viable but non-culturable cells demonstrates better fitness for revival. PLoS Pathogens, 17(1). Abstract.
Harrison J, Nelson K, Morcrette H, Morcrette C, Preston J, Helmer L, Titball RW, Butler CS, Wagley S (2021). The increased prevalence of Vibrio species and the first reporting of Vibrio jasicida and Vibrio rotiferianus at UK shellfish sites. Water Research, 211
Morcrette H, Kovacs-Simon A, Tennant RK, Love J, Wagley S, Yang ZR, Studholme DJ, Soyer OS, Champion OL, Butler CS, et al (2020). Campylobacter jejuni 11168H Exposed to Penicillin Forms Persister Cells and Cells with Altered Redox Protein Activity. Frontiers in Cellular and Infection Microbiology, 10 Abstract.
Witherall L, Wagley S, Butler C, Tyler CR, Temperton B (2019). Genome Sequences of Four Vibrio parahaemolyticus Strains Isolated from the English Channel and the River Thames. Microbiol Resour Announc, 8(24). Abstract.  Author URL.
Wagley S, Titball R, Butler C (2019). Uncovering the molecular basis of viable but non culturable (VBNC) cells. Access Microbiology, 1(1A).
Lampis S, Zonaro E, Bertolini C, Cecconi D, Monti F, Micaroni M, Turner RJ, Butler CS, Vallini G (2017). Selenite biotransformation and detoxification by Stenotrophomonas maltophilia SeITE02: Novel clues on the route to bacterial biogenesis of selenium nanoparticles. J Hazard Mater, 324(Pt A), 3-14. Abstract.  Author URL.
Hemsley CM, Luo JX, Andreae CA, Butler CS, Soyer OS, Titball RW (2014). Bacterial drug tolerance under clinical conditions is governed by anaerobic adaptation but not anaerobic respiration. Antimicrob Agents Chemother, 58(10), 5775-5783. Abstract.  Author URL.
Lampis S, Zonaro E, Bertolini C, Bernardi P, Butler CS, Vallini G (2014). Delayed formation of zero-valent selenium nanoparticles by Bacillus mycoides SeiTE01 as a consequence of selenite reduction under aerobic conditions. Microbial Cell Factories, 13(1), 1-14. Abstract.
Bertolini C, van Aerle R, Lampis S, Moore KA, Paszkiewicz K, Butler CS, Vallini G, van der Giezen M (2014). Draft Genome Sequence of Stenotrophomonas maltophilia SeITE02, a Gammaproteobacterium Isolated from Selenite-Contaminated Mining Soil. Genome Announc, 2(3). Abstract.  Author URL.
Andreae CA, Titball RW, Butler CS (2014). Influence of the molybdenum cofactor biosynthesis on anaerobic respiration, biofilm formation and motility in Burkholderia thailandensis. Res Microbiol, 165(1), 41-49. Abstract.  Author URL.
Wagley S, Hemsley C, Thomas R, Moule MG, Vanaporn M, Andreae C, Robinson M, Goldman S, Wren BW, Butler CS, et al (2014). The twin arginine translocation system is essential for aerobic growth and full virulence of Burkholderia thailandensis. J Bacteriol, 196(2), 407-416. Abstract.  Author URL.
Butler CS, Debieux CM, Dridge EJ, Splatt P, Wright M (2012). Biomineralization of selenium by the selenate-respiring bacterium Thauera selenatis. Biochemical Society Transactions, 40(6), 1239-1243. Abstract.
Butler CS (2012). Metals, non-metals and minerals: the complexity of bacterial selenate respiration. Biochemist, 34(5), 23-27. Abstract.
Debieux CM, Dridge EJ, Mueller CM, Splatt P, Paszkiewicz K, Knight I, Florance H, Love J, Titball RW, Lewis RJ, et al (2011). A bacterial process for selenium nanosphere assembly. Proceedings of the National Academy of Sciences of the United States of America, 108(33), 13480-13485. Abstract.
Gates AJ, Butler CS, Richardson DJ, Butt JN (2011). Electrocatalytic reduction of nitrate and selenate by NapAB. Biochemical Society Transactions, 39(1), 236-242. Abstract.
Lowe EC, Bydder S, Hartshorne RS, Tape HLU, Dridge EJ, Debieux CM, Paszkiewicz K, Singleton I, Lewis RJ, Santini JM, et al (2010). Quinol-cytochrome c oxidoreductase and cytochrome c4 mediate electron transfer during selenate respiration in Thauera selenatis. J Biol Chem, 285(24), 18433-18442. Abstract.  Author URL.
Dridge EJ, Butler CS (2010). Thermostable properties of the periplasmic selenate reductase from Thauera selenatis. Biochimie, 92(10), 1268-1273. Abstract.
Hall SJ, Hitchcock A, Butler CS, Kelly DJ (2009). A Multicopper Oxidase (Cj1516) and a CopA Homologue (Cj1161) Are Major Components of the Copper Homeostasis System of <i>Campylobacter jejuni</i> (vol 190, pg 8075, 2009). JOURNAL OF BACTERIOLOGY, 191(3), 1122-1122.  Author URL.
Hall SJ, Hitchcock A, Butler CS, Kelly DJ (2008). A multicopper oxidase (Cj1516) and a CopA homologue (Cj1161) are major components of the copper homeostasis system of Campylobacter jejuni. Journal of Bacteriology, 190(24), 8075-8085. Abstract.
Leaver JT, Richardson DJ, Butler CS (2008). Enterobacter cloacae SLD1a-1 gains a selective advantage from selenate reduction when growing in nitrate-depleted anaerobic environments. Journal of Industrial Microbiology and Biotechnology, 35(8), 867-873. Abstract.
Campbell SC, Aldibbiat A, Marriott CE, Landy C, Ali T, Ferris WF, Butler CS, Shaw JA, Macfarlane WM (2008). Selenium stimulates pancreatic beta-cell gene expression and enhances islet function. FEBS Letters, 582(15), 2333-2337. Abstract.
Huston WM, Harhangi HR, Leech AP, Butler CS, Jetten MSM, Op den Camp HJM, Moir JWB (2007). Expression and characterisation of a major c-type cytochrome encoded by gene kustc0563 from Kuenenia stuttgartiensis as a recombinant protein in Escherichia coli. Protein Expression and Purification, 51(1), 28-33. Abstract.
Dridge EJ, Watts CA, Jepson BJN, Line K, Santini JM, Richardson DJ, Butler CS (2007). Investigation of the redox centres of periplasmic selenate reductase from Thauera selenatis by EPR spectroscopy. Biochemical Journal, 408(1), 19-28. Abstract.
Martinez-Espinosa RM, Dridge EJ, Bonete MJ, Butt JN, Butler CS, Sargent F, Richardson DJ (2007). Look on the positive side! the orientation, identification and bioenergetics of 'Archaeal' membrane-bound nitrate reductases. FEMS Microbiology Letters, 276(2), 129-139. Abstract.
Campbell SC, Richardson H, Ferris WF, Butler CS, Macfarlane WM (2007). Nitric oxide stimulates insulin gene transcription in pancreatic β-cells. Biochemical and Biophysical Research Communications, 353(4), 1011-1016. Abstract.
Jepson BJN, Mohan S, Clarke TA, Gates AJ, Cole JA, Butler CS, Butt JN, Hemmings AM, Richardson DJ (2007). Spectropotentiometric and structural analysis of the periplasmic nitrate reductase from Escherichia coli. Journal of Biological Chemistry, 282(9), 6425-6437. Abstract.
Ridley H, Watts CA, Richardson DJ, Butler CS (2006). Development of a viologen-based microtiter plate assay for the analysis of oxyanion reductase activity: Application to the membrane-bound selenate reductase from Enterobacter cloacae SLD1a-1. Analytical Biochemistry, 358(2), 289-294. Abstract.
Jepson BJN, Marietou A, Mohan S, Cole JA, Butler CS, Richardson DJ (2006). Evolution of the soluble nitrate reductase: Defining the monomeric periplasmic nitrate reductase subgroup. Biochemical Society Transactions, 34(1), 122-126. Abstract.
Huston WM, Andrew CR, Servid AE, McKay AL, Leech AP, Butler CS, Moir JWB (2006). Heterologous overexpression and purification of cytochrome c′ from Rhodobacter capsulatus and a mutant (K42E) in the dimerization region. Mutation does not alter oligomerization but impacts the heme iron spin state and nitric oxide binding properties. Biochemistry, 45(14), 4388-4395. Abstract.
Ridley H, Watts CA, Richardson DJ, Butler CS (2006). Resolution of distinct membrane-bound enzymes from Enterobacter cloacae SLD1a-1 that are responsible for selective reduction of nitrate and selenate oxyanions. Applied and Environmental Microbiology, 72(8), 5173-5180. Abstract.
Huston WM, Lowe EC, Butler CS, Moir JWB (2005). Purification and characterization of cytochrome c′ from Neisseria meningitidis. Biochemical Society Transactions, 33(1), 187-189. Abstract.
Butler CS, Richardson DJ (2005). The emerging molecular structure of the nitrogen cycle: an introduction to the proceedings of the 10th annual N-cycle meeting. Biochemical Society Transactions, 33(1), 113-118. Abstract.
Borrelly GPM, Blindauer CA, Schmid R, Butler CS, Cooper CE, Harvey I, Sadler PJ, Robinson NJ (2004). A novel copper site in a cyanobacterial metallochaperone. Biochem J, 378(Pt 2), 293-297. Abstract.  Author URL.
Borrelly GPM, Blindauer CA, Schmid R, Butler CS, Cooper CE, Harvey I, Sadler PJ, Robinson NJ (2004). Accelerated publication: a novel copper site in a cyanobacterial metallochaperone. Biochemical Journal, 378(2), 293-297. Abstract.
Cheesman MR, Oganesyan VS, Watmough NJ, Butler CS, Thomson AJ (2004). The Nature of the Exchange Coupling between High-Spin Fe(III) Heme o <inf>3</inf> and Cu<inf>B</inf>(II) in Escherichia coli Quinol Oxidase, Cytochrome bo<inf>3</inf>: MCD and EPR Studies. Journal of the American Chemical Society, 126(13), 4157-4166. Abstract.
Jepsoni BJN, Anderson LJ, Rubio LM, Taylor CJ, Butler CS, Flores E, Herrero A, Butt JN, Richardson DJ (2004). Tuning a nitrate reductase for function. The first spectropotentiometric characterization of a bacterial assimilatory nitrate reductase reveals novel redox properties. Journal of Biological Chemistry, 279(31), 32212-32218. Abstract.
Gates AJ, Hughes RO, Sharp SR, Millington PD, Nilavongse A, Cole JA, Leach ER, Jepson B, Richardson DJ, Butler CS, et al (2003). Properties of the periplasmic nitrate reductases from Paracoccus pantotrophus and Escherichia coli after growth in tungsten-supplemented media. FEMS Microbiology Letters, 220(2), 261-269. Abstract.
Watts CA, Ridley H, Condie KL, Leaver JT, Richardson DJ, Butler CS (2003). Selenate reduction by Enterobacter cloacae SLD1a-1 is catalysed by a molybdenum-dependent membrane-bound enzyme that is distinct from the membrane-bound nitrate reductase. FEMS Microbiology Letters, 228(2), 273-279. Abstract.
Butler CS, Forte E, Maria Scandurra F, Arese M, Giuffré A, Greenwood C, Sarti P (2002). Cytochrome bo<inf>3</inf> from Escherichia coli: the binding and turnover of nitric oxide. Biochemical and Biophysical Research Communications, 296(5), 1272-1278. Abstract.
Butler CS, Fairhurst SA, Ferguson SJ, Thomson AJ, Berks BC, Richardson DJ, Lowe DJ (2002). Mo(V) co-ordination in the periplasmic nitrate reductase from Paracoccus pantotrophus probed by electron nuclear double resonance (ENDOR) spectroscopy. Biochem J, 363(Pt 3), 817-823. Abstract.  Author URL.
Butler CS, Ferguson SJ, Berks BC, Thomson AJ, Cheesman MR, Richardson DJ (2001). Assignment of haem ligands and detection of electronic absorption bands of molybdenum in the di-haem periplasmic nitrate reductase of Paracoccus pantotrophus. FEBS Letters, 500(1-2), 71-74. Abstract.
Hunter DJB, Oganesyan VS, Salerno JC, Butler CS, Ingledew WJ, Thomson AJ (2000). Angular dependences of perpendicular and parallel mode electron paramagnetic resonance of oxidized beef heart cytochrome c oxidase. Biophysical Journal, 78(1), 439-450. Abstract.
Butler CS, Charnock JM, Garner CD, Thomson AJ, Ferguson SJ, Berks BC, Richardson DJ (2000). Thiocyanate binding to the molybdenum centre of the periplasmic nitrate reductase from Paracoccus pantotrophus. Biochemical Journal, 352(3), 859-864. Abstract.
Butler CS, Charnock JM, Bennett B, Sears HJ, Reilly AJ, Ferguson SJ, Garner CD, Lowe DJ, Thomson AJ, Berks BC, et al (1999). Models for molybdenum coordination during the catalytic cycle of periplasmic nitrate reductase from Paracoccus denitrificans derived from EPR and EXAFS spectroscopy. Biochemistry, 38(28), 9000-9012. Abstract.
Oganesyan VS, Butler CS, Watmough NJ, Greenwood C, Thomson AJ, Cheesman MR (1998). Nature of the Coupling between the High-Spin Fe(III) Heme and CuB(II) in the Active Site of Terminal Oxidases: Dual-Mode EPR Spectra of Fluoride Cytochrome bo3. J. Am. Chem. Soc., 120, 4232-4233.
Watmough NJ, Cheesman MR, Butler CS, Little RH, Greenwood C, Thomson AJ (1998). The dinuclear center of cytochrome bo<inf>3</inf> from Escherichia coli. Journal of Bioenergetics and Biomembranes, 30(1), 55-62. Abstract.
Richardson DJ, Wehrfritz JM, Keech A, Crossman LC, Roldan MD, Sears HJ, Butler CS, Reilly A, Moir JWB, Berks BC, et al (1998). The diversity of redox proteins involved in bacterial heterotrophic nitrification and aerobic denitrification. Biochemical Society Transactions, 26(3), 401-408.
Moody AJ, Butler CS, Watmough NJ, Thomson AJ, Rich PR (1998). The reaction of halides with pulsed cytochrome bo from Escherichia coli. Biochemical Journal, 331(2), 459-464. Abstract.
Butler CS, Cheesman MR, Greenwood C, Thomson AJ, Watmough NJ (1997). Fast Cytochrome bo from Escherichia coli reacts with azide and nitric oxide to form a complex analogous to that formed by cytochrome c oxidase. Biochemical Society Transactions, 25(3).
Butler CS, Seward HE, Greenwood C, Thomson AJ (1997). Fast cytochrome bo from Escherichia coli binds two molecules of nitric oxide at CU(B). Biochemistry, 36(51), 16259-16266. Abstract.
Brittain T, Baker AR, Butler CS, Little RH, Lowe DJ, Greenwood C, Watmough NJ (1997). Reaction of variant sperm-whale myoglobins with hydrogen peroxide: the effects of mutating a histidine residue in the haem distal pocket. Biochemical Journal, 326(1), 109-115. Abstract.
Butler CS, Mason JR (1997). Structure-function analysis of the bacterial aromatic ring-hydroxylating dioxygenases. Advances in Microbial Physiology, 38, 75-84.
TAN HM, JOANNOU CL, COPPER CE, BUTLER CS, CAMMACK R, MASON JR (1994). THE EFFECT OF FERREDOXIN(BED) OVEREXPRESSION ON BENZENE DIOXYGENASE ACTIVITY IN PSEUDOMONAS-PUTIDA ML2. JOURNAL OF BACTERIOLOGY, 176(9), 2507-2512.  Author URL.

Conferences

Dridge EJ, Richardson DJ, Lewis RJ, Butler CS (2006). Developing structure-based models to predict substrate specificity of D-group (Type II) molybdenum enzymes: application to a molybdo-enzyme of unknown function from Archaeoglobus fulgidus. Abstract.  Author URL.
Lowe EC, Watts CA, Richardson DJ, Santini JM, Singleton I, Butler CS (2006). The bioenergetics of selenate respiration in Thauera selenatis.  Author URL.
Watts CA, Ridley H, Dridge EJ, Leaver JT, Reilly AJ, Richardson DJ, Butler CS (2005). Microbial reduction of selenate and nitrate: common themes and variations. Abstract.  Author URL.
Butler CS, Calvert JE (2004). Business for the Bio-scientist: a blueprint module for entrepreneurship in bioscience.
Mason JR, Butler CS, Cammack R, Shergill JK (1997). Structural studies on the catalytic component of benzene dioxygenase from Pseudomonos putido.
SHERGILL JK, BUTLER CS, WHITE AC, CAMMACK R, MASON JR (1994). EPR, ENDOR AND ESEEM STUDIES ON RECOMBINANT BENZENE DIOXYGENASE.  Author URL.

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External Engagement and Impact

Committee/panel activities

1994-2018 Biochemical Society

2001-2006 Theme Panel III (Bioenergetics) committee member


Invited lectures

21st European Nitrogen Cycle Meeting, University of East Anglia, Norwich, UK (2016)

Departmental Seminar, Biotechnology Institute, University of Minnesota, USA (2015)

Biochemical Society Meeting “Electron transfer at the microbe-mineral interface”, University of East Anglia, UK (2012)

Departmental Seminar, Centre for Nanoscience and Quantum Information, University of Bristol, UK (2011)

7th European Workshop on Bacterial Respiratory Chains, Lund, Sweden (2011)

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Teaching

  • Stage 1 Biochemistry (BIO1332)
  • Stage 2 Bioinorganic Chemistry (BIO2091)
  • Stage 3 Energy Metabolism (BIO3093– module co-ordinator)
  • Stage 4 Further Advanced Topics in Chemistry MSci (NSCM003)

Modules

2023/24


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Supervision / Group

Postdoctoral researchers

Postgraduate researchers

  • Roshan Singh

Alumni

  • Dr Clio Andreae PhD (2014) Understanding the role of anaerobic respiration in Burkholderia thailandensis and B. pseudomallei survival and virulence.
  • Claire Brimilcombe (2017) Resolving the molecular mechanisms for bacterial selenium nanoparticle production (MRes)
  • Dr Elizabeth Dridge PhD (2007) Molecular analysis of the Type II molybdoenzymes from Thauera selenatis and Archaeglobus fulgidus.
  • Charlotte Dridge (2014) Developing self-assembling nanocages with naturally occurring bacterial peptides (MRes)
  • Dr James Leaver PhD (2007) The enzymology and physiology of nitrate and selenate reduction/respiration in Enterobacter cloacae SLD1a-1 and Aeromonas hydrophila ATCC7966.
  • Dr Elisabeth Lowe PhD (2008) Resolving electron transport pathways in the selenate respiring bacterium Thauera selenatis.
  • Dr Helen Ridley PhD (2008) Purification and characterisation of the oxyanion reductases from Enterobacter cloacae SLD1a-1.
  • Dr Hannah Tape PhD (2012) The plieotropic effects of a TolC mutation in Vibrio furnesii.

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