Vibrational analysis of mononitrosyl complexes in hemerythrin and flavodiiron proteins: Relevance to detoxifying no reductase

Takahiro Hayashi, Jonathan D. Caranto, Hirotoshi Matsumura, Donald M. Kurtz, Pierre Moenne-Loccoz

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Abstract

Flavodiiron proteins (FDPs) play important roles in the microbial nitrosative stress response in low-oxygen environments by reductively scavenging nitric oxide (NO). Recently, we showed that FMN-free diferrous FDP from Thermotoga maritima exposed to 1 equiv NO forms a stable diiron-mononitrosyl complex (deflavo-FDP(NO)) that can react further with NO to form N 2O [ Hayashi, T.; Caranto, J. D.; Wampler, D. A; Kurtz, D. M., Jr.; Moënne-Loccoz, P.Biochemistry 2010, 49, 7040-7049 ]. Here we report resonance Raman and low-temperature photolysis FTIR data that better define the structure of this diiron-mononitrosyl complex. We first validate this approach using the stable diiron-mononitrosyl complex of hemerythrin, Hr(NO), for which we observe a ν(NO) at 1658 cm -1, the lowest ν(NO) ever reported for a nonheme {FeNO} 7 species. Both deflavo-FDP(NO) and the mononitrosyl adduct of the flavinated FPD (FDP(NO)) show ν(NO) at 1681 cm -1, which is also unusually low. These results indicate that, in Hr(NO) and FDP(NO), the coordinated NO is exceptionally electron rich, more closely approaching the Fe(III)(NO -) resonance structure. In the case of Hr(NO), this polarization may be promoted by steric enforcement of an unusually small FeNO angle, while in FDP(NO), the Fe(III)(NO -) structure may be due to a semibridging electrostatic interaction with the second Fe(II) ion. In Hr(NO), accessibility and steric constraints prevent further reaction of the diiron-mononitrosyl complex with NO, whereas in FDP(NO) the increased nucleophilicity of the nitrosyl group may promote attack by a second NO to produce N 2O. This latter scenario is supported by theoretical modeling [ Blomberg, L. M.; Blomberg, M. R.; Siegbahn, P. E.J. Biol. Inorg. Chem. 2007, 12, 79-89 ]. Published vibrational data on bioengineered models of denitrifying heme-nonheme NO reductases [ Hayashi, T.; Miner, K. D.; Yeung, N.; Lin, Y.-W.; Lu, Y.; Moënne-Loccoz, P.Biochemistry 2011, 50, 5939-5947 ] support a similar mode of activation of a heme {FeNO} 7 species by the nearby nonheme Fe(II).

Original languageEnglish (US)
Pages (from-to)6878-6884
Number of pages7
JournalJournal of the American Chemical Society
Volume134
Issue number15
DOIs
StatePublished - Apr 18 2012

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Hemerythrin
Nitric oxide
Oxidoreductases
Nitric Oxide
Proteins
Biochemistry
Heme

ASJC Scopus subject areas

  • Chemistry(all)
  • Catalysis
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

Vibrational analysis of mononitrosyl complexes in hemerythrin and flavodiiron proteins : Relevance to detoxifying no reductase. / Hayashi, Takahiro; Caranto, Jonathan D.; Matsumura, Hirotoshi; Kurtz, Donald M.; Moenne-Loccoz, Pierre.

In: Journal of the American Chemical Society, Vol. 134, No. 15, 18.04.2012, p. 6878-6884.

Research output: Contribution to journalArticle

Hayashi, Takahiro ; Caranto, Jonathan D. ; Matsumura, Hirotoshi ; Kurtz, Donald M. ; Moenne-Loccoz, Pierre. / Vibrational analysis of mononitrosyl complexes in hemerythrin and flavodiiron proteins : Relevance to detoxifying no reductase. In: Journal of the American Chemical Society. 2012 ; Vol. 134, No. 15. pp. 6878-6884.
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title = "Vibrational analysis of mononitrosyl complexes in hemerythrin and flavodiiron proteins: Relevance to detoxifying no reductase",
abstract = "Flavodiiron proteins (FDPs) play important roles in the microbial nitrosative stress response in low-oxygen environments by reductively scavenging nitric oxide (NO). Recently, we showed that FMN-free diferrous FDP from Thermotoga maritima exposed to 1 equiv NO forms a stable diiron-mononitrosyl complex (deflavo-FDP(NO)) that can react further with NO to form N 2O [ Hayashi, T.; Caranto, J. D.; Wampler, D. A; Kurtz, D. M., Jr.; Mo{\"e}nne-Loccoz, P.Biochemistry 2010, 49, 7040-7049 ]. Here we report resonance Raman and low-temperature photolysis FTIR data that better define the structure of this diiron-mononitrosyl complex. We first validate this approach using the stable diiron-mononitrosyl complex of hemerythrin, Hr(NO), for which we observe a ν(NO) at 1658 cm -1, the lowest ν(NO) ever reported for a nonheme {FeNO} 7 species. Both deflavo-FDP(NO) and the mononitrosyl adduct of the flavinated FPD (FDP(NO)) show ν(NO) at 1681 cm -1, which is also unusually low. These results indicate that, in Hr(NO) and FDP(NO), the coordinated NO is exceptionally electron rich, more closely approaching the Fe(III)(NO -) resonance structure. In the case of Hr(NO), this polarization may be promoted by steric enforcement of an unusually small FeNO angle, while in FDP(NO), the Fe(III)(NO -) structure may be due to a semibridging electrostatic interaction with the second Fe(II) ion. In Hr(NO), accessibility and steric constraints prevent further reaction of the diiron-mononitrosyl complex with NO, whereas in FDP(NO) the increased nucleophilicity of the nitrosyl group may promote attack by a second NO to produce N 2O. This latter scenario is supported by theoretical modeling [ Blomberg, L. M.; Blomberg, M. R.; Siegbahn, P. E.J. Biol. Inorg. Chem. 2007, 12, 79-89 ]. Published vibrational data on bioengineered models of denitrifying heme-nonheme NO reductases [ Hayashi, T.; Miner, K. D.; Yeung, N.; Lin, Y.-W.; Lu, Y.; Mo{\"e}nne-Loccoz, P.Biochemistry 2011, 50, 5939-5947 ] support a similar mode of activation of a heme {FeNO} 7 species by the nearby nonheme Fe(II).",
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T1 - Vibrational analysis of mononitrosyl complexes in hemerythrin and flavodiiron proteins

T2 - Relevance to detoxifying no reductase

AU - Hayashi, Takahiro

AU - Caranto, Jonathan D.

AU - Matsumura, Hirotoshi

AU - Kurtz, Donald M.

AU - Moenne-Loccoz, Pierre

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N2 - Flavodiiron proteins (FDPs) play important roles in the microbial nitrosative stress response in low-oxygen environments by reductively scavenging nitric oxide (NO). Recently, we showed that FMN-free diferrous FDP from Thermotoga maritima exposed to 1 equiv NO forms a stable diiron-mononitrosyl complex (deflavo-FDP(NO)) that can react further with NO to form N 2O [ Hayashi, T.; Caranto, J. D.; Wampler, D. A; Kurtz, D. M., Jr.; Moënne-Loccoz, P.Biochemistry 2010, 49, 7040-7049 ]. Here we report resonance Raman and low-temperature photolysis FTIR data that better define the structure of this diiron-mononitrosyl complex. We first validate this approach using the stable diiron-mononitrosyl complex of hemerythrin, Hr(NO), for which we observe a ν(NO) at 1658 cm -1, the lowest ν(NO) ever reported for a nonheme {FeNO} 7 species. Both deflavo-FDP(NO) and the mononitrosyl adduct of the flavinated FPD (FDP(NO)) show ν(NO) at 1681 cm -1, which is also unusually low. These results indicate that, in Hr(NO) and FDP(NO), the coordinated NO is exceptionally electron rich, more closely approaching the Fe(III)(NO -) resonance structure. In the case of Hr(NO), this polarization may be promoted by steric enforcement of an unusually small FeNO angle, while in FDP(NO), the Fe(III)(NO -) structure may be due to a semibridging electrostatic interaction with the second Fe(II) ion. In Hr(NO), accessibility and steric constraints prevent further reaction of the diiron-mononitrosyl complex with NO, whereas in FDP(NO) the increased nucleophilicity of the nitrosyl group may promote attack by a second NO to produce N 2O. This latter scenario is supported by theoretical modeling [ Blomberg, L. M.; Blomberg, M. R.; Siegbahn, P. E.J. Biol. Inorg. Chem. 2007, 12, 79-89 ]. Published vibrational data on bioengineered models of denitrifying heme-nonheme NO reductases [ Hayashi, T.; Miner, K. D.; Yeung, N.; Lin, Y.-W.; Lu, Y.; Moënne-Loccoz, P.Biochemistry 2011, 50, 5939-5947 ] support a similar mode of activation of a heme {FeNO} 7 species by the nearby nonheme Fe(II).

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