Advertisement

JBIC Journal of Biological Inorganic Chemistry

, Volume 23, Issue 7, pp 957–967 | Cite as

β-Hydroxyaspartic acid in siderophores: biosynthesis and reactivity

  • Clifford D. Hardy
  • Alison ButlerEmail author
Minireview
Part of the following topical collections:
  1. Alison Butler: Papers in Celebration of Her 2018 ACS Alfred Bader Award in Bioorganic or Bioinorganic Chemistry

Abstract

A growing number of siderophores are found to contain β-hydroxyaspartic acid (β-OH-Asp) as a functional group for Fe(III) coordination, along with the more common catechol and hydroxamic acid groups. This review covers the structures, biosynthesis, and reactions of peptidic β-OH-Asp siderophores. Hydroxylation of Asp in siderophore biosynthesis is predicted to be carried out either through discrete aspartyl β-hydroxylating enzymes or through hydroxylating domains within non-ribosomal peptide synthetases, both of which display sequence homology to known non-heme iron(II), α-ketoglutarate-dependent dioxygenases. Ferric complexes of β-OH-Asp siderophores are photoreactive, resulting in reduction of Fe(III) and oxidative cleavage of the siderophore to yield distinct types of photoproducts. Probing the photoreactivity of synthetic Fe(III)-α-hydroxycarboxylate clusters yields mechanistic insights into the different photoproducts observed for β-OH-Asp and other α-hydroxycarboxylate siderophore Fe(III) complexes.

Keywords

Siderophore β-Hydroxyaspartic acid Iron Biosynthesis Photoreactivity 

Notes

Acknowledgements

We are grateful for support from NSF CHE-1710761.

References

  1. 1.
    Zane H, Butler A (2013) In: Reedijk J, Poppelmeier K (eds) Comprehensive inorganic chemistry II, vol 3. Elsevier, Amsterdam, pp 1–20Google Scholar
  2. 2.
    Sandy M, Butler A (2009) Chem Rev 109:4580–4595CrossRefGoogle Scholar
  3. 3.
    Gibson F, Magrath DI (1969) Biochim Biophys Acta 192:175–184CrossRefGoogle Scholar
  4. 4.
    Amin SA, Green DH, Küpper FC, Carrano CJ (2009) Inorg Chem 48:11451–11458CrossRefGoogle Scholar
  5. 5.
    Teintze M, Hossain MB, Barnes CL, Leong J, Van der Helm D (1981) Biochemistry 20:6446–6457CrossRefGoogle Scholar
  6. 6.
    Teintze M, Leong J (1981) Biochemistry 20:6457–6462CrossRefGoogle Scholar
  7. 7.
    Reid RT, Livet DH, Faulkner DJ, Butler A (1993) Nature 366:455CrossRefGoogle Scholar
  8. 8.
    Kem MP, Butler A (2015) Biometals 28:445–459CrossRefGoogle Scholar
  9. 9.
    Martinez JS, Zhang GP, Holt PD, Jung HT, Carrano CJ, Haygood MG, Butler A (2000) Science 287:1245–1247CrossRefGoogle Scholar
  10. 10.
    Homann VV, Sandy M, Tincu JA, Templeton AS, Tebo BM, Butler A (2009) J Nat Prod 72:884–888CrossRefGoogle Scholar
  11. 11.
    Robertson AW, McCarville NG, MacIntyre LW, Correa H, Haltli B, Marchbank DH, Kerr RG (2018) J Nat Prod.  https://doi.org/10.1021/acs.jnatprod.7b00943 CrossRefPubMedGoogle Scholar
  12. 12.
    Matthijs S, Brandt N, Ongena M, Achouak W, Meyer J-M, Budzikiewicz H (2016) Biometals 29:467–485CrossRefGoogle Scholar
  13. 13.
    Matthijs S, Budzikiewicz H, Schäfer M, Wathelet B, Cornelis P (2008) Z Naturforsch C Biosci 63:8–12CrossRefGoogle Scholar
  14. 14.
    Risse D, Beiderbeck H, Taraz K, Budzikiewicz H, Gustine D (1998) Z Naturforsch C Biosci 53:295–304CrossRefGoogle Scholar
  15. 15.
    Rosconi F, Davyt D, Martínez V, Martínez M, Abin-Carriquiry JA, Zane H, Butler A, de Souza EM, Fabiano E (2013) Environ Microbiol 15:916–927CrossRefGoogle Scholar
  16. 16.
    Kurth C, Schieferdecker S, Athanasopoulou K, Seccareccia I, Nett M (2016) J Nat Prod 79:865–872CrossRefGoogle Scholar
  17. 17.
    Kreutzer MF, Nett M (2012) Org Biomol Chem 10:9338–9343CrossRefGoogle Scholar
  18. 18.
    Baars O, Zhang X, Gibson MI, Stone AT, Morel FMM, Seyedsayamdost MR (2017) Angew Chem 130:545–550CrossRefGoogle Scholar
  19. 19.
    Johnston CW, Skinnider MA, Wyatt MA, Li X, Ranieri MRM, Yang L, Zechel DL, Ma B, Magarvey NA (2015) Nat Commun 6:8421CrossRefGoogle Scholar
  20. 20.
    Kreutzer MF, Kage H, Nett M (2012) J Am Chem Soc 134:5415–5422CrossRefGoogle Scholar
  21. 21.
    Serrano Figueroa LO, Pitts B, Uchida M, Richards AM (2015) Can J Chem 94:35–43CrossRefGoogle Scholar
  22. 22.
    Serrano Figueroa LO, Schwarz B, Richards AM (2015) Extremophiles 19:1183–1192CrossRefGoogle Scholar
  23. 23.
    Richards AM (2007) Identification and structural characterization of siderophores produced by halophilic and alkaliphilic bacteria. http://www.dissertations.wsu.edu/Dissertations/Summer2007/A_Richards_072707.pdf. Accessed 30 April 2018
  24. 24.
    Demange P, Bateman A, Dell A, Abdallah MA (1988) Biochemistry 27:2745–2752CrossRefGoogle Scholar
  25. 25.
    Kanoh K, Kamino K, Leleo G, Adachi K, Shizuri Y (2003) J Antibiot 56:871–875CrossRefGoogle Scholar
  26. 26.
    Vargas-Straube MJ, Cámara B, Tello M, Montero-Silva F, Cárdenas F, Seeger M (2016) PLoS One 11:e0151273CrossRefGoogle Scholar
  27. 27.
    Franke J, Ishida K, Hertweck C (2015) Chem Eur J 21:8010–8014CrossRefGoogle Scholar
  28. 28.
    Franke J, Ishida K, Ishida-Ito M, Hertweck C (2013) Angew Chem Int Ed 52:8271–8275CrossRefGoogle Scholar
  29. 29.
    Johnston CW, Wyatt MA, Li X, Ibrahim A, Shuster J, Southam G, Magarvey NA (2013) Nat Chem Biol 9:241–243CrossRefGoogle Scholar
  30. 30.
    Vraspir JM, Holt PD, Butler A (2011) Biometals 24:85–92CrossRefGoogle Scholar
  31. 31.
    Martinez JS, Butler A (2007) J Inorg Biochem 101:1692–1698CrossRefGoogle Scholar
  32. 32.
    Meyer J-M, Van Van T, Stintzi A, Berge O, Winkelmann G (1995) Biometals 8:309–317CrossRefGoogle Scholar
  33. 33.
    Stephan H, Freund S, Beck W, Jung G, Meyer J-M, Winkelmann G (1993) Biometals 6:93–100CrossRefGoogle Scholar
  34. 34.
    Koglin A, Walsh CT (2009) Nat Prod Rep 26:987–1000CrossRefGoogle Scholar
  35. 35.
    Crosa JH, Walsh CT (2002) Microbiol Mol Biol Rev 66:223–249CrossRefGoogle Scholar
  36. 36.
    Sattely ES, Fischbach MA, Walsh CT (2008) Nat Prod Rep 25:757–793CrossRefGoogle Scholar
  37. 37.
    Parker DL, Lee S-W, Geszvain K, Davis RE, Gruffaz C, Meyer J-M, Torpey JW, Tebo BM (2014) Front Microbiol 5:202CrossRefGoogle Scholar
  38. 38.
    Chen H, Thomas MG, O’Connor SE, Hubbard BK, Burkart MD, Walsh CT (2001) Biochemistry 40:11651–11659CrossRefGoogle Scholar
  39. 39.
    Chen H, Hubbard BK, O’Connor SE, Walsh CT (2002) Chem Biol 9:103–112CrossRefGoogle Scholar
  40. 40.
    Chen H, Walsh CT (2001) Chem Biol 8:301–312CrossRefGoogle Scholar
  41. 41.
    Strieker M, Kopp F, Mahlert C, Essen L-O, Marahiel MA (2007) ACS Chem Biol 2:187–196CrossRefGoogle Scholar
  42. 42.
    Yin X, Zabriskie TM (2004) ChemBioChem 5:1274–1277CrossRefGoogle Scholar
  43. 43.
    Hashizume H, Hattori S, Igarashi M, Akamatsu Y (2004) J Antibiot 57:394–399CrossRefGoogle Scholar
  44. 44.
    Maki H, Miura K, Yamano Y (2001) Antimicrob Agents Chemother 45:1823–1827CrossRefGoogle Scholar
  45. 45.
    Naruse N, Tenmyo O, Tomita K, Konishi M, Miyaki T, Kawaguchi H, Fukase K, Wakamiya T, Shiba T (1989) J Antibiot 42:837–845CrossRefGoogle Scholar
  46. 46.
    Scaloni A, Bachmann RC, Takemoto JY, Barra D, Simmaco M, Ballio A (1994) Nat Prod Lett 4:159–164CrossRefGoogle Scholar
  47. 47.
    Fukuchi N, Isogai A, Nakayama J, Takayama S, Yamashita S, Suyama K, Takemoto JY, Suzuki A (1992) J Chem Soc. Perkin Trans 1:1149–1157CrossRefGoogle Scholar
  48. 48.
    Di Giorgio D, Camoni L, Marchiafava C, Ballio A (1997) Phytochemistry 45:1385–1391CrossRefGoogle Scholar
  49. 49.
    Scaloni A, Dalla Serra M, Amodeo P, Mannina L, Vitale RM, Segre AL, Cruciani O, Lodovichetti F, Greco ML, Fiore A, Gallo M, Ambrosio C, Coraiola M, Menestrina G, Graniti A, Fogliano V (2004) Biochem J 384:25–36CrossRefGoogle Scholar
  50. 50.
    Singh GM, Fortin PD, Koglin A, Walsh CT (2008) Biochemistry 47:11310–11320CrossRefGoogle Scholar
  51. 51.
    Eichhorn E, van der Ploeg JR, Kertesz MA, Leisinger T (1997) J Biol Chem 272:23031–23036CrossRefGoogle Scholar
  52. 52.
    Neidig ML, Brown CD, Light KM, Fujimori DG, Nolan EM, Price JC, Barr EW, Bollinger JM, Krebs C, Walsh CT, Solomon EI (2007) J Am Chem Soc 129:14224–14231CrossRefGoogle Scholar
  53. 53.
    Koehntop KD, Emerson JP, Que L (2005) J Biol Inorg Chem 10:87–93CrossRefGoogle Scholar
  54. 54.
    Bollinger JM, Price John C, Hoffart Lee M, Barr Eric W, Krebs C (2005) Eur J Inorg Chem 2005:4245–4254CrossRefGoogle Scholar
  55. 55.
    Price JC, Barr EW, Tirupati B, Bollinger JM, Krebs C (2003) Biochemistry 42:7497–7508CrossRefGoogle Scholar
  56. 56.
    Price JC, Barr EW, Glass TE, Krebs C, Bollinger JM (2003) J Am Chem Soc 125:13008–13009CrossRefGoogle Scholar
  57. 57.
    Krebs C, Galonić Fujimori D, Walsh CT, Bollinger JM (2007) Acc Chem Res 40:484–492CrossRefGoogle Scholar
  58. 58.
    Krebs C, Price JC, Baldwin J, Saleh L, Green MT, Bollinger JM (2005) Inorg Chem 44:742–757CrossRefGoogle Scholar
  59. 59.
    Grzyska PK, Appelman EH, Hausinger RP, Proshlyakov DA (2010) Proc Natl Acad Sci USA 107:3982–3987CrossRefGoogle Scholar
  60. 60.
    Mitchell AJ, Dunham NP, Martinie RJ, Bergman JA, Pollock CJ, Hu K, Allen BD, Chang W-C, Silakov A, Bollinger JM, Krebs C, Boal AK (2017) J Am Chem Soc 139:13830–13836CrossRefGoogle Scholar
  61. 61.
    Bollinger JM, Chang W, Matthews ML, Martinie RJ, Boal AK, Krebs C (2015) 2-Oxoglutarate-dependent oxygenases. R Soc Chem, London, pp 95–122CrossRefGoogle Scholar
  62. 62.
    Agnoli K, Lowe CA, Farmer KL, Husnain SI, Thomas MS (2006) J Bacteriol 188:3631–3644CrossRefGoogle Scholar
  63. 63.
    Matthijs S, Laus G, Meyer J-M, Abbaspour-Tehrani K, Schäfer M, Budzikiewicz H, Cornelis P (2009) Biometals 22:951CrossRefGoogle Scholar
  64. 64.
    Stachelhaus T, Mootz HD, Marahiel MA (1999) Chem Biol 6:493–505CrossRefGoogle Scholar
  65. 65.
    Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ, Kautsar SA, Suarez Duran HG, de los Santos ELC, Kim HU, Nave M, Dickschat JS, Mitchell DA, Shelest E, Breitling R, Takano E, Lee SY, Weber T, Medema MH (2017) Nucleic Acids Res 45:W36–W41CrossRefGoogle Scholar
  66. 66.
    Skinnider MA, Dejong CA, Rees PN, Johnston CW, Li H, Webster Andrew LH, Wyatt MA, Magarvey NA (2015) Nucleic Acids Res 43:9645–9662PubMedPubMedCentralGoogle Scholar
  67. 67.
    Holt PD, Reid RR, Lewis BL, Luther GW, Butler A (2005) Inorg Chem 44:7671–7677CrossRefGoogle Scholar
  68. 68.
    Zhang G, Amin SA, Küpper FC, Holt PD, Carrano CJ, Butler A (2009) Inorg Chem 48:11466–11473CrossRefGoogle Scholar
  69. 69.
    Butler A, Theisen RM (2010) Coord Chem Rev 254:288–296CrossRefGoogle Scholar
  70. 70.
    Fry HS, Gerwe EG (1928) Ind Eng Chem 20:1392–1394CrossRefGoogle Scholar
  71. 71.
    Abrahamson HB, Rezvani AB, Brushmiller JG (1994) Inorg Chim Acta 226:117–127CrossRefGoogle Scholar
  72. 72.
    Shweky I, Bino A, Goldberg DP, Lippard SJ (1994) Inorg Chem 33:5161–5162CrossRefGoogle Scholar
  73. 73.
    Küpper FC, Carrano CJ, Kuhn J-U, Butler A (2006) Inorg Chem 45:6028–6033CrossRefGoogle Scholar
  74. 74.
    Abergel RJ, Zawadzka AM, Raymond KN (2008) J Am Chem Soc 130:2124–2125CrossRefGoogle Scholar
  75. 75.
    Hickford SJH, Küpper FC, Zhang G, Carrano CJ, Blunt JW, Butler A (2004) J Nat Prod 67:1897–1899CrossRefGoogle Scholar
  76. 76.
    Martin JD, Ito Y, Homann VV, Haygood MG, Butler A (2006) J Biol Inorg Chem 11:633–641CrossRefGoogle Scholar
  77. 77.
    Barbeau K, Rue EL, Bruland KW, Butler A (2001) Nature 413:409–413CrossRefGoogle Scholar
  78. 78.
    Sayre H, Milos K, Goldcamp MJ, Schroll CA, Krause JA, Baldwin MJ (2010) Inorg Chem 49:4433–4439CrossRefGoogle Scholar
  79. 79.
    Grabo JE, Chrisman MA, Webb LM, Baldwin MJ (2014) Inorg Chem 53:5781–5787CrossRefGoogle Scholar
  80. 80.
    Vernia JE, Warmin MR, Krause JA, Tierney DL, Baldwin MJ (2017) Inorg Chem 56:13029–13034CrossRefGoogle Scholar
  81. 81.
    Glebov EM, Pozdnyakov IP, Grivin VP, Plyusnin VF, Zhang X, Wu F, Deng N (2011) Photochem Photobiol Sci 10:425–430CrossRefGoogle Scholar
  82. 82.
    Grabo JE, Trotta SM, Baldwin MJ (2017) Inorg Chem Commun 84:204–206CrossRefGoogle Scholar
  83. 83.
    Barbeau K (2006) Photochem Photobiol 82:1505–1516CrossRefGoogle Scholar
  84. 84.
    Barbeau K, Rue EL, Trick CG, Bruland KW, Butler A (2003) Limnol Oceanogr 48:1069–1078CrossRefGoogle Scholar
  85. 85.
    O’Sullivan DW, Hanson AK, Miller WL, Kester DR (1991) Limnol Oceanogr 36:1727–1741CrossRefGoogle Scholar
  86. 86.
    Johnson KS, Coale KH, Elrod VA, Tindale NW (1994) Mar Chem 46:319–334CrossRefGoogle Scholar
  87. 87.
    Waite TD, Szymczak R, Espey QI, Furnas MJ (1995) Mar Chem 50:79–91CrossRefGoogle Scholar
  88. 88.
    Gledhill M, van den Berg CMG (1994) Mar Chem 47:41–54CrossRefGoogle Scholar
  89. 89.
    Rue EL, Bruland KW (1995) Mar Chem 50:117–138CrossRefGoogle Scholar
  90. 90.
    Gärdes A, Triana C, Amin SA, Green DH, Romano A, Trimble L, Carrano CJ (2013) Biometals 26:507–516CrossRefGoogle Scholar
  91. 91.
    Zawadzka AM, Abergel RJ, Nichiporuk R, Andersen UN, Raymond KN (2009) Biochemistry 48:3645–3657CrossRefGoogle Scholar
  92. 92.
    Zawadzka AM, Kim Y, Maltseva N, Nichiporuk R, Fan Y, Joachimiak A, Raymond KN (2009) Proc Natl Acad Sci USA 106:21854CrossRefGoogle Scholar
  93. 93.
    Anderson MA, Morel FMM (1982) Limnol Oceanogr 27:789–813CrossRefGoogle Scholar
  94. 94.
    Amin SA, Green DH, Hart MC, Küpper FC, Sunda WG, Carrano CJ (2009) Proc Natl Acad Sci USA 106:17071–17076CrossRefGoogle Scholar

Copyright information

© SBIC 2018

Authors and Affiliations

  1. 1.Department of Chemistry and BiochemistryUniversity of CaliforniaSanta BarbaraUSA

Personalised recommendations