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Recent advances in the biosynthesis of modified tetrapyrroles: the discovery of an alternative pathway for the formation of heme and heme d 1

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Abstract

Hemes (a, b, c, and o) and heme d 1 belong to the group of modified tetrapyrroles, which also includes chlorophylls, cobalamins, coenzyme F430, and siroheme. These compounds are found throughout all domains of life and are involved in a variety of essential biological processes ranging from photosynthesis to methanogenesis. The biosynthesis of heme b has been well studied in many organisms, but in sulfate-reducing bacteria and archaea, the pathway has remained a mystery, as many of the enzymes involved in these characterized steps are absent. The heme pathway in most organisms proceeds from the cyclic precursor of all modified tetrapyrroles uroporphyrinogen III, to coproporphyrinogen III, which is followed by oxidation of the ring and finally iron insertion. Sulfate-reducing bacteria and some archaea lack the genetic information necessary to convert uroporphyrinogen III to heme along the “classical” route and instead use an “alternative” pathway. Biosynthesis of the isobacteriochlorin heme d 1, a cofactor of the dissimilatory nitrite reductase cytochrome cd 1, has also been a subject of much research, although the biosynthetic pathway and its intermediates have evaded discovery for quite some time. This review focuses on the recent advances in the understanding of these two pathways and their surprisingly close relationship via the unlikely intermediate siroheme, which is also a cofactor of sulfite and nitrite reductases in many organisms. The evolutionary questions raised by this discovery will also be discussed along with the potential regulation required by organisms with overlapping tetrapyrrole biosynthesis pathways.

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References

  1. Battersby AR (2000) Tetrapyrroles: the pigments of life. Nat Prod Rep 17(6):507–526. doi:10.1039/b002635m

    CAS  PubMed  Google Scholar 

  2. Rudiger W (1997) Chlorophyll metabolism: from outer space down to the molecular level. Phytochemistry 46(7):1151–1167. doi:10.1016/S0031-9422(97)00449-4

    CAS  Google Scholar 

  3. Moulin M, Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Paper presented at the Conference on coenzymology: biochemistry of vitamin biogenesis and cofactor-containing enzymes. King Coll, Cambridge

    Google Scholar 

  4. Lockhart PJ, Larkum AWD, Steel MA, Waddell PJ, Penny D (1996) Evolution of chlorophyll and bacteriochlorophyll: the problem of invariant sites in sequence analysis. Proc Natl Acad Sci USA 93(5):1930–1934. doi:10.1073/pnas.93.5.1930

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23(3):94–97. doi:10.1016/S0968-0004(98)01186-4

    CAS  PubMed  Google Scholar 

  6. Friedmann HC, Thauer RK (1992) Macrocyclic tetrapyrrole biosynthesis in bacteria. Encyclopedia of microbiology, vol 1-4. Academic Press, New York, pp 1–19

    Google Scholar 

  7. Thauer RK, Bonacker LG (1994) Biosynthesis of coenzyme F430, a nickel porphinoid involved in methanogenesis. In: Chadwick DJA (ed) Biosynthesis of the tetrapyrrole pigments, vol 180. CIBA Foundation Symposia, John Wiley & Sons Ltd, Chichester, pp 210–222 discussion 222–217

    Google Scholar 

  8. Friedmann HC, Klein A, Thauer RK (1991) Biochemistry of coenzyme F430 a nickel porphinoid involved in methanogenesis. In: Jordan PME (ed) New comprehensive biochemistry, vol 19. Elsevier Science Publishers B.V, New York, pp 139–154

    Google Scholar 

  9. O’Brian MR, Thony-Meyer L (2002) Biochemistry, regulation and genomics of haem biosynthesis in prokaryotes. Adv Microb Physiol 46:257–318. doi:10.1016/S0065-2911(02)46006-7

    PubMed  Google Scholar 

  10. Layer G, Reichelt J, Jahn D, Heinz DW (2010) Structure and function of enzymes in heme biosynthesis. Protein Sci 19(6):1137–1161. doi:10.1002/pro.405

    CAS  PubMed Central  PubMed  Google Scholar 

  11. Bernhardt R (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124(1):128–145. doi:10.1016/j.jbiotec.2006.01.026

    CAS  PubMed  Google Scholar 

  12. Sono M, Roach MP, Coulter ED, Dawson JH (1996) Heme-containing oxygenases. Chem Rev 96(7):2841–2888. doi:10.1021/cr9500500

    CAS  PubMed  Google Scholar 

  13. Wilks A, Burkhard KA (2007) Heme and virulence: how bacterial pathogens regulate, transport and utilize heme. Nat Prod Rep 24(3):511–522. doi:10.1039/b604193k

    CAS  PubMed  Google Scholar 

  14. Zajicek RS, Bali S, Arnold S, Brindley AA, Warren MJ, Ferguson SJ (2009) d 1 haem biogenesis: assessing the roles of three nir gene products. FEBS J 276(21):6399–6411. doi:10.1111/j.1742-4658.2009.07354.x

    CAS  PubMed  Google Scholar 

  15. Simon J, Kroneck PM (2013) Microbial sulfite respiration. Adv Microb Physiol 62:45–117. doi:10.1016/B978-0-12-410515-7.00002-0

    CAS  PubMed  Google Scholar 

  16. Wilks A (2002) Analysis of heme and hemoproteins. In: Alison G, Smith MW (eds) Heme, chlorophyll, and bilines. Humana Press, Totova, pp 157–184

    Google Scholar 

  17. Sanders CTS, Onder O, Frawley ER, Kranz RG, Koch HG, Daldal F (2009) Biogenesis of c-type cytochromes and cytochrome complexes. In: Hunter NCDF, Thurnauer MC, Beatty JT (eds) The purple phototrophic bacteria, vol 28. Springer Science + Business Media B.V, Netherlands, pp 407–423

    Google Scholar 

  18. Kranz RG, Richard-Fogal C, Taylor JS, Frawley ER (2009) Cytochrome c biogenesis: mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol Mol Biol Rev 73(3):510–528. doi:10.1128/MMBR.00001-09 Table of Contents

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Hederstedt L (2012) Heme a biosynthesis. Biochim Biophys Acta 1817(6):920–927. doi:10.1016/j.bbabio.2012.03.025

    CAS  PubMed  Google Scholar 

  20. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647. doi:10.1146/annurev.micro.58.030603.123811

    CAS  PubMed  Google Scholar 

  21. DeRosa MC, Crutchley RJ (2002) Photosensitized singlet oxygen and its applications. Coordin Chem Rev 233:351–371. doi:10.1016/S0010-8545(02)00034-6

    Google Scholar 

  22. Dougherty TJ (1987) Photosensitizers: therapy and detection of malignant tumors. Photochem Photobiol 45(6):879–889. doi:10.1111/j.1751-1097.1987.tb07898.x

    CAS  PubMed  Google Scholar 

  23. Demidova TN, Hamblin MR (2004) Photodynamic therapy targeted to pathogens. Int J Immunopathol Pharmacol 17(3):245–254

    CAS  PubMed Central  PubMed  Google Scholar 

  24. Chang CK (1985) On the structure of heme-d 1: an isobacteriochlorin derivative as the prosthetic group of dissimilatory nitrite reductase. J Biol Chem 260(17):9520–9522

    CAS  PubMed  Google Scholar 

  25. Chang CK, Timkovich R, Wu W (1986) Evidence that heme d 1 is a 1,3-porphyrindione. Biochemistry 25(26):8447–8453. doi:10.1021/bi00374a019

    CAS  PubMed  Google Scholar 

  26. Chang CK, Wu W (1986) The porphinedione structure of heme-d 1: synthesis and spectral properties of model compounds of the prosthetic group of dissimilatory nitrite reductase. J Biol Chem 261(19):8593–8596

    CAS  PubMed  Google Scholar 

  27. Carlson CA, Ingraham JL (1983) Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans. Appl Environ Microbiol 45(4):1247–1253

    CAS  PubMed Central  PubMed  Google Scholar 

  28. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):533–616

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Jones WL, Schroeder ED, Wilderer PA (1990) Denitrification in a batch waste-water treatment system using sequestered organic-substances. Res J Water Pollut C 62(3):259–267

    CAS  Google Scholar 

  30. Tavares P, Pereira AS, Moura JJG, Moura I (2006) Metalloenzymes of the denitrification pathway. J Inorg Biochem 100(12):2087–2100. doi:10.1016/j.jinorgbio.2006.09.003

    CAS  PubMed  Google Scholar 

  31. Fulop V, Moir JWB, Ferguson SJ, Hajdu J (1995) The anatomy of a bifunctional enzyme: structural basis for reduction of oxygen to water and synthesis of nitric-oxide by cytochrome cd 1. Cell 81(3):369–377. doi:10.1016/0092-8674(95)90390-9

    CAS  PubMed  Google Scholar 

  32. Pearson IV, Page MD, van Spanning RJM, Ferguson SJ (2003) A mutant of Paracoccus denitrificans with disrupted genes coding for cytochrome c 550 and pseudoazurin establishes these two proteins as the in vivo electron donors to cytochrome cd 1 nitrite reductase. J Bacteriol 185(21):6308–6315. doi:10.1128/jb.185.21.6308-6315.2003

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Allen JW, Ferguson SJ, Fülöp V (2011) Cytochrome cd 1 nitrite reductase. Encyclop Inorgan Bioinorgan Chem. doi:10.1002/9781119951438.eibc0557

    Google Scholar 

  34. Zajicek RS, Cartron ML, Ferguson SJ (2006) Probing the unusual oxidation/reduction behavior of Paracoccus pantotrophus cytochrome cd 1 nitrite reductase by replacing a switchable methionine heme iron ligand with histidine. Biochemistry 45(37):11208–11216. doi:10.1021/bi0604983

    CAS  PubMed  Google Scholar 

  35. Radoul M, Bykov D, Rinaldo S, Cutruzzola F, Neese F, Goldfarb D (2011) Dynamic hydrogen-bonding network in the distal pocket of the nitrosyl complex of P. aeruginosa cd 1 nitrite reductase. J Am Chem Soc 133(9):3043–3055. doi:10.1021/ja109688w

    CAS  PubMed  Google Scholar 

  36. Shemin D, Rittenberg D (1946) The biological utilization of glycine for the synthesis of the protoporphyrin of hemoglobin. J Biol Chem 166(2):621–625

    CAS  PubMed  Google Scholar 

  37. Kikuchi G, Kumar A, Talmage P, Shemin D (1958) The enzymatic synthesis of delta-aminolevulinic acid. J Biol Chem 233(5):1214–1219

    CAS  PubMed  Google Scholar 

  38. Beale SI, Castelfranco PA (1973) 14 C incorporation from exogenous compounds into––aminolevulinic acid by greening cucumber cotyledons. Biochem Biophys Res Commun 52(1):143–149. doi:10.1016/0006-291X(73)90966-2

    CAS  PubMed  Google Scholar 

  39. Jahn D, Heinz DW (2009) Biosynthesis of 5-aminolevulinic acid. In: Warren MJ, Smith AG (eds) Tetrapyrroles: birth, life, and death. Landes Bioscience, Austin. doi:10.1007/978-0-387-78518-9_2

    Google Scholar 

  40. Weinstein JD, Beale SI (1983) Separate physiological roles and subcellular compartments for two tetrapyrrole biosynthetic pathways in Euglena gracilis. J Biol Chem 258(11):6799–6807

    CAS  PubMed  Google Scholar 

  41. Iida K, Mimura I, Kajiwara M (2002) Evaluation of two biosynthetic pathways to delta-aminolevulinic acid in E. gracilis. Eur J Biochem 269(1):291–297. doi:10.1046/j.0014-2956.2001.02651.x

    CAS  PubMed  Google Scholar 

  42. Cavallaro G, Decaria L, Rosato A (2008) Genome-based analysis of heme biosynthesis and uptake in prokaryotic systems. J Proteome Res 7(11):4946–4954. doi:10.1021/pr8004309

    CAS  PubMed  Google Scholar 

  43. Ishida T, Yu L, Akutsu H, Ozawa K, Kawanishi S, Seto A, Inubushi T, Sano S (1998) A primitive pathway of porphyrin biosynthesis and enzymology in D. vulgaris. Proc Natl Acad Sci USA 95(9):4853–4858. doi:10.1073/pnas.95.9.4853

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Bali S, Lawrence AD, Lobo SA, Saraiva LM, Golding BT, Palmer DJ, Howard MJ, Ferguson SJ, Warren MJ (2011) Molecular hijacking of siroheme for the synthesis of heme and d 1 heme. Proc Natl Acad Sci USA 108(45):18260–18265. doi:10.1073/pnas.1108228108

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Muir HM, Neuberger A (1950) The biogenesis of porphyrins. 2. The origin of the methyne carbon atoms. Biochem J 47(1):97–104

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Ferreira GC, Gong J (1995) 5-aminolevulinate synthase and the first step of heme-biosynthesis. J Bioenerg Biomembr 27(2):151–159. doi:10.1007/Bf02110030

    CAS  PubMed  Google Scholar 

  47. Fanica-Gaignier M, Clement-Metral J (1973) 5-aminolevulinic-acid synthetase of Rhodopseudomonas spheroides Y. kinetic mechanism and inhibition by ATP. Eur J Biochem 40(1):19–24. doi:10.1111/j.1432-1033.1973.tb03164.x

    CAS  PubMed  Google Scholar 

  48. Astner I, Schulze JO, van den Heuvel J, Jahn D, Schubert WD, Heinz DW (2005) Crystal structure of 5-aminolevulinate synthase, the first enzyme of heme biosynthesis, and its link to XLSA in humans. EMBO J 24(18):3166–3177. doi:10.1038/sj.emboj.7600792

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Beale SI, Gough SP, Granick S (1975) Biosynthesis of delta-aminolevulinic acid from the intact carbon skeleton of glutamic acid in greening barley. Proc Natl Acad Sci USA 72(7):2719–2723. doi:10.1073/pnas.72.7.2719

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Schon A, Krupp G, Gough S, Berry-Lowe S, Kannangara CG, Soll D (1986) The RNA required in the first step of chlorophyll biosynthesis is a chloroplast glutamate tRNA. Nature 322(6076):281–284. doi:10.1038/322281a0

    CAS  PubMed  Google Scholar 

  51. Moser J, Lorenz S, Hubschwerlen C, Rompf A, Jahn D (1999) Methanopyrus kandleri glutamyl-tRNA reductase. J Biol Chem 274(43):30679–30685. doi:10.1074/jbc.274.43.30679

    CAS  PubMed  Google Scholar 

  52. Chen MW, Jahn D, O’Neill GP, Soll D (1990) Purification of the glutamyl-tRNA reductase from Chlamydomonas reinhardtii involved in delta-aminolevulinic acid formation during chlorophyll biosynthesis. J Biol Chem 265(7):4058–4063

    CAS  PubMed  Google Scholar 

  53. Hoober JK, Kahn A, Ash DE, Gough S, Kannangara CG (1988) Biosynthesis of delta-aminolevulinate in greening barley leaves. IX. Structure of the substrate, mode of gabaculine inhibition, and the catalytic mechanism of glutamate 1-semialdehyde aminotransferase. Carlsberg Res Commun 53(1):11–25. doi:10.1007/BF02908411

    CAS  PubMed  Google Scholar 

  54. Hennig M, Grimm B, Contestabile R, John RA, Jansonius JN (1997) Crystal structure of glutamate-1-semialdehyde aminomutase: an alpha2-dimeric vitamin B6-dependent enzyme with asymmetry in structure and active site reactivity. Proc Natl Acad Sci USA 94(10):4866–4871. doi:10.1073/pnas.94.10.4866

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Moser J, Schubert WD, Beier V, Bringemeier I, Jahn D, Heinz DW (2001) V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. EMBO J 20(23):6583–6590. doi:10.1093/emboj/20.23.6583

    CAS  PubMed Central  PubMed  Google Scholar 

  56. Schulze JO, Schubert WD, Moser J, Jahn D, Heinz DW (2006) Evolutionary relationship between initial enzymes of tetrapyrrole biosynthesis. J Mol Biol 358(5):1212–1220. doi:10.1016/j.jmb.2006.02.064

    CAS  PubMed  Google Scholar 

  57. Luer C, Schauer S, Mobius K, Schulze J, Schubert WD, Heinz DW, Jahn D, Moser J (2005) Complex formation between glutamyl-tRNA reductase and glutamate-1-semialdehyde 2,1-aminomutase in E. coli during the initial reactions of porphyrin biosynthesis. J Biol Chem 280(19):18568–18572. doi:10.1074/jbc.M500440200

    PubMed  Google Scholar 

  58. Nogaj LA, Beale SI (2005) Physical and kinetic interactions between glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase of Chlamydomonas reinhardtii. J Biol Chem 280(26):24301–24307. doi:10.1074/jbc.M502483200

    CAS  PubMed  Google Scholar 

  59. Deery E, Schroeder S, Lawrence AD, Taylor SL, Seyedarabi A, Waterman J, Wilson KS, Brown D, Geeves MA, Howard MJ, Pickersgill RW, Warren MJ (2012) An enzyme-trap approach allows isolation of intermediates in cobalamin biosynthesis. Nat Chem Biol 8(11):933–940. doi:10.1038/nchembio.1086

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Gibson KD, Neuberger A, Scott JJ (1954) The enzymic conversion of delta-aminolaevulic acid to porphobilinogen. Biochem J 58(4):xli–xlii

    CAS  PubMed  Google Scholar 

  61. Bollivar DW, Clauson C, Lighthall R, Forbes S, Kokona B, Fairman R, Kundrat L, Jaffe EK (2004) Rhodobacter capsulatus porphobilinogen synthase, a high activity metal ion independent hexamer. BMC Biochem 5:17. doi:10.1186/1471-2091-5-17

    PubMed Central  PubMed  Google Scholar 

  62. Senior NM, Brocklehurst K, Cooper JB, Wood SP, Erskine P, Shoolingin-Jordan PM, Thomas PG, Warren MJ (1996) Comparative studies on the 5-aminolaevulinic acid dehydratases from Pisum sativum, E. coli and S. cerevisiae. Biochem J 320(Pt 2):401–412

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Jaffe EK (2000) The porphobilinogen synthase family of metalloenzymes. Acta Crystallogr D Biol Crystallogr 56(Pt 2):115–128. doi:10.1107/S0907444999014894

    CAS  PubMed  Google Scholar 

  64. Shoolingin-Jordan PM, Spencer P, Sarwar M, Erskine PE, Cheung KM, Cooper JB, Norton EB (2002) 5-aminolaevulinic acid dehydratase: metals, mutants and mechanism. Paper presented at the Colloquium on Tetrapyrroles: Their Life, Birth and Death Heriot-Watt, Edinburgh

    Google Scholar 

  65. Frankenberg N, Erskine PT, Cooper JB, Shoolingin-Jordan PM, Jahn D, Heinz DW (1999) High-resolution crystal structure of a Mg2+-dependent porphobilinogen synthase. J Mol Biol 289(3):591–602. doi:10.1006/jmbi.1999.2808

    CAS  PubMed  Google Scholar 

  66. Erskine PT, Newbold R, Brindley AA, Wood SP, Shoolingin-Jordan PM, Warren MJ, Cooper JB (2001) The X-ray structure of yeast 5-aminolaevulinic acid dehydratase complexed with substrate and three inhibitors. J Mol Biol 312(1):133–141. doi:10.1006/jmbi2001.4947

    CAS  PubMed  Google Scholar 

  67. Erskine PT, Norton E, Cooper JB, Lambert R, Coker A, Lewis G, Spencer P, Sarwar M, Wood SP, Warren MJ, Shoolingin-Jordan PM (1999) X-ray structure of 5-aminolaevulinic acid dehydratase from E. coli complexed with the inhibitor levulinic acid at 2.0-A resolution. Biochemistry 38(14):4266–4276. doi:10.1021/bi982137w

    CAS  PubMed  Google Scholar 

  68. Warren MJ, Jordan PM (1988) Investigation into the nature of substrate binding to the dipyrromethane cofactor of E. coli porphobilinogen deaminase. Biochemistry 27(25):9020–9030. doi:10.1021/bi00425a021

    CAS  PubMed  Google Scholar 

  69. Awan SJ, Siligardi G, Shoolingin-Jordan PM, Warren MJ (1997) Reconstitution of the holoenzyme form of E. coli porphobilinogen deaminase from apoenzyme with porphobilinogen and pre-uroporphyrinogen: a study using circular dichroism spectroscopy. Biochemistry 36(30):9273–9282. doi:10.1021/bi9702602

    CAS  PubMed  Google Scholar 

  70. Hart GJ, Miller AD, Leeper FJ, Battersby AR (1987) Biosynthesis of the natural porphyrins: proof that hydroxymethylbilane synthase (Porphobilinogen Deaminase) uses a novel binding group in its catalytic action. J Chem Soc Chem Comm 23:1762–1764. doi:10.1039/C39870001762

    Google Scholar 

  71. Warren MJ, Scott AI (1990) Tetrapyrrole assembly and modification into the ligands of biologically functional cofactors. Trends Biochem Sci 15(12):486–491. doi:10.1016/0968-0004(90)90304-T

    PubMed  Google Scholar 

  72. Louie GV, Brownlie PD, Lambert R, Cooper JB, Blundell TL, Wood SP, Warren MJ, Woodcock SC, Jordan PM (1992) Structure of porphobilinogen deaminase reveals a flexible multidomain polymerase with a single catalytic site. Nature 359(6390):33–39. doi:10.1038/359033a0

    CAS  PubMed  Google Scholar 

  73. Shoolingin-Jordan PM (1995) Porphobilinogen deaminase and uroporphyrinogen III synthase: structure, molecular biology, and mechanism. J Bioenerg Biomembr 27(2):181–195. doi:10.1007/BF02110033

    CAS  PubMed  Google Scholar 

  74. Burton G, Fagerness PE, Hosozawa S, Jordan PM, Scott AI (1979) 13C NMR evidence for a new intermediate, pre-uroporphyrinogen, in the enzymic transformation of porphobilinogen into uroporphyrinogens I and III. J Chem Soc Chem Comm 5:202. doi:10.1039/c39790000202

    Google Scholar 

  75. Timkovich R, Burkhalter RS, Xavier AV, Chen L, Legall J (1994) Iron uroporphyrin-I and a heme c-derivative are prosthetic groups in D. gigas rubredoxin oxidase. Bioorg Chem 22(3):284–293. doi:10.1006/bioo1994.1022

    CAS  Google Scholar 

  76. Schubert HL, Raux E, Matthews MAA, Phillips JD, Wilson KS, Hill CP, Warren MJ (2002) Structural diversity in metal ion chelation and the structure of uroporphyrinogen III synthase. In: Colloquium on tetrapyrroles: their life, birth and death, Heriot-Watt, Edinburgh, pp 595–600

  77. Luo J, Lim CK (1993) Order of uroporphyrinogen III decarboxylation on incubation of porphobilinogen and uroporphyrinogen III with erythrocyte uroporphyrinogen decarboxylase. Biochem J 289(Pt 2):529–532

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Dailey HA (2002) Terminal steps of haem biosynthesis. Biochem Soc Trans 4:590–595

    Google Scholar 

  79. Whitby FG (1998) Crystal structure of human uroporphyrinogen decarboxylase. EMBO J 17(9):2463–2471. doi:10.1093/emboj/17.9.2463

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Phillips JD, Warby CA, Whitby FG, Kushner JP, Hill CP (2009) Substrate shuttling between active sites of uroporphyrinogen decarboxylase is not required to generate coproporphyrinogen. J Mol Biol 389(2):306–314. doi:10.1016/j.jmb.2009.04.013

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Medlock AE, Dailey HA (1996) Human coproporphyrinogen oxidase is not a metalloprotein. J Biol Chem 271(51):32507–32510

    CAS  PubMed  Google Scholar 

  82. Cavaleiro JA, Kenner GW, Smith KM (1974) Pyrroles and related compounds. XXXII. Biosynthesis of protoporphyrin-IX from coproporphyrinogen-III. J Chem Soc Perkin 110:1188–1194. doi:10.1039/P19740001188

    Google Scholar 

  83. Elder GH, Evans JO, Jackson JR, Jackson AH (1978) Factors determining sequence of oxidative decarboxylation of 2-propionate and 4-propionate substituents of coproporphyrinogen-Iii by coproporphyrinogen oxidase in rat-liver. Biochem J 169(1):215–223

    CAS  PubMed Central  PubMed  Google Scholar 

  84. Jackson AH, Jones DM, Philip G, Lash TD, Batlle AM, Smith SG (1980) Synthetic and biosynthetic studies of porphyrins, Part IV. Further studies of the conversion of corporporhyrinogen-III to protoporphyrin-IX: mass spectrometric investigations of the incubation of specifically deuteriated corporporhyringen-III with chicken red cell haemolysates. Int J Biochem 12(5–6):681–688. doi:10.1016/0020-711X(80)90144-5

    CAS  PubMed  Google Scholar 

  85. Phillips JD, Whitby FG, Warby CA, Labbe P, Yang C, Pflugrath JW, Ferrara JD, Robinson H, Kushner JP, Hill CP (2004) Crystal structure of the oxygen-dependant coproporphyrinogen oxidase (Hem13p) of S. cerevisiae. J Biol Chem 279(37):38960–38968. doi:10.1074/jbc.M406050200

    CAS  PubMed  Google Scholar 

  86. Lee DS, Flachsova E, Bodnarova M, Demeler B, Martasek P, Raman CS (2005) Structural basis of hereditary coproporphyria. Natl Acad Sci USA 102(40):14232–14237. doi:10.1073/pnas.0506557102

    CAS  Google Scholar 

  87. Stephenson JR, Stacey JA, Morgenthaler JB, Friesen JA, Lash TD, Jones MA (2007) Role of aspartate 400, arginine 262, and arginine 401 in the catalytic mechanism of human coproporphyrinogen oxidase. Protein Sci 16(3):401–410. doi:10.1110/ps.062636907

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Silva PJ, Ramos MJ (2008) A comparative density-functional study of the reaction mechanism of the O2-dependent coproporphyrinogen III oxidase. Bioorg Med Chem Lett 16(6):2726–2733. doi:10.1016/j.bmc.2008.01.008

    CAS  Google Scholar 

  89. Lash TD (2005) The enigma of coproporphyrinogen oxidase: how does this unusual enzyme carry out oxidative decarboxylations to afford vinyl groups? Bioorg Med Chem Lett 15(20):4506–4509. doi:10.1016/j.bmcl.2005.07.010

    CAS  PubMed  Google Scholar 

  90. Layer G, Grage K, Teschner T, Schunemann V, Breckau D, Masoumi A, Jahn M, Heathcote P, Trautwein AX, Jahn D (2005) Radical S-adenosylmethionine enzyme coproporphyrinogen III oxidase HemN: functional features of the [4Fe–4S] cluster and the two bound S-adenosyl-l-methionines. J Biol Chem 280(32):29038–29046. doi:10.1074/jbc.M501275200

    CAS  PubMed  Google Scholar 

  91. Atta M, Mulliez E, Arragain S, Forouhar F, Hunt JF, Fontecave M (2010) S-Adenosylmethionine-dependent radical-based modification of biological macromolecules. Curr Opin Struc Biol 20(6):684–692. doi:10.1016/j.sbi.2010.09.009

    CAS  Google Scholar 

  92. Booker SJ (2009) Anaerobic functionalization of unactivated C–H bonds. Curr Opin Chem Biol 13(1):58–73. doi:10.1016/j.cbpa.2009.02.036

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Layer G, Heinz DW, Jahn D, Schubert WD (2004) Structure and function of radical SAM enzymes. Curr Opin Chem Biol 8(5):468–476. doi:10.1016/j.cbpa.2004.08.001

    CAS  PubMed  Google Scholar 

  94. Layer G, Pierik AJ, Trost M, Rigby SE, Leech HK, Grage K, Breckau D, Astner I, Jansch L, Heathcote P, Warren MJ, Heinz DW, Jahn D (2006) The substrate radical of E. coli oxygen-independent coproporphyrinogen III oxidase HemN. J Biol Chem 281(23):15727–15734. doi:10.1074/jbc.M512628200

    CAS  PubMed  Google Scholar 

  95. Abicht HK, Martinez J, Layer G, Jahn D, Solioz M (2012) Lactococcus lactis HemW (HemN) is a haem-binding protein with a putative role in haem trafficking. Biochem J 442(2):335–343. doi:10.1042/BJ20111618

    CAS  PubMed  Google Scholar 

  96. Dailey HA, Dailey TA (1996) Protoporphyrinogen oxidase of Myxococcus xanthus. Expression, purification, and characterization of the cloned enzyme. J Biol Chem 271(15):8714–8718

    CAS  PubMed  Google Scholar 

  97. Sasarman A, Letowski J, Czaika G, Ramirez V, Nead MA, Jacobs JM, Morais R (1993) Nucleotide-sequence of the hemG gene involved in the protoporphyrinogen oxidase activity of E. coli K12. Can J Microbiol 39(12):1155–1161

    CAS  PubMed  Google Scholar 

  98. Boynton TO, Gerdes S, Craven SH, Neidle EL, Phillips JD, Dailey HA (2011) Discovery of a gene involved in a third bacterial protoporphyrinogen oxidase activity through comparative genomic analysis and functional complementation. Appl Environ Microbiol 77(14):4795–4801. doi:10.1128/AEM.00171-11

    CAS  PubMed Central  PubMed  Google Scholar 

  99. Dailey TA, Dailey HA (1997) Expression, purification, and characteristics of mammalian protoporphyrinogen oxidase. In: McCormick D, Suttie J, Wagner C (eds.) Methods in Enzymology, vol 281. pp 340–349

  100. Hansson M, Hederstedt L (1994) Bacillus subtilis HemY is a peripheral membrane-protein essential for protoheme-IX synthesis which can oxidize coproporphyrinogen-III and protoporphyrinogen-IX. J Bacteriol 176(19):5962–5970

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Dailey TA, Meissner P, Dailey HA (1994) Expression of a cloned protoporphyrinogen oxidase. J Biol Chem 269(2):813–815

    CAS  PubMed  Google Scholar 

  102. Koch M, Breithaupt C, Kiefersauer R, Freigang J, Huber R, Messerschmidt A (2004) Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J 23(8):1720–1728. doi:10.1038/sj.emboj.7600189

    CAS  PubMed Central  PubMed  Google Scholar 

  103. Corradi HR, Corrigall AV, Boix E, Mohan CG, Sturrock ED, Meissner PN, Acharya KR (2006) Crystal structure of protoporphyrinogen oxidase from Myxococcus xanthus and its complex with the inhibitor acifluorfen. J Biol Chem 281(50):38625–38633. doi:10.1074/jbc.M606640200

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Heinemann IU, Diekmann N, Masoumi A, Koch M, Messerschmidt A, Jahn M, Jahn D (2007) Functional definition of the tobacco protoporphyrinogen IX oxidase substrate-binding site. Biochem J 402(3):575–580. doi:10.1042/BJ20061321

    CAS  PubMed Central  PubMed  Google Scholar 

  105. Boynton TO, Daugherty LE, Dailey TA, Dailey HA (2009) Identification of E. coli HemG as a novel, menadione-dependent flavodoxin with protoporphyrinogen oxidase activity. Biochemistry 48(29):6705–6711. doi:10.1021/Bi900850y

    CAS  PubMed Central  PubMed  Google Scholar 

  106. Mobius K, Arias-Cartin R, Breckau D, Hannig AL, Riedmann K, Biedendieck R, Schroder S, Becher D, Magalon A, Moser J, Jahn M, Jahn D (2010) Heme biosynthesis is coupled to electron transport chains for energy generation. Proc Natl Acad Sci USA 107(23):10436–10441. doi:10.1073/pnas.1000956107

    PubMed Central  PubMed  Google Scholar 

  107. Kato K, Tanaka R, Sano S, Tanaka A, Hosaka H (2010) Identification of a gene essential for protoporphyrinogen IX oxidase activity in the cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci USA 107(38):16649–16654. doi:10.1073/pnas.1000771107

    CAS  PubMed Central  PubMed  Google Scholar 

  108. Dailey HA, Dailey TA, Wu CK, Medlock AE, Wang KF, Rose JP, Wang BC (2000) Ferrochelatase at the millennium: structures, mechanisms and [2Fe–2S] clusters. Cell Mol Life Sci 57(13–14):1909–1926. doi:10.1007/PL00000672

    CAS  PubMed  Google Scholar 

  109. Corrigall AV, Siziba KB, Maneli MH, Shephard EG, Ziman M, Dailey TA, Dailey HA, Kirsch RE, Meissner PN (1998) Purification of and kinetic studies on a cloned protoporphyrinogen oxidase from the aerobic bacterium B. subtilis. Arch Biochem Biophys 358(2):251–256. doi:10.1006/abbi1998.0834

    CAS  PubMed  Google Scholar 

  110. Hansson M, Hederstedt L (1994) Purification and characterisation of a water-soluble ferrochelatase from B. subtilis. Eur J Biochem 220(1):201–208. doi:10.1111/j.1432-1033.1994.tb18615.x

    CAS  PubMed  Google Scholar 

  111. Romao CV, Ladakis D, Lobo SA, Carrondo MA, Brindley AA, Deery E, Matias PM, Pickersgill RW, Saraiva LM, Warren MJ (2011) Evolution in a family of chelatases facilitated by the introduction of active site asymmetry and protein oligomerization. Proc Natl Acad Sci USA 108(1):97–102. doi:10.1073/pnas.1014298108

    PubMed Central  PubMed  Google Scholar 

  112. Dailey TA, Boynton TO, Albetel AN, Gerdes S, Johnson MK, Dailey HA (2010) Discovery and characterization of HemQ: an essential heme biosynthetic pathway component. J Biol Chem 285(34):25978–25986. doi:10.1074/jbc.M110.142604

    CAS  PubMed Central  PubMed  Google Scholar 

  113. Raux E, Leech HK, Beck R, Schubert HL, Santander PJ, Roessner CA, Scott AI, Martens JH, Jahn D, Thermes C, Rambach A, Warren MJ (2003) Identification and functional analysis of enzymes required for precorrin-2 dehydrogenation and metal ion insertion in the biosynthesis of sirohaem and cobalamin in Bacillus megaterium. Biochem J 370(2):505–516. doi:10.1042/BJ20021443

    CAS  PubMed Central  PubMed  Google Scholar 

  114. Raux E, McVeigh T, Peters SE, Leustek T, Warren MJ (1999) The role of S. cerevisiae Met1p and Met8p in sirohaem and cobalamin biosynthesis. Biochem J 338:701–708. doi:10.1042/0264-6021:3380701

    CAS  PubMed Central  PubMed  Google Scholar 

  115. Warren MJ, Bolt EL, Roessner CA, Scott AI, Spencer JB, Woodcock SC (1994) Gene dissection demonstrates that the E. coli cysG gene encodes a multifunctional protein. Biochem J 302(Pt 3):837–844

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Warren MJ, Raux E, Schubert HL, Escalante-Semerena JC (2002) The biosynthesis of adenosylcobalamin (vitamin B12). Nat Prod Rep 19(4):390–412. doi:10.1069/b108967f

    CAS  PubMed  Google Scholar 

  117. Platt MD, Schurr MJ, Sauer K, Vazquez G, Kukavica-Ibrulj I, Potvin E, Levesque RC, Fedynak A, Brinkman FS, Schurr J, Hwang SH, Lau GW, Limbach PA, Rowe JJ, Lieberman MA, Barraud N, Webb J, Kjelleberg S, Hunt DF, Hassett DJ (2008) Proteomic, microarray, and signature-tagged mutagenesis analyses of anaerobic P. aeruginosa at pH 6.5, likely representing chronic, late-stage cystic fibrosis airway conditions. J Bacteriol 190(8):2739–2758. doi:10.1128/JB.01683-07

    CAS  PubMed Central  PubMed  Google Scholar 

  118. Storbeck S, Rolfes S, Raux-Deery E, Warren MJ, Jahn D, Layer G (2010) A novel pathway for the biosynthesis of heme in  : genome-based bioinformatic predictions and experimental evidence. Archaea 2010:175050. doi:10.1155/2010/175050

    PubMed Central  PubMed  Google Scholar 

  119. Brindley AA, Raux E, Leech HK, Schubert HL, Warren MJ (2003) A story of chelatase evolution: identification and characterization of a small 13–15-kDa “ancestral” cobaltochelatase (CbiXS) in the archaea. J Biol Chem 278(25):22388–22395. doi:10.1074/jbc.M302468200

    CAS  PubMed  Google Scholar 

  120. Lobo SA, Brindley A, Warren MJ, Saraiva LM (2009) Functional characterization of the early steps of tetrapyrrole biosynthesis and modification in D. vulgaris Hildenborough. Biochem J 420(2):317–325. doi:10.1042/BJ20090151

    CAS  PubMed  Google Scholar 

  121. Lobo SAL, Brindley AA, Romao CV, Leech HK, Warren MJ, Saraiva LM (2008) Two distinct roles for two functional cobaltochelatases (CbiK) in D. vulgaris Hildenborough. Biochemistry 47(21):5851–5857. doi:10.1021/Bi800342c

    CAS  PubMed  Google Scholar 

  122. Lobo SAL, Warren MJ, Saraiva LM (2012) Chapter seven––sulfate-reducing bacteria reveal a new branch of tetrapyrrole metabolism. In: Robert KP (ed) Advance microbiol physiology, vol 61. Amsterdam, Netherlands, pp 267–295. doi:10.1016/B978-0-12-394423-8.00007-X

    Google Scholar 

  123. Tripathy BC, Sherameti I, Oelmuller R (2010) Siroheme: an essential component for life on earth. Plant Sign Behav 5(1):14–20

    CAS  Google Scholar 

  124. Yapbondoc F, Bondoc LL, Timkovich R, Baker DC, Hebbler A (1990) C-methylation occurs during the biosynthesis of heme d 1. J Biol Chem 265(23):13498–13500

    CAS  Google Scholar 

  125. Bali S, Warren MJ, Ferguson SJ (2010) NirF is a periplasmic protein that binds d 1 heme as part of its essential role in d 1 heme biogenesis. FEBS J 277(23):4944–4955. doi:10.1111/j.1742-4658.2010.07899.x

    CAS  PubMed  Google Scholar 

  126. Suzuki M, Hirai T, Arai H, Ishii M, Igarashi Y (2006) Purification, characterization, and gene cloning of thermophilic cytochrome cd 1 nitrite reductase from Hydrogenobacter thermophilus TK-6. J Biosci Bioeng 101(5):391–397. doi:10.1263/jbb.101.391

    CAS  PubMed  Google Scholar 

  127. Palmedo G, Seither P, Korner H, Matthews JC, Burkhalter RS, Timkovich R, Zumft WG (1995) Resolution of the nirD locus for heme d 1 synthesis of cytochrome cd 1 (respiratory nitrite reductase) from Pseudomonas stutzeri. Eur J Biochem 232(3):737–746. doi:10.1111/j.1432-1033.1995.tb20868.x

    CAS  PubMed  Google Scholar 

  128. Glockner AB, Zumft WG (1996) Sequence analysis of an internal 9.72-kb segment from the 30-kb denitrification gene cluster of Pseudomonas stutzeri. Biochimica Et Biophysica Acta-Bioenergetics 1277((1-2)):6–12. doi:10.1016/s0005-2728(96)00108-9

    CAS  Google Scholar 

  129. Kawasaki S, Arai H, Kodama T, Igarashi Y (1997) Gene cluster for dissimilatory nitrite reductase (nir) from P. aeruginosa: sequencing and identification of a locus for heme d 1 biosynthesis. J Bacteriol 179(1):235–242

    CAS  PubMed Central  PubMed  Google Scholar 

  130. Silvestrini MC, Cutruzzola F, D’Alessandro R, Brunori M, Fochesato N, Zennaro E (1992) Expression of P. aeruginosa nitrite reductase in P. putida and characterization of the recombinant protein. Biochem J 285(Pt 2):661–666

    CAS  PubMed Central  PubMed  Google Scholar 

  131. Deboer APN, Reijnders WNM, Kuenen JG, Stouthamer AH, Vanspanning RJM (1994) Isolation, sequencing and mutational analysis of a gene-cluster involved in nitrite reduction in Paracoccus denitrificans. Anton Leeuw Int J G 66(1–3):111–127

    CAS  Google Scholar 

  132. Ohshima T, Sugiyama M, Uozumi N, Iijima S, Kobayashi T (1993) Cloning and sequencing of a gene encoding nitrite reductase from Paracoccus denitrificans and expression of the gene in E. coli. J Ferment Bioeng 76(2):82–88. doi:10.1016/0922-338x(93)90061-c

    CAS  Google Scholar 

  133. Warren MJ, Smith AG, Deery E, Rose RS (2009) Biosynthesis of Siroheme and Coenzyme F430. In: Tetrapyrroles: birth, life and death. Molecular biology intelligence unit. Springer, Berlin Heidelberg New York, pp 344–351, doi: 10.1007/978-0-387-78518-9_22

  134. Storbeck S, Walther J, Mueller J, Parmar V, Schiebel HM, Kemken D, Duelcks T, Warren MJ, Layer G (2009) The P. aeruginosa nirE gene encodes the S-adenosyl-l-methionine-dependent uroporphyrinogen III methyltransferase required for heme d 1 biosynthesis. FEBS J 276(20):5973–5982. doi:10.1111/j.1742-4658.2009.07306.x

    CAS  PubMed  Google Scholar 

  135. Stroupe ME, Leech HK, Daniels DS, Warren MJ, Getzoff ED (2003) CysG structure reveals tetrapyrrole-binding features and novel regulation of siroheme biosynthesis. Nat Struct Biol 10(12):1064–1073. doi:10.1038/nsb1007

    CAS  PubMed  Google Scholar 

  136. Hasegawa N, Arai H, Igarashi Y (2001) Two c-type cytochromes, NirM and NirC, encoded in the nir gene cluster of P. aeruginosa act as electron donors for nitrite reductase. Biochem Biophys Res Commun 288(5):1223–1230. doi:10.1006/bbrc2001.5919

    CAS  PubMed  Google Scholar 

  137. Nicke T, Schnitzer T, Munch K, Adamczack J, Haufschildt K, Buchmeier S, Kucklick M, Felgentrager U, Jansch L, Riedel K, Layer G (2013) Maturation of the cytochrome cd 1 nitrite reductase NirS from P. aeruginosa requires transient interactions between the three proteins NirS. Biosci Rep NirN NirF. doi:10.1042/BSR20130043

    Google Scholar 

  138. Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of a nucleotide-binding protein. Nature 250(5463):194–199. doi:10.1038/250194a0

    CAS  PubMed  Google Scholar 

  139. Bali S, Ferguson SJ (2011) Assembly of respiratory proteins of the nitrogen cycle In: Moir JWB (ed) Nitrogen cycling in bacteria: molecular analysis, pp 163–175

  140. Heikkila MP, Honisch U, Wunsch P, Zumft WG (2001) Role of the tat transport system in nitrous oxide reductase translocation and cytochrome cd 1 biosynthesis in Pseudomonas stutzeri. J Bacteriol 183(5):1663–1671. doi:10.1128/jb.183.5.1663-1671.2001

    CAS  PubMed Central  PubMed  Google Scholar 

  141. Brinkman AB, Ettema TJ, de Vos WM, van der Oost J (2003) The Lrp family of transcriptional regulators. Mol Microbiol 48(2):287–294. doi:10.1046/j.1365-2958.2003.03442.x

    CAS  PubMed  Google Scholar 

  142. Xiong J, Bauer CE, Pancholy A (2007) Insight into the haem d 1 biosynthesis pathway in heliobacteria through bioinformatics analysis. Microbiol Sgm 153:3548–3562. doi:10.1099/mic.0.2007/007930-0

    CAS  Google Scholar 

  143. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE (2001) Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucl Acids Res 29(5):1097–1106. doi:10.1093/nar/29.5.1097

    CAS  PubMed Central  PubMed  Google Scholar 

  144. Frey PA, Hegeman AD, Ruzicka FJ (2008) The radical SAM superfamily. Crit Rev Biochem Mol 43(1):63–88. doi:10.1080/10409230701829169

    CAS  Google Scholar 

  145. Brindley AA, Zajicek R, Warren MJ, Ferguson SJ, Rigby SE (2010) NirJ, a radical SAM family member of the d 1 heme biogenesis cluster. FEBS Lett 584(11):2461–2466. doi:10.1016/j.febslet.2010.04.053

    CAS  PubMed  Google Scholar 

  146. Hanzelmann P, Schindelin H (2004) Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc Natl Acad Sci USA 101(35):12870–12875. doi:10.1073/pnas.0404624101

    PubMed Central  PubMed  Google Scholar 

  147. Hanzelmann P, Hernandez HL, Menzel C, Garcia-Serres R, Huynh BH, Johnson MK, Mendel RR, Schindelin H (2004) Characterization of MOCS1A, an oxygen-sensitive iron–sulfur protein involved in human molybdenum cofactor biosynthesis. J Biol Chem 279(33):34721–34732. doi:10.1074/jbc.M313398200

    PubMed  Google Scholar 

  148. Fluhe L, Knappe TA, Gattner MJ, Schafer A, Burghaus O, Linne U, Marahiel MA (2012) The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat Chem Biol 8(4):350–357. doi:10.1038/nchembio.798

    PubMed  Google Scholar 

  149. Yokoyama K, Numakura M, Kudo F, Ohmori D, Eguchi T (2007) Characterization and mechanistic study of a radical SAM dehydrogenase in the biosynthesis of butirosin. J Am Chem Soc 129(49):15147–15155. doi:10.1021/ja072481t

    CAS  PubMed  Google Scholar 

  150. Benjdia A, Subramanian S, Leprince J, Vaudry H, Johnson MK, Berteau O (2008) Anaerobic sulfatase-maturating enzymes, first dual substrate radical S-adenosylmethionine enzymes. J Biol Chem 283(26):17815–17826. doi:10.1074/jbc.M710074200

    CAS  PubMed Central  PubMed  Google Scholar 

  151. Grove TL, Ahlum JH, Sharma P, Krebs C, Booker SJ (2010) A consensus mechanism for radical SAM-dependent dehydrogenation? BtrN contains two 4Fe–4S clusters. Biochemistry 49(18):3783–3785. doi:10.1021/bi9022126

    CAS  PubMed Central  PubMed  Google Scholar 

  152. Grove TL, Lee K-H, St. Clair J, Krebs C, Booker C (2008) In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three 4Fe-4S clusters. Biochemistry 47(28):7523–7538. doi:10.1021/bi8004297

    CAS  PubMed Central  PubMed  Google Scholar 

  153. Akutsu H, Park JS, Sano S (1993) l-methionine methyl is specifically incorporated into the C-2 and C-7 positions of the porphyrin of cytochrome-c3 in a strictly anaerobic bacterium, D. vulgaris. J Am Chem Soc 115(25):12185–12186. doi:10.1021/Ja00078a075

    CAS  Google Scholar 

  154. Scott AI (1990) Mechanistic and evolutionary aspects of vitamin-B12 biosynthesis. Acc Chem Res 23(9):308–317. doi:10.1021/Ar00177a007

    CAS  Google Scholar 

  155. Panek H, O’Brian MR (2002) A whole genome view of prokaryotic haem biosynthesis. Microbiol Sgm 148:2273–2282

    CAS  Google Scholar 

  156. Buchenau B, Kahnt J, Heinemann IU, Jahn D, Thauer RK (2006) Heme biosynthesis in Methanosarcina barkeri via a pathway involving two methylation reactions. J Biol Chem 188(24):8666–8668. doi:10.1128/Jb.01349-06

    CAS  Google Scholar 

  157. Susanti D, Mukhopadhyay B (2012) An intertwined evolutionary history of methanogenic archaea and sulfate reduction. Plos One. doi:10.1371/journal.pone.0045313

    PubMed Central  PubMed  Google Scholar 

  158. Layer G, Moser J, Heinz DW, Jahn D, Schubert WD (2003) Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J 22(23):6214–6224. doi:10.1093/emboj/cdg598

    CAS  PubMed Central  PubMed  Google Scholar 

  159. Romao CV, Louro R, Timkovich R, Lubben M, Liu MY, LeGall J, Xavier AV, Teixeira M (2000) Iron-coproporphyrin III is a natural cofactor in bacterioferritin from the anaerobic bacterium Desulfovibrio desulfuricans. FEBS Lett 480(2–3):213–216. doi:10.1016/S0014-5793(00)01939-6

    CAS  PubMed  Google Scholar 

  160. Oglesby-Sherrouse AG, Vasil ML (2010) Characterization of a heme-regulated non-coding RNA encoded by the prrF locus of P. aeruginosa. PLoS ONE 5(4):e9930. doi:10.1371/journal.pone.0009930

    PubMed Central  PubMed  Google Scholar 

  161. Benner SA, Ellington AD, Tauer A (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA 86(18):7054–7058. doi:10.1073/pnas.86.18.7054

    CAS  PubMed Central  PubMed  Google Scholar 

  162. Dickman SR (1977) Ribonucleotide reduction and possible role of cobalamin in evolution. J Mol Evol 10(3):251–260. doi:10.1007/bf01764600

    CAS  PubMed  Google Scholar 

  163. Banerjee R, Ragsdale SW (2003) The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes. Annu Rev Biochem 72:209–247. doi:10.1146/annurev.biochem.72.121801.161828

    CAS  PubMed  Google Scholar 

  164. Frey PA, Magnusson OT (2003) S-Adenosylmethionine: a wolf in sheep’s clothing, or a rich man’s adenosylcobalamin? Chem Rev 103(6):2129–2148. doi:10.1021/cr020422m

    CAS  PubMed  Google Scholar 

  165. Nicolet Y, Drennan CL (2004) AdoMet radical proteins: from structure to evolution––alignment of divergent protein sequences reveals strong secondary structure element conservation. Nucl Acids Res 32(13):4015–4025. doi:10.1093/nar/gkh728

    CAS  PubMed Central  PubMed  Google Scholar 

  166. Gough SP, Petersen BO, Duus JO (2000) Anaerobic chlorophyll isocyclic ring formation in Rhodobacter capsulatus requires a cobalamin cofactor. Proc Natl Acad Sci USA 97(12):6908–6913. doi:10.1073/pnas.97.12.6908

    CAS  PubMed Central  PubMed  Google Scholar 

  167. Holliday GL, Thornton JM, Marquet A, Smith AG, Rebeille F, Mendel R, Schubert HL, Lawrence AD, Warren MJ (2007) Evolution of enzymes and pathways for the biosynthesis of cofactors. Nat Prod Rep 24(5):972–987. doi:10.1039/b703107f

    CAS  PubMed  Google Scholar 

  168. Ferguson SJ (2011) Remarkable diversity in biosynthesis of c-type cytochromes in eukaryotes and prokaryotes. FEBS J 278(22):4169. doi:10.1111/j.1742-4658.2011.08378.x

    CAS  PubMed  Google Scholar 

  169. Ducluzeau AL, van Lis R, Duval S, Schoepp-Cothenet B, Russell MJ, Nitschke W (2009) Was nitric oxide the first deep electron sink? Trends Biochem Sci 34(1):9–15. doi:10.1016/j.tibs.2008.10.005

    CAS  PubMed  Google Scholar 

  170. Crane BR, Getzoff ED (1996) The relationship between structure and function for the sulfite reductases. Curr Opin Struc Biol 6(6):744–756. doi:10.1016/s0959-440x(96)80003-0

    CAS  Google Scholar 

  171. Lubben M, Morand K (1994) Novel prenylated hemes as cofactors of cytochrome oxidases: archaea have modified heme a and heme o. J Biol Chem 269(34):21473–21479

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by BBSRC grants BBE0229441 and BB/E024203 to S.J.F and M.J.W.

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Correspondence to Martin J. Warren.

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S. Bali, D. J. Palmer, and S. Schroeder contributed equally to this work.

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Bali, S., Palmer, D.J., Schroeder, S. et al. Recent advances in the biosynthesis of modified tetrapyrroles: the discovery of an alternative pathway for the formation of heme and heme d 1 . Cell. Mol. Life Sci. 71, 2837–2863 (2014). https://doi.org/10.1007/s00018-014-1563-x

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