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Current Understanding of the Biosynthesis of the Unique Nitrogenase Cofactor Core

  • Caleb J. Hiller
  • Lee A. Rettberg
  • Chi Chung Lee
  • Martin T. Stiebritz
  • Yilin HuEmail author
Chapter
Part of the Structure and Bonding book series (STRUCTURE, volume 179)

Abstract

Nitrogenase catalyzes the remarkable chemical transformations of N2 to NH3, and C1 substrates to hydrocarbons, under ambient conditions. The best-studied Mo-nitrogenase utilizes a complex metallocofactor ([MoFe7S9C(R-homocitrate)]) for substrate binding and reduction; however, the complexity of this cofactor has hindered a better understanding of its mechanistic details and chemical synthesis so far. Driven by the pressing questions related to the structure and function of the nitrogenase cofactor, research in the past decades has been focused on unraveling the biosynthetic mechanism of this metallocluster in order to cultivate knowledge of how the cofactor is functionalized in this process. In this review, we summarize the recent advances toward a better understanding of the biosynthesis of the nitrogenase cofactor, with a particular focus on the biosynthetic events related to the generation of its unique core structure. Information derived from these studies has unveiled a novel, radical SAM-dependent mechanism of carbide insertion that orchestrates the coupling and rearrangement of two 4Fe cluster modules into a unique 8Fe cofactor core, as well as a sulfite-based route that incorporates a ‘9th sulfur’ at the catalytically important “belt” region of the cofactor. Continued efforts along this line of investigation will further unravel the biosynthetic mechanism of the nitrogenase cofactor while facilitating investigations into the elusive catalytic mechanism of nitrogenase.

Keywords

‘9th sulfur’ Interstitial carbide M-cluster (cofactor) Nitrogenase Radical SAM 

Notes

Acknowledgements

This work was supported by NIH-NIGMS grant GM67626 (to Markus W. Ribbe and Yilin Hu).

References

  1. 1.
    Burgess BK, Lowe DJ (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96:2983–3011PubMedGoogle Scholar
  2. 2.
    Howard JB, Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96:2965–2982PubMedGoogle Scholar
  3. 3.
    Hoffman BM, Lukoyanov D, Yang ZY et al (2014) Mechanism of nitrogen fixation by nitrogenase: the next stage. Chem Rev 114:4041–4062PubMedPubMedCentralGoogle Scholar
  4. 4.
    Lee CC, Hu Y, Ribbe MW (2010) Vanadium nitrogenase reduces CO. Science 329:642PubMedPubMedCentralGoogle Scholar
  5. 5.
    Hu Y, Lee CC, Ribbe MW (2011) Extending the carbon chain: hydrocarbon formation catalyzed by vanadium/molybdenum nitrogenases. Science 333:753–755PubMedPubMedCentralGoogle Scholar
  6. 6.
    Lee CC, Hu Y, Ribbe MW (2011) Tracing the hydrogen source of hydrocarbons formed by vanadium nitrogenase. Angew Chem Int Ed Engl 50:5545–5547PubMedGoogle Scholar
  7. 7.
    Rebelein JG, Hu Y, Ribbe MW (2014) Differential reduction of CO2 by molybdenum and vanadium nitrogenases. Angew Chem Int Ed Engl 53:11543–11546PubMedPubMedCentralGoogle Scholar
  8. 8.
    Lee CC, Hu Y, Ribbe MW (2015) Catalytic reduction of CN, CO, and CO2 by nitrogenase cofactors in lanthanide-driven reactions. Angew Chem Int Ed Engl 54:1219–1222PubMedGoogle Scholar
  9. 9.
    Rebelein JG, Hu Y, Ribbe MW (2015) Widening the product profile of carbon dioxide reduction by vanadium nitrogenase. Chembiochem 16:1993–1996PubMedPubMedCentralGoogle Scholar
  10. 10.
    Yang ZY, Dean DR, Seefeldt LC (2011) Molybdenum nitrogenase catalyzes the reduction and coupling of CO to form hydrocarbons. J Biol Chem 286:19417–19421PubMedPubMedCentralGoogle Scholar
  11. 11.
    Yang ZY, Moure VR, Dean DR et al (2012) Carbon dioxide reduction to methane and coupling with acetylene to form propylene catalyzed by remodeled nitrogenase. Proc Natl Acad Sci U S A 109:19644–19648PubMedPubMedCentralGoogle Scholar
  12. 12.
    Schlögl R (2003) Catalytic synthesis of ammonia-a “never-ending story”. Angew Chem Int Ed Engl 42:2004–2008PubMedGoogle Scholar
  13. 13.
    Rofer-DePoorter CK (1981) A comprehensive mechanism for the Fischer-Tropsch synthesis. Chem Rev 81:447–474Google Scholar
  14. 14.
    Einsle O, Tezcan FA, Andrade SL et al (2002) Nitrogenase MoFe-protein at 1.16 Å resolution: a central ligand in the FeMo-cofactor. Science 297:1696–1700PubMedGoogle Scholar
  15. 15.
    Spatzal T, Aksoyoglu M, Zhang L et al (2011) Evidence for interstitial carbon in nitrogenase FeMo cofactor. Science 334:940PubMedPubMedCentralGoogle Scholar
  16. 16.
    Kim J, Rees DC (1992) Crystallographic structure and functional implications of the nitrogenase molybdenum-iron protein from Azotobacter vinelandii. Nature 360:553–560PubMedGoogle Scholar
  17. 17.
    Lancaster KM, Roemelt M, Ettenhuber P et al (2011) X-ray emission spectroscopy evidences a central carbon in the nitrogenase iron-molybdenum cofactor. Science 334:974–977PubMedPubMedCentralGoogle Scholar
  18. 18.
    Tezcan FA, Kaiser JT, Mustafi D et al (2005) Nitrogenase complexes: multiple docking sites for a nucleotide switch protein. Science 309:1377–1380PubMedGoogle Scholar
  19. 19.
    Schindelin H, Kisker C, Schlessman JL et al (1997) Structure of ADP x AIF4 -stabilized nitrogenase complex and its implications for signal transduction. Nature 387:370–376PubMedGoogle Scholar
  20. 20.
    Fay AW, Lee CC, Wiig JA et al (2011) Protocols for cofactor isolation of nitrogenase. Methods Mol Biol 766:239–248PubMedGoogle Scholar
  21. 21.
    Burgess BK (1990) The iron-molybdenum cofactor of nitrogenase. Chem Rev 90:1377–1406Google Scholar
  22. 22.
    Shah VK, Brill WJ (1977) Isolation of an iron-molybdenum cofactor from nitrogenase. Proc Natl Acad Sci U S A 74:3249–3253PubMedPubMedCentralGoogle Scholar
  23. 23.
    Lee HI, Hales BJ, Hoffman BM (1997) Metal-ion valencies of the FeMo cofactor in CO-inhibited and resting state nitrogenase by 57Fe Q-band ENDOR. J Am Chem Soc 119:11395–11400Google Scholar
  24. 24.
    Yoo SJ, Angove HC, Papaefthymiou V et al (2000) Mössbauer study of the MoFe protein of nitrogenase from Azotobacter vinelandii using selective 57Fe enrichment of the M-centers. J Am Chem Soc 122:4926–4936Google Scholar
  25. 25.
    Wiig JA, Lee CC, Hu Y et al (2013) Tracing the interstitial carbide of the nitrogenase cofactor during substrate turnover. J Am Chem Soc 135:4982–4983PubMedPubMedCentralGoogle Scholar
  26. 26.
    Lee HI, Benton PM, Laryukhin M et al (2003) The interstitial atom of the nitrogenase FeMo-cofactor: ENDOR and ESEEM show it is not an exchangeable nitrogen. J Am Chem Soc 125:5604–5605PubMedGoogle Scholar
  27. 27.
    Spatzal T, Perez KA, Einsle O et al (2014) Ligand binding to the FeMo-cofactor: structures of CO-bound and reactivated nitrogenase. Science 345:1620–1623PubMedPubMedCentralGoogle Scholar
  28. 28.
    Spatzal T, Perez KA, Howard JB et al (2015) Catalysis-dependent selenium incorporation and migration in the nitrogenase active site iron-molybdenum cofactor. elife 4:e11620PubMedPubMedCentralGoogle Scholar
  29. 29.
    Moret ME, Peters JC (2011) N2 functionalization at iron metallaboratranes. J Am Chem Soc 133:18118–18121PubMedPubMedCentralGoogle Scholar
  30. 30.
    Lee CC, Hu Y, Ribbe MW (2012) ATP-independent formation of hydrocarbons catalyzed by isolated nitrogenase cofactors. Angew Chem Int Ed Engl 51:1947–1949PubMedPubMedCentralGoogle Scholar
  31. 31.
    Lee CC, Hu Y, Ribbe MW (2015) Insights into hydrocarbon formation by nitrogenase cofactor homologs. MBio 6:e00307–e00315PubMedPubMedCentralGoogle Scholar
  32. 32.
    Tanifuji K, Sickerman N, Lee CC et al (2016) Structure and reactivity of an asymmetric synthetic mimic of nitrogenase cofactor. Angew Chem Int Ed Engl 55:15633–15636PubMedGoogle Scholar
  33. 33.
    Dos Santos PC, Dean DR, Hu Y et al (2004) Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem Rev 104:1159–1173PubMedGoogle Scholar
  34. 34.
    Kennedy C, Dean D (1992) The nifU, nifS and nifV gene products are required for activity of all three nitrogenases of Azotobacter vinelandii. Mol Gen Genet 231:494–498 PubMedGoogle Scholar
  35. 35.
    Zheng L, White RH, Cash VL et al (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33:4714–4720PubMedGoogle Scholar
  36. 36.
    Zheng L, White RH, Cash VL et al (1993) Cysteine desulfurase activity indicates a role for NifS in metallocluster biosynthesis. Proc Natl Acad Sci U S A 90:2754–2758 PubMedPubMedCentralGoogle Scholar
  37. 37.
    Dos Santos PC, Johnson DC, Ragle BE et al (2007) Controlled expression of nif and isc iron-sulfur protein maturation components reveals target specificity and limited functional replacement between the two systems. J Bacteriol 189:2854–2862 PubMedPubMedCentralGoogle Scholar
  38. 38.
    Smith AD, Jameson GNL, Dos Santos PC et al (2005) NifS-mediated assembly of [4Fe-4S] clusters in the N- and C-terminal domains of the NifU scaffold protein. Biochemistry 44:12955–12969 PubMedGoogle Scholar
  39. 39.
    Yuvaniyama P, Agar JN, Cash VL et al (2000) NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc Natl Acad Sci U S A 97:599–604 PubMedPubMedCentralGoogle Scholar
  40. 40.
    Zheng LM, Dean DR (1994) Catalytic formation of a nitrogenase iron-sulfur cluster. J Biol Chem 269:18723–18726 PubMedGoogle Scholar
  41. 41.
    Christiansen J, Goodwin PJ, Lanzilotta WN et al (1998) Catalytic and biophysical properties of a nitrogenase apo-MoFe protein produced by a nifB-deletion mutant of Azotobacter vinelandii. Biochemistry 37:12611–12623 PubMedGoogle Scholar
  42. 42.
    Paustian TD, Shah VK, Roberts GP (1990) Apodinitrogenase: purification, association with a 20-kilodalton protein, and activation by the iron-molybdenum cofactor in the absence of dinitrogenase reductase. Biochemistry 29:3515–3522 PubMedGoogle Scholar
  43. 43.
    Hawkes TR, Smith BE (1983) Purification and characterization of the inactive MoFe protein (NifB-Kp1) of the nitrogenase from nifB mutants of Klebsiella pneumoniae. Biochem J 209:43–50 PubMedPubMedCentralGoogle Scholar
  44. 44.
    Hawkes TR, Smith BE (1984) The inactive MoFe protein (NifB-Kp1) of the nitrogenase from nifB mutants of Klebsiella pneumoniae. Its interaction with FeMo-cofactor and the properties of the active MoFe protein formed. Biochem J 223:783–792 PubMedPubMedCentralGoogle Scholar
  45. 45.
    Shah VK, Allen JR, Spangler NJ et al (1994) In vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Purification and characterization of NifB cofactor, the product of NifB protein. J Biol Chem 269:1154–1158PubMedGoogle Scholar
  46. 46.
    Allen RM, Chatterjee R, Ludden PW et al (1995) Incorporation of iron and sulfur from NifB cofactor into the iron-molybdenum cofactor of dinitrogenase. J Biol Chem 270:26890–26896PubMedGoogle Scholar
  47. 47.
    George SJ, Igarashi RY, Xiao Y et al (2008) Extended X-ray absorption fine structure and nuclear resonance vibrational spectroscopy reveal that NifB-co, a FeMo-co precursor, comprises a 6Fe core with an interstitial light atom. J Am Chem Soc 130:5673–5680PubMedPubMedCentralGoogle Scholar
  48. 48.
    Rubio LM, Ludden PW (2008) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu Rev Microbiol 62:93–111PubMedGoogle Scholar
  49. 49.
    Roll JT, Shah VK, Dean DR et al (1995) Characteristics of NifNE in Azotobacter vinelandii strains. Implications for the synthesis of the iron-molybdenum cofactor of dinitrogenase. J Biol Chem 270:4432–4437PubMedGoogle Scholar
  50. 50.
    Robinson AC, Burgess BK, Dean DR (1986) Activity, reconstitution, and accumulation of nitrogenase components in Azotobacter vinelandii mutant strains containing defined deletions within the nitrogenase structural gene cluster. J Bacteriol 166:180–186PubMedPubMedCentralGoogle Scholar
  51. 51.
    Filler WA, Kemp RM, Ng JC et al (1986) The nifH gene product is required for the synthesis or stability of the iron-molybdenum cofactor of nitrogenase from Klebsiella pneumoniae. Eur J Biochem 160:371–377PubMedGoogle Scholar
  52. 52.
    Robinson AC, Dean DR, Burgess BK (1987) Iron-molybdenum cofactor biosynthesis in Azotobacter vinelandii requires the iron protein of nitrogenase. J Biol Chem 262:14327–14332PubMedGoogle Scholar
  53. 53.
    Hoover TR, Imperial J, Ludden PW et al (1988) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Biofactors 1:199–205PubMedGoogle Scholar
  54. 54.
    Robinson AC, Chun TW, Li JG et al (1989) Iron-molybdenum cofactor insertion into the apo-MoFe protein of nitrogenase involves the iron protein-MgATP complex. J Biol Chem 264:10088–10095PubMedGoogle Scholar
  55. 55.
    Tal S, Chun TW, Gavini N et al (1991) The ΔnifB (or ΔnifE) FeMo cofactor-deficient MoFe protein is different from the ΔnifH protein. J Biol Chem 266:10654–10657PubMedGoogle Scholar
  56. 56.
    Gavini N, Burgess BK (1992) FeMo cofactor synthesis by a nifH mutant with altered MgATP reactivity. J Biol Chem 267:21179–21186PubMedGoogle Scholar
  57. 57.
    Allen RM, Homer MJ, Chatterjee R et al (1993) Dinitrogenase reductase- and MgATP-dependent maturation of apodinitrogenase from Azotobacter vinelandii. J Biol Chem 268:23670–23674PubMedGoogle Scholar
  58. 58.
    Rangaraj P, Ludden PW (2002) Accumulation of 99Mo-containing iron-molybdenum cofactor precursors of nitrogenase on NifNE, NifH, and NifX of Azotobacter vinelandii. J Biol Chem 277:40106–40111PubMedGoogle Scholar
  59. 59.
    Zheng LM, White RH, Dean DR (1997) Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase. J Bacteriol 179:5963–5966PubMedPubMedCentralGoogle Scholar
  60. 60.
    Pau RN, Lawson DM (2002) Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. Met Ions Biol Syst 39:31–74PubMedGoogle Scholar
  61. 61.
    Hernandez JA, Curatti L, Aznar CP et al (2008) Metal trafficking for nitrogen fixation: NifQ donates molybdenum to NifEN/NifH for the biosynthesis of the nitrogenase FeMo-cofactor. Proc Natl Acad Sci U S A 105:11679–11684PubMedPubMedCentralGoogle Scholar
  62. 62.
    Imperial J, Ugalde RA, Shah VK et al (1984) Role of the nifQ gene product in the incorporation of molybdenum into nitrogenase in Klebsiella pneumoniae. J Bacteriol 158:187–194PubMedPubMedCentralGoogle Scholar
  63. 63.
    Ugalde RA, Imperial J, Shah VK et al (1985) Biosynthesis of the iron-molybdenum cofactor and the molybdenum cofactor in Klebsiella pneumoniae: effect of sulfur source. J Bacteriol 164:1081–1087PubMedPubMedCentralGoogle Scholar
  64. 64.
    Rangaraj P, Ruttimann-Johnson C, Shah VK et al (2001) Accumulation of 55Fe-labeled precursors of the iron-molybdenum cofactor of nitrogenase on NifH and NifX of Azotobacter vinelandii. J Biol Chem 276:15968–15974PubMedGoogle Scholar
  65. 65.
    Homer MJ, Dean DR, Roberts GP (1995) Characterization of the gamma protein and its involvement in the metallocluster assembly and maturation of dinitrogenase from Azotobacter vinelandii. J Biol Chem 270:24745–24752PubMedGoogle Scholar
  66. 66.
    Hernandez JA, Igarashi RY, Soboh B et al (2007) NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway. Mol Microbiol 63:177–192PubMedGoogle Scholar
  67. 67.
    Rubio LM, Rangaraj P, Homer MJ et al (2002) Cloning and mutational analysis of the gamma gene from Azotobacter vinelandii defines a new family of proteins capable of metallocluster binding and protein stabilization. J Biol Chem 277:14299–14305PubMedGoogle Scholar
  68. 68.
    Dean DR, Jacobson MR (1992) Biochemical genetics of nitrogenase. In: Stacey G, Burris RH, Evan HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 763–834Google Scholar
  69. 69.
    Hu Y, Ribbe MW (2016) Biosynthesis of the metalloclusters of nitrogenases. Annu Rev Biochem 85:455–483PubMedGoogle Scholar
  70. 70.
    Hu Y, Ribbe MW (2016) Maturation of nitrogenase cofactor-the role of a class E radical SAM methyltransferase NifB. Curr Opin Chem Biol 31:188–194PubMedPubMedCentralGoogle Scholar
  71. 71.
    Hu Y, Ribbe MW (2016) Nitrogenases – a tale of carbon atom(s). Angew Chem Int Ed Engl 55:8216–8226PubMedGoogle Scholar
  72. 72.
    Ribbe MW, Hu Y, Hodgson KO et al (2014) Biosynthesis of nitrogenase metalloclusters. Chem Rev 114:4063–4080PubMedGoogle Scholar
  73. 73.
    Hu Y, Ribbe MW (2013) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. J Biol Chem 288:13173–13177PubMedPubMedCentralGoogle Scholar
  74. 74.
    Hu Y, Ribbe MW (2013) Nitrogenase assembly. Biochim Biophys Acta 1827:1112–1122PubMedGoogle Scholar
  75. 75.
    Hu Y, Ribbe MW (2011) Biosynthesis of nitrogenase FeMoco. Coord Chem Rev 255:1218–1224PubMedPubMedCentralGoogle Scholar
  76. 76.
    Hu Y, Ribbe MW (2011) Biosynthesis of the metalloclusters of molybdenum nitrogenase. Microbiol Mol Biol Rev 75:664–677PubMedPubMedCentralGoogle Scholar
  77. 77.
    Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460:839–847PubMedGoogle Scholar
  78. 78.
    Hu Y, Fay AW, Lee CC et al (2008) Assembly of nitrogenase MoFe protein. Biochemistry 47:3973–3981PubMedGoogle Scholar
  79. 79.
    Zheng L, White RH, Cash VL et al (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33:4714–4120PubMedGoogle Scholar
  80. 80.
    Schmid B, Ribbe MW, Einsle O et al (2002) Structure of a cofactor-deficient nitrogenase MoFe protein. Science 296:352–356PubMedGoogle Scholar
  81. 81.
    Wiig JA, Hu Y, Ribbe MW (2011) NifEN-B complex of Azotobacter vinelandii is fully functional in nitrogenase FeMo cofactor assembly. Proc Natl Acad Sci U S A 108:8623–8627PubMedPubMedCentralGoogle Scholar
  82. 82.
    Kaiser JT, Hu Y, Wiig JA et al (2011) Structure of precursor-bound NifEN: a nitrogenase FeMo cofactor maturase/insertase. Science 331:91–94PubMedPubMedCentralGoogle Scholar
  83. 83.
    Fay AW, Blank MA, Lee CC et al (2011) Spectroscopic characterization of the isolated iron-molybdenum cofactor (FeMoco) precursor from the protein NifEN. Angew Chem Int Ed Engl 50:7787–7790PubMedPubMedCentralGoogle Scholar
  84. 84.
    Corbett MC, Hu Y, Fay AW et al (2006) Structural insights into a protein-bound iron-molybdenum cofactor precursor. Proc Natl Acad Sci U S A 103:1238–1243PubMedPubMedCentralGoogle Scholar
  85. 85.
    Lancaster KM, Hu Y, Bergmann U et al (2013) X-ray spectroscopic observation of an interstitial carbide in NifEN-bound FeMoco precursor. J Am Chem Soc 136:610–612Google Scholar
  86. 86.
    Fay AW, Wiig JA, Lee CC et al (2015) Identification and characterization of functional homologs of nitrogenase cofactor biosynthesis protein NifB from methanogens. Proc Natl Acad Sci U S A 112:14829–14833PubMedPubMedCentralGoogle Scholar
  87. 87.
    Rettberg LA, Wilcoxen J, Lee CC et al (2018) Probing the coordination and function of Fe4S4 modules in nitrogenase assembly protein NifB. Nat Commun 9:2824PubMedPubMedCentralGoogle Scholar
  88. 88.
    Wiig JA, Hu Y, Lee CC et al (2012) Radical SAM-dependent carbon insertion into the nitrogenase M-cluster. Science 337:1672–1675PubMedGoogle Scholar
  89. 89.
    Boal AK, Rosenzweig AC (2012) Biochemistry. A radical route for nitrogenase carbide insertion. Science 337:1617–1618PubMedGoogle Scholar
  90. 90.
    Boal AK, Grove TL, McLaughlin MI et al (2011) Structural basis for methyl transfer by a radical SAM enzyme. Science 332:1089–1092PubMedPubMedCentralGoogle Scholar
  91. 91.
    Grove TL, Benner JS, Radle MI et al (2011) A radically different mechanism for S-adenosylmethionine-dependent methyltransferases. Science 332:604–607PubMedGoogle Scholar
  92. 92.
    Wiig JA, Hu Y, Ribbe MW (2015) Refining the pathway of carbide insertion into the nitrogenase M-cluster. Nat Commun 6:8034PubMedPubMedCentralGoogle Scholar
  93. 93.
    Tanifuji K, Lee CC, Sickerman NS et al (2018) Tracing the 'ninth sulfur' of the nitrogenase cofactor via a semi-synthetic approach. Nat Chem 10:568–572PubMedPubMedCentralGoogle Scholar
  94. 94.
    Vincent KA, Tilley GJ, Quammie NC et al (2003) Instantaneous, stoichiometric generation of powerfully reducing states of protein active sites using Eu(II) and polyaminocarboxylate ligands. Chem Commun 20:2590–2591Google Scholar
  95. 95.
    Brychkova G, Grishkevich V, Fluhr R et al (2013) An essential role for tomato sulfite oxidase and enzymes of the sulfite network in maintaining leaf sulfite homeostasis. Plant Physiol 161:148–164PubMedGoogle Scholar
  96. 96.
    Carbonero F, Benefiel AC, Alizadeh-Ghamsari AH et al (2012) Microbial pathways in colonic sulfur metabolism and links with health and disease. Front Physiol 3:448PubMedPubMedCentralGoogle Scholar
  97. 97.
    Kertesz MA (2000) Riding the sulfur cycle – metabolism of sulfonates and sulfate esters in gram-negative bacteria. FEMS Microbiol Rev 24:135–175PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Caleb J. Hiller
    • 1
    • 2
  • Lee A. Rettberg
    • 1
  • Chi Chung Lee
    • 1
  • Martin T. Stiebritz
    • 1
  • Yilin Hu
    • 1
    Email author
  1. 1.Department of Molecular Biology and BiochemistryUniversity of California, IrvineIrvineUSA
  2. 2.Department of ChemistryUniversity of California, IrvineIrvineUSA

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