Spiro Lab

Publications

  1. Ray, A. and Spiro, S. (2023) DksA homologs, ppGpp and RegAB regulate dissimilatory nitrogen metabolism in Paracoccus denitrificans. BioRxiv doi: https://doi.org/10.1101/2023.01.17.523660

  2. Kumar, S. and Spiro, S. (2017) Environmental and genetic determinants of biofilm formation in Paracoccus denitrificans.  mSphere 2: e00350-17.

  3. Spiro, S. (2016) Regulation of denitrification.  In ‘Denitrification’ (Moura, J., Ed.), Royal Society of Chemistry, London, pp. 312-330.

  4. Mehta, H.H., Liu, Y., Zhang, M.Q. and Spiro S. (2015) Genome-wide analysis of the response to nitric oxide in uropathogenic Escherichia coli CFT073.  Microbial Genomics 1: doi:  10.1099/mgen.0.000031 

  5. Chhabra, S. and Spiro, S. (2015) Inefficient translation of nsrR constrains the behaviour of the NsrR regulon in Escherichia coli. Microbiology 161: 2029-2038.

  6. Zeng, J. and Spiro, S. (2013) Finely-tuned regulation of the aromatic amine degradation pathway in Escherichia coli.  Journal of Bacteriology 195: 5141-5150.

  7. McKethan, B.L. and Spiro, S. (2013) Cooperative and allosterically controlled nucleotide binding regulates the DNA binding activity of NrdR.  Molecular Microbiology 90: 278-289.

  8. Spiro, S. and D’Autréaux, B. (2012) Non-heme iron sensors of reactive oxygen and nitrogen species.  Antioxidants and Redox Signaling 17: 1264-1276.

  9. Spiro, S. (2012) Genome-wide mapping of the binding sites of proteins that interact with DNA.  In ‘Microbial systems biology: methods and protocols’ (Navid, A., Ed.), Springer, New York.

  10. Spiro, S. (2012) Nitrous oxide production and consumption: regulation of gene expression by gas-sensitive transcription factors.  Proceedings of the Royal Society B 367: 1213-1225.

  11. Spiro, S. (2011) Nitric oxide stress in Escherichia coli and Salmonella.  pp 48-67 in ‘Stress response in pathogenic bacteria’ (Kidd, S.P., Ed.), CAB International, U.K.

  12. Spiro, S. (2011) Another target for NO.  Cell Host and Microbe 10: 1-2.

  13. Spiro, S. (2011) Nitric oxide metabolism: physiology and regulatory mechanisms.  pp 177-196 in ‘Nitrogen cycling in bacteria. Molecular analysis’ (Moir, J.W.B., Ed.), Caister Academic Press, U.K.

  14. Browning, D.F., Lee, D.J., Spiro, S. and Busby, S.J. (2010) Down-regulation of the Escherichia coli K-12 nrf promoter by binding of the NsrR nitric oxide-sensing transcription repressor to an upstream site.  Journal of Bacteriology 192: 3824-3828.

  15. Wang, Y., Dunn, A.K., Wilneff, J., McFall-Ngai, M.J., Spiro, S. and Ruby, E.G. (2010) Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid-Vibrio symbiosis.  Molecular Microbiology 78: 903-915.

  16. Spiro, S. and Dixon R., Editors. (2010) Sensory mechanisms in bacteria. Molecular aspects of signal recognition. Caister Academic Press, U.K.

  17. Spiro, S. (2010) An alternative route to nitric oxide resistance.  Molecular Microbiology 77: 6-10.

  18. Storz, G. and Spiro, S. (2010) Sensing and responding to reactive oxygen and nitrogen species.  In ‘Bacterial Stress Responses, 2nd Edition’, (Storz, G. and Hengge, R., Eds.), ASM Press, Washington, DC.

  19. Partridge, J.D., Bodenmiller, D.M., Humphrys, M.S. and Spiro, S. (2009). NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility.  Molecular Microbiology 73: 680-694.

  20. Rankin, L.D., Bodenmiller, D.M., Partridge, J.D., Nishino, S.F., Spain, J.C. and Spiro, S. (2008) Escherichia coli NsrR regulates a pathway for the oxidation of 3-nitrotyramine to 4-hydroxy-3-nitrophenylacetate.  Journal of Bacteriology 190: 6170-6177.

  21. Mills, P.C., Rowley, G., Spiro, S., Hinton, J.C.D. and Richardson, D.J. (2008) A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 154: 1218-1228.

  22. Tucker, N.P., D’Autréaux, B., Yousafzai, F., Fairhurst, S., Spiro, S. and Dixon, R. (2008) Analysis of the nitric oxide-sensing non-heme iron center in the NorR regulatory protein.  Journal of Biological Chemistry 208: 908-918.

  23. Spiro, S. (2008) Metalloregulatory proteins and nitric oxide signalling in bacteria.  Biochemical Society Transactions  36: 1160-1164.

  24. Efromovich, S., Grainger, D., Bodenmiller, D. and Spiro, S. (2008) Genome-wide identification of binding sites for the nitric oxide sensitive transcriptional regulator NsrR.  Methods in Enzymology  437: 211-233.

  25. D’Autréaux, B., Tucker, N., Spiro, S. and Dixon, R. (2008) Characterisation of the NO-reactive transcriptional activator NorR.  Methods in Enzymology  437: 235-251.

  26. Clarke, T.A., Mills, P.C., Poock, S.R., Butt, J.N., Cheesman, M.R., Cole, J.A., Hinton, J.C., Hemmings, A.M., Kemp, G., Soderberg, C., Spiro, S., van Wonderen, J. and Richardson, D.J. (2008) Escherichia coli cytochrome c-nitrite reductase.  Methods in Enzymology 437: 263-277.

  27. Filenko, N., Spiro, S., Browning, D.F., Squire, D., Overton, T.W., Cole, J. and Constantinidou, C. (2007) The NsrR regulon of Escherichia coli K12 includes genes encoding the hybrid cluster protein and the periplasmic, respiratory nitrite reductase.  Journal of Bacteriology  189: 4410-4417.

  28. Spiro, S. (2007) Regulators of bacterial responses to nitric oxide.  FEMS Microbiology Reviews  31: 193-211.  

  29. Lee, Y-Y., Shearer, N. and Spiro, S. (2006) Transcription factor NNR from Paracoccus denitrificans is a sensor of both nitric oxide and oxygen: isolation of nnr* alleles encoding effector-independent proteins and evidence for a haem-based sensing mechanism.  Microbiology 152: 1461-1470.

  30. Bodenmiller, D.M. and Spiro, S. (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide sensitive regulator of transcription.  Journal of Bacteriology 188: 874-881.

  31. Spiro, S. (2006) Nitric oxide sensing mechanisms in Escherichia coli.  Biochemical Society Transactions 34: 200-202.

  32. Tucker, N.P., D’Autréaux, B., Spiro, S. and Dixon, R. (2006) Mechanism of transcriptional regulation by the Escherichia coli nitric oxide sensor NorR. Biochemical Society Transactions 34: 191-194.  

  33. D’Autréaux, B., Tucker, N.P., Dixon, R. and Spiro, S. (2005) A non-haem iron centre in the transcription factor NorR senses nitric oxide.  Nature 437: 769-772.

  34. Spreadbury, C.L., Pallen, M.J., Overton, T., Behr, M.A., Mostowy, S., Spiro, S., Busby, S.J.W. and Cole, J.A. (2005) Point mutations in the DNA- and cNMP-binding domains of the homologue of the cAMP receptor protein (CRP) in Mycobacterium bovis BCG: implications for the inactivation of a global regulator and strain attenuation. Microbiology 151: 547-556.

  35. Mills, P.C., Richardson, D.J., Hinton, J.C. and Spiro, S. (2005) Detoxification of nitric oxide by the flavorubredoxin of Salmonella enterica serovar Typhimurium.  Biochemical Society Transactions 33: 198-199.

  36. Tucker, N., D’Autréaux, B., Spiro, S. and Dixon, R. (2005) DNA binding properties of the Escherichia coli nitric oxide sensor NorR: towards an understanding of the regulation of flavorubredoxin expression.  Biochemical Society Transcations 33: 181-183.

  37. Tucker, N.P., D’Autréaux, B., Studholme, D.J., Spiro, S. and Dixon, R. (2004) DNA binding activity of the Escherichia coli nitric oxide sensor NorR suggests a conserved target sequence in diverse proteobacteria. Journal of Bacteriology 186: 6656-6660.

  38. Taylor, C.J., Bain, L.A., Richardson, D.J., Spiro, S. and Russell, D.A. (2004) Construction of a whole cell reporter for the fluorescent bioassay of nitrate. Analytical Biochemistry 328: 60-66.

  39. Malone, S.A., Lewin, A., Kilic, M.A., Svistunenko, D.A., Cooper, C.E., Wilson, M.T., Le Brun, N.E., Spiro, S. and Moore, G.R. (2004) Protein-template-driven formation of polynuclear iron species. Journal of the American Chemical Society 126: 406-594.

  40. Kilic, M.A., Spiro, S. and Moore, G.R. (2003) Stability of a 24-meric homopolymer: comparative studies of assembly-defective mutants of Rhodobacter capsulatus bacterioferritin and the native protein. Protein Science 12: 1663-1674.

  41. Ellington, M.J.K., Sawers, G., Sears, H.J., Spiro, S., Richardson, D.J. and Ferguson, S.J. (2003) Characterization of the expression and activity of the periplasmic nitrate reductase of Paracoccus pantotrophus in chemostat cultures. Microbiology 149: 1533-1540.

  42. Gregory, L.G., Bond, P.L., Richardson, D.J. and Spiro, S. (2003) Characterisation of a nitrate respiring bacterial community using the nitrate reductase gene (narG) as a functional marker. Microbiology 149: 229-237.

  43. Hutchings, M.I., Mandhana, N. and Spiro, S. (2002) The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species. Journal of Bacteriology 184: 4640-4643.

  44. Lewin, A.C., Doughty, P.A, Flegg, L., Moore, G.R. and Spiro, S. (2002) The ferric uptake regulator of Pseudomonas aeruginosa has no essential cysteine residues and does not contain a structural zinc ion. Microbiology 148: 2449-2456.

  45. Field, S.J., Prior, L., Roldán, M.D., Cheesman, M.R., Thomson, A.J., Spiro, S., Butt, J., Watmough, N.J. and Richardson, D.J. (2002) Spectral properties of bacterial nitric oxide reductase: resolution of pH dependent forms of the active site heme b3. Journal of Biological Chemistry 277: 20146-20150.

  46. Hutchings, M.I., Crack, J.C., Shearer, N., Thompson, B.J., Thomson, A.J. and Spiro, S. (2002) Transcription factor FnrP from Paracoccus denitrificans contains an iron-sulfur cluster and is activated by anoxia: identification of essential cysteine residues. Journal of Bacteriology 184: 503-508.

  47. Butland, G., Spiro, S., Watmough, N.J. and Richardson, D.J. (2001) Two conserved glutamates in the bacterial nitric oxide reductase are essential for activity but not assembly of the enzyme. Journal of Bacteriology 183: 189-199.

  48. Richardson, D.J., Berks, B.C., Russell, D.A., Spiro, S. and Taylor, C.J. (2001)  Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cellular and Molecular Life Sciences 58: 165-178.

  49. Hutchings, M.I., Shearer, N., Wastell, S., Van Spanning, R.J.M. and Spiro, S (2000) Heterologous NNR-mediated nitric oxide signaling in Escherichia coli. Journal of Bacteriology 182: 6434-6439.

  50. Hutchings, M.I. and Spiro, S. (2000) The nitric oxide regulated nor promoter of Paracoccus denitrificans.  Microbiology 146: 2635-2641.

  51. Gregory, L.G., Karakas-Sen, A., Richardson, D.J. and Spiro, S. (2000) Detection of genes for membrane-bound nitrate reductase in nitrate-respiring bacteria and in community DNA. FEMS Microbiology Letters 183: 273-279.

  52. Shearer, N., Hinsley, A.P., Van Spanning, R.J.M. and Spiro, S. (1999) Anaerobic growth of Paracoccus denitrificans requires cobalamin: characterization of cobK and cobJ genes.  Journal of Bacteriology 181: 6907-6913.

  53. Grönberg, K.L.C., Roldán, M.D., Prior, L., Butland, G., Cheesman, M.R., Richardson, D.J., Spiro, S., Thomson, A.J. and Watmough, N.J. (1999) A low-redox potential heme in the dinuclear center of bacterial nitric oxide reductase: implications for the evolution of energy-conserving heme-copper oxidases. Biochemistry 38: 13780-13786.

  54. Flanagan, D.A., Gregory, L.G., Carter, J.P., Karakas-Sen, A., Richardson, D.J. and Spiro, S. (1999) Detection of genes for periplasmic nitrate reductase in nitrate-respiring bacteria and in community DNA. FEMS Microbiology Letters 177: 263-270.

  55. Van Spanning, R.J.M., Houben, E., Reijnders, W.N.M., Spiro, S., Westerhoff, H.V. and Saunders, N. (1999) Nitric oxide is a signal for NNR-mediated transcription activation in Paracoccus denitrificans. Journal of Bacteriology 181: 4129-4132.

  56. Watmough, N.J., Butland, G., Cheesman, M.R., Moir, J.W.B., Richardson, D.J. and Spiro, S. (1999) Nitric oxide in bacteria synthesis and consumption. Biochemica et Biophysica Acta 1411: 456-474.

  57. Spiro, S., Kilic, M.A., Lewin, A., Dobbin-Namiranian, S., Thomson, A.J. and Moore, G.R. (1999)  Interactions of heme and other metal ion complexes with the bacterial Fe-uptake regulatory protein and with bacterioferritin.  pp 211-226 in ‘Iron metabolism. Inorganic biochemistry and regulatory mechanisms’ (Ferreira, G.C., Moura, J.J.G. and Franco, R. eds.) Wiley-VCH, Germany.

  58. Richardson, D.J., Wehrfritz, J-M., Keech, A., Crossman, L.C., Roldan, M.D., Sears, H.J., Butler, C.S., Reilly, A., Moir, J.W.B., Berks, B.C., Ferguson, S.J., Thomson, A.J. and Spiro, S. (1998)  The diversity of redox proteins involved in bacterial heterotrophic nitrification and aerobic denitrification. Biochemical Society Transactions 26: 401-408.

  59. Crossman, L.C., Moir, J.W.B., Spiro, S. and Richardson, D.J. (1998) Heterotrophic nitrification in Paracoccus denitrificans. Biochemical Society Transactions 26: S208.

  60. Richardson, D.J., Sears, H.J., Berks, B.C., Ferguson, S.J. and Spiro, S. (1998) The bacterial nitrate reductases.  pp 565-574 in ‘Avances en el metabolismo del nitrogeno: de la fisiologia a la biologia molecular’ (Vega, J.M., Aparicio, P.J., Castillo, F. and Maldonado, J.M., Eds.) Servicio de Publicaciones, Universidad de Sevilla, Sevilla.

  61. Crossman, L.C., Moir, J.W.B., Enticknap, J., Richardson, D.J. and Spiro, S. (1997) Heterologous expression of heterotrophic nitrification genes. Microbiology 143: 3775-3783.

  62. Sears, H.J., Spiro, S. and Richardson, D.J. (1997) The effect of carbon substrate and aeration on nitrate reduction and expression of the periplasmic and membrane-bound nitrate reductases in carbon-limited continuous cultures of Paracoccus denitrificans. Microbiology 143: 3767-3774.

  63. Wehrfritz, J.M., Carter, J.P., Spiro, S. and Richardson, D.J. (1997) Hydroxylamine oxidation in heterotrophic nitrate reducing soil bacteria and purification of a hydroxylamine-cytochrome c oxidoreductase from a Pseudomonas species. Archives of Microbiology 166: 421-424.

  64. Sears, H.J., Little, P.J., Richardson, D.J., Berks, B.C., Spiro, S. and Ferguson, S.J. (1997) Identification of an assimilatory nitrate reductase in mutants of Paracoccus denitrificans GB17 deficient in nitrate respiration. Archives of Microbiology 167: 61-66.

  65. Moir, J.W.B., Crossman, L.C., Spiro, S. and Richardson, D.J. (1996) The purification of ammonia monooxygenase from Paracoccus denitrificans.  FEBS Letters 387: 71-74.

  66. Penfold, C.N., Ringeling, P.L., Davy, S.L., Moore, G.R., McEwan, A.G. and Spiro, S. (1996) Isolation, characterisation and expression of the bacterioferritin gene of Rhodobacter capsulatus.  FEMS Microbiology Letters 139: 143-148.

  67. Moir, J.W.B., Wehrfritz, J-M., Spiro, S. and Richardson, D.J. (1996) The biochemical characterisation of a novel non-haem iron hydroxylamine oxidase from Paracoccus denitrificans  GB17. Biochemical Journal 319: 823-827.

  68. Bishop, N.D., Lea, E.J.A., Mobasheri, H. and Spiro, S. (1996) Altered voltage sensitivity of mutant OmpC porin channels.  FEBS Letters 379: 295-298.

  69. Guest, J.R., Green, J., Irvine, A.S. and Spiro, S. (1996) The FNR modulon and FNR-regulated gene expression.  pp 317-342 in ‘Regulation of gene expression in Escherichia coli’  (Lin, E.C.C. and Lynch, A.S. Eds)  R.G. Landes Co., Austin, Texas.

  70. Van Spanning, R.J.M., De Boer, A.P.N., Reijnders, W.N.M., Spiro, S., Westerhoff, H.V., Stouthamer, A.H. and Van der Oost, J. (1995) Nitrite and nitric oxide reduction in Paracoccus denitrificans is under the control of NNR, a regulatory protein that belongs to the FNR family of transcriptional activators.  FEBS Letters 360: 151-154.

  71. Carter, J.P., Richardson, D.J. and Spiro, S. (1995) Isolation and characterisation of a strain of Pseudomonas putida that can express a periplasmic nitrate reductase. Archives of Microbiology 163: 159-166.

  72. Carter, J.P., Hsiao, Y.H., Spiro, S. and Richardson, D.J. (1995) Soil and sediment bacteria capable of aerobic nitrate respiration. Applied and Environmental Microbiology 61: 2852-2858.

  73. Sears, H.J., Bennett, B., Spiro, S., Thomson, A.J. and Richardson, D.J. (1995) Identification of periplasmic nitrate reductase Mo(V) EPR signals in intact cells of Paracoccus denitrificans. Biochemical Journal 310: 311-314.

  74. Hinsley, A.P., Duchars, M.G. and Spiro, S. (1995) Transcriptional regulation of denitrification genes in Paracoccus denitrificans.  Biochemical Society Transactions 23: 126S.

  75. Kucera, I., Matchova, I. and Spiro, S. (1994) Respiratory inhibitors activate an FNR-like regulatory protein in Paracoccus denitrificans: implications for the regulation of the denitrification pathway. Biochemistry and Molecular Biology International 32: 245-250.

  76. Spiro, S. (1994) The FNR family of transcriptional regulators. Antonie van Leeuwenhoek 66: 23-36.

  77. Sears, H.J., Ferguson, S.J., Richardson, D.J. and Spiro, S. (1993) The identification of a periplasmic nitrate reductase in Paracoccus denitrificans. FEMS Microbiology Letters 113: 107-112.

  78. Wehrfritz, J-M., Reilly, A., Spiro, S. and Richardson, D.J. (1993) Purification of hydroxylamine oxidase from Thiosphaera pantotropha: identification of electron acceptors that couple heterotrophic nitrification to aerobic denitrification. FEBS Letters 335: 246-250.

  79. Spiro, S. (1992) An FNR-dependent promoter from Escherichia coli is active and anaerobically inducible in Paracoccus denitrificans. FEMS Microbiology Letters 98: 145-148.

  80. Spiro, S. and Guest, J.R. (1991) Adaptive responses to oxygen limitation in Escherichia coli. Trends in Biochemical Sciences 16: 310-314.

  81. Trageser, M., Spiro, S., Duchene, A., Kojro, E., Fahrenholz, F., Guest, J.R. and Unden, G. (1990) Isolation of intact FNR protein (Mr 30 000) of Escherichia coli. Molecular Microbiology 4: 21-27.

  82. Spiro, S., Gaston, K.L., Bell, A.I., Roberts, R.E., Busby, S.J.W. and Guest, J.R. (1990) Interconversion of the DNA-binding specificities of two transcription regulators, CRP and FNR. Molecular Microbiology 4: 1831-1838.

  83. Spiro, S. and Guest, J.R. (1990) FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiology Reviews 75: 399-428.

  84. Guest, J.R., Green, J., Spiro, S., Prodromou, C. and Sharrocks, A.D. (1990) Regulation of gene expression by oxygen in Escherichia coli. In ‘The molecular basis of bacterial metabolism’ (Hanska, G. and Thauer, R., Eds) pp 134-145, Springer, Heidelberg.

  85. Spiro, S., Roberts, R.E. and Guest, J.R. (1989) FNR-dependent repression of the ndh gene of Escherichia coli and metal ion requirement for FNR-regulated gene expression. Molecular Microbiology 3: 601-608.

  86. Spiro, S. and Guest, J.R. (1988) Inactivation of the FNR protein of Escherichia coli by targeted mutagenesis in the N -terminal region. Molecular Microbiology 2: 701-707.

  87. Wright, J.J., Spiro, S., Howe, K.M. and Hayward, R. (1988) Neither strong promoter of the rpoKAJL rpoBC operon is subject to stringent control in Escherichia coli. Molecular Genetics (Life Science Advances) 7: 201-205.

  88. Spiro, S., Todd, M.H., Artymiuk, P.J. and Guest, J.R. (1988) A proposal for the DNA-binding specificity of the FNR protein of E. coli. Biochemical Society Transactions 16: 755-756.

  89. Spiro, S. and Guest, J.R. (1987) Regulation and over-expression of the fnr gene of Escherichia coli. Journal of General Microbiology 133: 3279-3288.

  90. Spiro, S. and Guest, J.R. (1987) Regulation of fnr gene expression in Escherichia coli and over-production of the FNR protein. Biochemical Society Transactions 15: 909-911.  

  91. Spiro, S. and Guest, J.R. (1987) Activation of the lac operon of Escherichia coli by a mutant FNR protein. Molecular Microbiology 1: 53-58.