Professor Per Bullough

All publications

Journal articles

• Morales Angeles D, Coleman K, Progress Odika C, Graham CLB, Chan H, Gilmore M, Taib N, Bauda E, Moriscot C, Gallet B , Fisher H et al (2025) SpoIIIL is a forespore factor required for efficient cell-cell signalling during Bacillus subtilis sporulation. PLOS Genetics, 21(7). View this article in WRRO
• Wilson JS, Fortier L-C, Fagan RP & Bullough PA (2025) Molecular mechanism of bacteriophage contraction structure of an S-layer–penetrating bacteriophage. Life Science Alliance, 8(6). View this article in WRRO
• Stevenson SR, Tzokov SB, Lahiri I, Ayscough KR & Bullough PA (2025) Cryo-EM reconstruction of yeast ADP-actin filament at 2.5 Å resolution. A comparison with vertebrate F-actin. Structure, 33(3), 435-442.e3. View this article in WRRO
• Lanzoni-Mangutchi P, Banerji O, Wilson J, Barwinska-Sendra A, Kirk JA, Vaz F, O’Beirne S, Baslé A, El Omari K, Wagner A , Fairweather NF et al (2022) Structure and assembly of the S-layer in C. difficile. Nature Communications, 13(1). View this article in WRRO
• Salamaga B, Kong L, Pasquina-Lemonche L, Lafage L, von und zur Muhlen M, Gibson JF, Grybchuk D, Tooke AK, Panchal V, Culp EJ , Tatham E et al (2021) Demonstration of the role of cell wall homeostasis in Staphylococcus aureus growth and the action of bactericidal antibiotics. Proceedings of the National Academy of Sciences, 118(44). View this article in WRRO
• Tank RKG, Lund VA, Kumar S, Turner RD, Lafage L, Pasquina Lemonche L, Bullough PA, Cadby A, Foster SJ & Hobbs JK (2021) Correlative super-resolution optical and atomic force microscopy reveals relationships between bacterial cell wall architecture and synthesis in Bacillus subtilis. ACS Nano, 15(10), 16011-16018. View this article in WRRO
• Janganan TK, Mullin N, Dafis-Sagarmendi A, Brunt J, Tzokov SB, Stringer S, Moir A, Chaudhuri RR, Fagan RP, Hobbs JK & Bullough PA (2020) Architecture and self-assembly of clostridium sporogenes and clostridium botulinum spore surfaces illustrate a general protective strategy across spore formers. mSphere, 5(4). View this article in WRRO
• Pasquina-Lemonche L, Burns J, Turner RD, Kumar S, Tank R, Mullin N, Wilson JS, Chakrabarti B, Bullough PA, Foster SJ & Hobbs JK (2020) The architecture of the Gram-positive bacterial cell wall. Nature, 582(7811), 294-297. View this article in WRRO
• Wilson JS, Churchill-Angus AM, Davies SP, Sedelnikova SE, Tzokov SB, Rafferty JB, Bullough PA, Bisson C & Baker PJ (2019) Identification and structural analysis of the tripartite α-pore forming toxin of Aeromonas hydrophila. Nature Communications, 10(1). View this article in WRRO
• Ji S, Dix SR, Aziz AA, Sedelnikova SE, Baker PJ, Rafferty JB, Bullough PA, Tzokov SB, Agirre J, Li F-L & Rice DW (2019) The molecular basis of endolytic activity of a multidomain alginate lyase from Defluviitalea phaphyphila, a representative of a new lyase family, PL39. Journal of Biological Chemistry, 294(48), 18077-18091. View this article in WRRO
• Hill CJ, Fleming JR, Mousavinejad M, Nicholson R, Tzokov SB, Bullough PA, Bogomolovas J, Morgan MR, Mayans O & Murray P (2019) Self‐Assembling Proteins as High‐Performance Substrates for Embryonic Stem Cell Self‐Renewal. Advanced Materials, 31(17).
• Dix SR, Owen HJ, Sun R, Ahmad A, Shastri S, Spiewak HL, Mosby DJ, Harris MJ, Batters SL, Brooker TA , Tzokov SB et al (2018) Structural insights into the function of type VI secretion system TssA subunits.. Nature Communications, 9. View this article in WRRO
• Terry C, Jiang S, Radford DS, Qiang W, Tzokov S, Moir A & Bullough PA (2017) Molecular tiling on the surface of a bacterial spore – the exosporium of the Bacillus anthracis/cereus/thuringiensis group. Molecular Microbiology, 104(4), 539-552.
• Ma C, Hao Z, Huysmans G, Lesiuk A, Bullough P, Wang Y, Bartlam M, Phillips SE, Young JD, Goldman A , Baldwin SA et al (2015) A Versatile Strategy for Production of Membrane Proteins with Diverse Topologies: Application to Investigation of Bacterial Homologues of Human Divalent Metal Ion and Nucleoside Transporters. PLOS ONE, 10(11), e0143010-e0143010.
• Jiang S, Wan Q, Krajcikova D, Tang J, Tzokov SB, Barak I & Bullough PA (2015) Diverse supramolecular structures formed by self-assembling proteins of the B acillus subtilis spore coat. Molecular Microbiology, 97(2), 347-359.
• Adams NBP, Marklew CJ, Qian P, Brindley AA, Davison PA, Bullough PA & Hunter CN (2014) Structural and functional consequences of removing the N-terminal domain from the magnesium chelatase ChlH subunit of Thermosynechococcus elongatus. Biochemical Journal, 464(3), 315-322. View this article in WRRO
• Yamashita M, Shepherd M, Booth WI, Xie H, Postis V, Nyathi Y, Tzokov SB, Poole RK, Baldwin SA & Bullough PA (2014) 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.
• Qian P, Papiz MZ, Jackson PJ, Brindley AA, Ng IW, Olsen JD, Dickman MJ, Bullough PA & Hunter CN (2013) Three-dimensional structure of the Rhodobacter sphaeroides RC-LH1-PufX complex: dimerization and quinone channels promoted by PufX.. Biochemistry, 52(43), 7575-7585.
• Huysmans GHM, Chan N, Baldwin JM, Postis VLG, Tzokov SB, Deacon SE, Yao SYM, Young JD, McPherson MJ, Bullough PA & Baldwin SA (2012) A urea channel from Bacillus cereus reveals a novel hexameric structure.. Biochem J, 445(2), 157-166.
• Qian P, Marklew CJ, Viney J, Davison PA, Brindley AA, Söderberg C, Al-Karadaghi S, Bullough PA, Grossmann JG & Hunter CN (2012) Structure of the cyanobacterial Magnesium Chelatase H subunit determined by single particle reconstruction and small-angle X-ray scattering.. J Biol Chem, 287(7), 4946-4956.
• Glover CAP, Postis VLG, Charalambous K, Tzokov SB, Booth WI, Deacon SE, Wallace BA, Baldwin SA & Bullough PA (2011) AcrB contamination in 2-D crystallization of membrane proteins: Lessons from a sodium channel and a putative monovalent cation/proton antiporter. Journal of Structural Biology, 176(3), 419-424.
• Glover CAP, Postis VLG, Charalambous K, Tzokov SB, Booth WI, Deacon SE, Wallace BA, Baldwin SA & Bullough PA (2011) AcrB contamination in 2-D crystallization of membrane proteins: lessons from a sodium channel and a putative monovalent cation/proton antiporter.. J Struct Biol, 176(3), 419-424.
• Kailas L, Terry C, Abbott N, Taylor R, Mullin N, Tzokov SB, Todd SJ, Wallace BA, Hobbs JK, Moir A & Bullough PA (2011) Surface architecture of endospores of the Bacillus cereus/anthracis/thuringiensis family at the subnanometer scale.. Proc Natl Acad Sci U S A, 108(38), 16014-16019.
• Terry C, Shepherd A, Radford DS, Moir A & Bullough PA (2011) YwdL in Bacillus cereus: its role in germination and exosporium structure.. PLoS One, 6(8), e23801.
• Charalambous K, O'Reilly AO, Bullough PA & Wallace BA (2009) Thermal and chemical unfolding and refolding of a eukaryotic sodium channel.. Biochim Biophys Acta, 1788(6), 1279-1286.
• Ball DA, Taylor R, Todd SJ, Redmond C, Couture-Tosi E, Sylvestre P, Moir A & Bullough PA (2008) Structure of the exosporium and sublayers of spores of the Bacillus cereus family revealed by electron crystallography.. Mol Microbiol, 68(4), 947-958.
• Baboolal TG, Conroy MJ, Gill K, Ridley H, Visudtiphole V, Bullough PA & Lakey JH (2008) Colicin N binds to the periphery of its receptor and translocator, outer membrane protein F.. Structure, 16(3), 371-379.
• Qian P, Bullough PA & Hunter CN (2008) Three-dimensional reconstruction of a membrane-bending complex: the RC-LH1-PufX core dimer of Rhodobacter sphaeroides.. J Biol Chem, 283(20), 14002-14011.
• Hunt S, Moir AJG, Tzokov S, Bullough PA, Artymiuk PJ & Green J (2008) The formation and structure of Escherichia coli K-12 haemolysin E pores.. Microbiology (Reading), 154(Pt 2), 633-642.
• Qian P, Bullough P & Hunter N (2007) Single particle analysis of the dimeric RC-LH1-PufX complex from Rhodobacter sphaeroides. PHOTOSYNTH RES, 91(2-3), 171-171.
• Conroy MJ, Durand A, Lupo D, Li X-D, Bullough PA, Winkler FK & Merrick M (2007) The crystal structure of the Escherichia coli AmtB-GlnK complex reveals how GlnK regulates the ammonia channel.. Proc Natl Acad Sci U S A, 104(4), 1213-1218.
• Tzokov SB, Wyborn NR, Stillman TJ, Jamieson S, Czudnochowski N, Artymiuk PJ, Green J & Bullough PA (2006) Structure of the hemolysin E (HlyE, ClyA, and SheA) channel in its membrane-bound form.. J Biol Chem, 281(32), 23042-23049.
• Merrick M, Javelle A, Durand A, Severi E, Thornton J, Avent ND, Conroy MJ & Bullough PA (2006) The Escherichia coli AmtB protein as a model system for understanding ammonium transport by Amt and Rh proteins.. Transfus Clin Biol, 13(1-2), 97-102.
• Conroy MJ, Bullough PA, Merrick M & Avent ND (2005) Modelling the human rhesus proteins: implications for structure and function.. Br J Haematol, 131(4), 543-551.
• Stillman TJ, Upadhyay M, Norte VA, Sedelnikova SE, Carradus M, Tzokov S, Bullough PA, Shearman CA, Gasson MJ, Williams CH , Artymiuk PJ et al (2005) The crystal structures of Lactococcus lactis MG1363 Dps proteins reveal the presence of an N-terminal helix that is required for DNA binding.. Mol Microbiol, 57(4), 1101-1112.
• Jelinska C, Conroy MJ, Craven CJ, Hounslow AM, Bullough PA, Waltho JP, Taylor GL & White MF (2005) Obligate heterodimerization of the archaeal Alba2 protein with Alba1 provides a mechanism for control of DNA packaging.. Structure, 13(7), 963-971.
• Qian P, Hunter CN & Bullough PA (2005) The 8.5A projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides.. J Mol Biol, 349(5), 948-960.
• Conroy MJ, Jamieson SJ, Blakey D, Kaufmann T, Engel A, Fotiadis D, Merrick M & Bullough PA (2004) Electron and atomic force microscopy of the trimeric ammonium transporter AmtB.. EMBO Rep, 5(12), 1153-1158.
• Bahatyrova S, Frese RN, Siebert CA, Olsen JD, Van Der Werf KO, Van Grondelle R, Niederman RA, Bullough PA, Otto C & Hunter CN (2004) The native architecture of a photosynthetic membrane.. Nature, 430(7003), 1058-1062.
• Bullough PA (2004) Conformational flexibility in assembly of photosynthetic membrane protein complexes in vivo. Microscopy and Microanalysis, 10(SUPPL. 2), 1496-1497.
• Wyborn NR, Clark A, Roberts RE, Jamieson SJ, Tzokov S, Bullough PA, Stillman TJ, Artymiuk PJ, Galen JE, Zhao L , Levine MM et al (2004) Properties of haemolysin E (HlyE) from a pathogenic Escherichia coli avian isolate and studies of HlyE export.. Microbiology (Reading), 150(Pt 5), 1495-1505.
• Siebert CA, Qian P, Fotiadis D, Engel A, Hunter CN & Bullough PA (2004) Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX.. EMBO J, 23(4), 690-700.
• Fotiadis D, Qian P, Philippsen A, Bullough PA, Engel A & Hunter CN (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy.. J Biol Chem, 279(3), 2063-2068.
• Olsen JD, Robert B, Siebert CA, Bullough PA & Hunter CN (2003) Role of the C-terminal extrinsic region of the alpha polypeptide of the light-harvesting 2 complex of Rhodobacter sphaeroides: a domain swap study.. Biochemistry, 42(51), 15114-15123.
• Reid JD, Siebert CA, Bullough PA & Hunter CN (2003) The ATPase activity of the ChlI subunit of magnesium chelatase and formation of a heptameric AAA+ ring.. Biochemistry, 42(22), 6912-6920.
• Qian P, Addlesee HA, Ruban AV, Wang P, Bullough PA & Hunter CN (2003) A reaction center-light-harvesting 1 complex (RC-LH1) from a Rhodospirillum rubrum mutant with altered esterifying pigments: characterization by optical spectroscopy and cryo-electron microscopy.. J Biol Chem, 278(26), 23678-23685.
• Jamieson SJ, Wang P, Qian P, Kirkland JY, Conroy MJ, Hunter CN & Bullough PA (2002) Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 A resolution.. EMBO J, 21(15), 3927-3935.
• Ruzheinikov SN, Burke J, Sedelnikova S, Baker PJ, Taylor R, Bullough PA, Muir NM, Gore MG & Rice DW (2001) Glycerol dehydrogenase. structure, specificity, and mechanism of a family III polyol dehydrogenase.. Structure, 9(9), 789-802.
• Prince SM, Feron C, Janssens D, Lobet Y, Achtman M, Kusecek B, Bullough PA & Derrick JP (2001) Expression, refolding and crystallization of the OpcA invasin from Neisseria meningitidis.. Acta Crystallogr D Biol Crystallogr, 57(Pt 8), 1164-1166.
• Yin CC, Aldema-Ramos ML, Borges-Walmsley MI, Taylor RW, Walmsley AR, Levy SB & Bullough PA (2000) The quarternary molecular architecture of TetA, a secondary tetracycline transporter from Escherichia coli.. Mol Microbiol, 38(3), 482-492.
• Wallace AJ, Stillman TJ, Atkins A, Jamieson SJ, Bullough PA, Green J & Artymiuk PJ (2000) E. coli hemolysin E (HlyE, ClyA, SheA): X-ray crystal structure of the toxin and observation of membrane pores by electron microscopy.. Cell, 100(2), 265-276.
• Collins R, Achtman M, Ford R, Bullough P & Derrick J (1999) Projection structure of reconstituted Opc outer membrane protein from Neisseria meningitidis. MOL MICROBIOL, 32(1), 217-219.
• Bullough PA & Henderson R (1999) The projection structure of the low temperature K intermediate of the bacteriorhodopsin photocycle determined by electron diffraction.. J Mol Biol, 286(5), 1663-1671.
• Subramaniam S, Lindahl M, Bullough PA, Faruqi AR, Tittor J, Oesterhelt D, Brown L, Lanyi J & Henderson R (1999) Protein Conformational Changes in the Bacteriorhodopsin Photocycle. Journal of Molecular Biology, 287, 145-161.
• Walz T, Jamieson SJ, Bowers CM, Bullough PA & Hunter CN (1998) Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 A, LH1 and RC-LH1 at 25 A.. J Mol Biol, 282(4), 833-845.
• Henderson R, Bullough P, Lindahl M & Subramaniam S (1997) Structural changes underlying proton pumping by Bacteriorhodopsin. FASEB J, 11(9), A992-A992.
• Karrasch S, Bullough PA & Ghosh R (1995) The 8.5 A projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits.. EMBO J, 14(4), 631-638.
• Skehel JJ, Bizebard T, Bullough PA, Hughson FM, Knossow M, Steinhauer DA, Wharton SA & Wiley DC (1995) Membrane fusion by influenza hemagglutinin.. Cold Spring Harb Symp Quant Biol, 60, 573-580.
• Bullough PA, Hughson FM, Skehel JJ & Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion.. Nature, 371(6492), 37-43.
• Bullough PA, Hughson FM, Treharne AC, Ruigrok RW, Skehel JJ & Wiley DC (1994) Crystals of a fragment of influenza haemagglutinin in the low pH induced conformation.. J Mol Biol, 236(4), 1262-1265.
• Bullough PA & Tulloch PA (1991) Spot-scan imaging of microcrystals of an influenza neuraminidase-antibody fragment complex.. Ultramicroscopy, 35(2), 131-143.
• Bullough PA & Tulloch PA (1990) High-resolution spot-scan electron microscopy of microcrystals of an alpha-helical coiled-coil protein.. J Mol Biol, 215(1), 161-173.
• Bullough PA & Henderson R (1990) Phase accuracy in high-resolution electron microscopy of trigonal and orthorhombic purple membrane.. Biophys J, 58(3), 705-711.
• Bullough PA (1990) Imaging of protein molecules--towards atomic resolution.. Electron Microsc Rev, 3(2), 249-267.
• BULLOUGH P & HENDERSON R (1987) USE OF SPOT-SCAN PROCEDURE FOR RECORDING LOW-DOSE MICROGRAPHS OF BEAM-SENSITIVE SPECIMENS. ULTRAMICROSCOPY, 21(3), 223-229.
• Bakker SE, Bergeron J, Bharadwaj A, Bhella D, Bullough P, Chau P-L, Frank RAW, Jakobi AJ, Joseph AP, Kühlbrandt W , Lahiri I et al () Map/model validation and machine learning in EM: general discussion. Faraday Discussions, 240, 229-242.
• Bakker SE, Bhella D, Brescia R, Bullough P, Clare DK, Daum B, Frank RAW, Gold VAM, Jackson Hirst I, Kühlbrandt W , Lu P et al () Pushing the limits in single particle cryo-EM: general discussion. Faraday Discussions, 240, 312-322.
• Al-Otaibi N, Aminian J. A, Anane RF, Baatsen P, Bakker SE, Bergeron J, Bharadwaj A, Bhella D, Braun T, Brescia R , Bullough P et al () Sample preparation in single particle cryo-EM: general discussion. Faraday Discussions, 240, 81-100.
• Al-Otaibi N, Baatsen P, Bhella D, Brescia R, Bullough P, Daum B, de Bruin R, Frank R, Kühlbrandt W, López-Iglesias C , McLaren M et al () Tomographic analysis, CLEM: general discussion. Faraday Discussions, 240, 142-151.
• Janganan TK, Mullin N, Tzokov SB, Stringer S, Fagan RP, Hobbs JK, Moir A & Bullough PA () Characterization of the spore surface and exosporium proteins of Clostridium sporogenes; implications for C. botulinum Group I strains. Food Microbiology, 59, 205-212. View this article in WRRO

Book chapters

• (2021) Refining a correlative light electron microscopy workflow using luminescent metal complexes, Methods in Cell Biology (pp. 69-87). Elsevier
• Bullough P (2013) Electron Diffraction, Encyclopedia of Biophysics (pp. 581-586). Springer Berlin Heidelberg
• Bullough PA, Qian P & Hunter CN (2009) Reaction Center-Light-Harvesting Core Complexes of Purple Bacteria, Advances in Photosynthesis and Respiration (pp. 155-179). Springer Netherlands
• Karrasch S, Bullough PA & Ghosh R (1995) 8.5 Å Projection Map of the Light-Harvesting Complex I from Rhodospirillum Rubrum Reveals a Ring Composed of 16 Subunits, Photosynthesis: from Light to Biosphere (pp. 81-84). Springer Netherlands

Conference proceedings

• Baboolal TG, Conroy MJ, Gill K, Bullough P & Lakey JH (2005) The colicin N- OmpF translocation complex. BIOPHYSICAL JOURNAL, Vol. 88(1) (pp 50A-51A)
• Bullough PA, Jamieson SJ, Walz T, Hunter CN, Bowers CM, Karrasch S, Ghosh R, Henderson R & Subramaniam S (1999) Energy production in biological systems probed by electron crystallography. ELECTRON MICROSCOPY AND ANALYSIS 1999(161) (pp 127-132)
• Bullough PA (1996) Conformational changes in influenza haemagglutinin at the pH of membrane fusion. OPTIONS FOR THE CONTROL OF INFLUENZA III, Vol. 1123 (pp 307-314)
• Karrasch S, Bullough PA & Ghosh R (1995) 8.5 angstrom projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. PHOTOSYNTHESIS: FROM LIGHT TO BIOSPHERE, VOL I (pp 81-84)
• SKEHEL JJ, STEINHAUER D, WHARTON SA, BULLOUGH PA, HUGHSON FM, WATOWICH SJ & WILEY DC (1994) RECEPTOR BINDING AND MEMBRANE FUSION BY INFLUENZA HEMAGGLUTININ. CELLULAR RECEPTORS FOR ANIMAL VIRUSES (pp 187-193)

Datasets

• Lemonche LP, Burns J, Turner R, Kumar S, Tank R, Mullin N, Wilson J, Chakrabarti B, Bullough P, Foster S & Hobbs J (2020) The architecture of the Gram-positive bacterial cell wall.

Preprints

• Stevenson SR, Tzokov SB, Lahiri I, Ayscough KR & Bullough PA (2024) CryoEM Reconstruction of Yeast ADP-Actin Filament at 2.5 Å resolution. A comparison with mammalian and avian F-actin, Cold Spring Harbor Laboratory.
• Janganan TK, Mullin N, Dafis-Sagarmendi A, Brunt J, Tzokov SB, Stringer S, Moir A, Chaudhuri R, Fagan RP, Hobbs JK & Bullough PA (2020) Architecture and self-assembly of theClostridium sporogenes/botulinumspore surface illustrate a general protective strategy across spore formers, Cold Spring Harbor Laboratory.
• Mohasin M, Balbirnie-Cumming K, Fisk E, Prestwich EC, Russell CD, Marshall J, Pridans C, Allen SP, Shaw PJ, De Vos KJ , Hill CJ et al (2019) Mitochondrial fission is increased in macrophages during mROS production in response to S. pneumoniae, Cold Spring Harbor Laboratory.