Structural Basis for the Unusual Qy Red-Shift and Enhanced Thermostability of the LH1 Complex from Thermochromatium tepidum

Long-Jiang Yu, Tomoaki Kawakami, Yukihiro Kimura, Zheng Yu Wang-Otomo

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

While the majority of the core light-harvesting complexes (LH1) in purple photosynthetic bacteria exhibit a Qy absorption band in the range of 870-890 nm, LH1 from the thermophilic bacterium Thermochromatium tepidum displays the Qy band at 915 nm with an enhanced thermostability. These properties are regulated by Ca2+ ions. Substitution of the Ca2+ with other divalent metal ions results in a complex with the Qy band blue-shifted to 880-890 nm and a reduced thermostability. Following the recent publication of the structure of the Ca-bound LH1-reaction center (RC) complex [Niwa, S., et al. (2014) Nature 508, 228], we have determined the crystal structures of the Sr- and Ba-substituted LH1-RC complexes with the LH1 Qy band at 888 nm. Sixteen Sr2+ and Ba2+ ions are identified in the LH1 complexes. Both Sr2+ and Ba2+ are located at the same positions, and these are clearly different from, though close to, the Ca2+-binding sites. Conformational rearrangement induced by the substitution is limited to the metal-binding sites. Unlike the Ca-LH1-RC complex, only the α-polypeptides are involved in the Sr and Ba coordinations in LH1. The difference in the thermostability between these complexes can be attributed to the different patterns of the network formed by metal binding. The Sr- and Ba-LH1-RC complexes form a single-ring network by the LH1 α-polypeptides only, in contrast to the double-ring network composed of both α- and β-polypeptides in the Ca-LH1-RC complex. On the basis of the structural information, a combined effect of hydrogen bonding, structural integrity, and charge distribution is considered to influence the spectral properties of the core antenna complex.

Original languageEnglish
Pages (from-to)6495-6504
Number of pages10
JournalBiochemistry
Volume55
Issue number47
DOIs
Publication statusPublished - Nov 29 2016

Fingerprint

Metals
Ions
Peptides
Bacteria
Substitution reactions
Binding Sites
Proteobacteria
Charge distribution
Structural integrity
Hydrogen Bonding
Metal ions
Absorption spectra
Hydrogen bonds
Crystal structure
Antennas
Light

ASJC Scopus subject areas

  • Biochemistry

Cite this

Structural Basis for the Unusual Qy Red-Shift and Enhanced Thermostability of the LH1 Complex from Thermochromatium tepidum. / Yu, Long-Jiang; Kawakami, Tomoaki; Kimura, Yukihiro; Wang-Otomo, Zheng Yu.

In: Biochemistry, Vol. 55, No. 47, 29.11.2016, p. 6495-6504.

Research output: Contribution to journalArticle

Yu, Long-Jiang ; Kawakami, Tomoaki ; Kimura, Yukihiro ; Wang-Otomo, Zheng Yu. / Structural Basis for the Unusual Qy Red-Shift and Enhanced Thermostability of the LH1 Complex from Thermochromatium tepidum. In: Biochemistry. 2016 ; Vol. 55, No. 47. pp. 6495-6504.
@article{7abbd95b322e45749bc0d4c6aede0bc7,
title = "Structural Basis for the Unusual Qy Red-Shift and Enhanced Thermostability of the LH1 Complex from Thermochromatium tepidum",
abstract = "While the majority of the core light-harvesting complexes (LH1) in purple photosynthetic bacteria exhibit a Qy absorption band in the range of 870-890 nm, LH1 from the thermophilic bacterium Thermochromatium tepidum displays the Qy band at 915 nm with an enhanced thermostability. These properties are regulated by Ca2+ ions. Substitution of the Ca2+ with other divalent metal ions results in a complex with the Qy band blue-shifted to 880-890 nm and a reduced thermostability. Following the recent publication of the structure of the Ca-bound LH1-reaction center (RC) complex [Niwa, S., et al. (2014) Nature 508, 228], we have determined the crystal structures of the Sr- and Ba-substituted LH1-RC complexes with the LH1 Qy band at 888 nm. Sixteen Sr2+ and Ba2+ ions are identified in the LH1 complexes. Both Sr2+ and Ba2+ are located at the same positions, and these are clearly different from, though close to, the Ca2+-binding sites. Conformational rearrangement induced by the substitution is limited to the metal-binding sites. Unlike the Ca-LH1-RC complex, only the α-polypeptides are involved in the Sr and Ba coordinations in LH1. The difference in the thermostability between these complexes can be attributed to the different patterns of the network formed by metal binding. The Sr- and Ba-LH1-RC complexes form a single-ring network by the LH1 α-polypeptides only, in contrast to the double-ring network composed of both α- and β-polypeptides in the Ca-LH1-RC complex. On the basis of the structural information, a combined effect of hydrogen bonding, structural integrity, and charge distribution is considered to influence the spectral properties of the core antenna complex.",
author = "Long-Jiang Yu and Tomoaki Kawakami and Yukihiro Kimura and Wang-Otomo, {Zheng Yu}",
year = "2016",
month = "11",
day = "29",
doi = "10.1021/acs.biochem.6b00742",
language = "English",
volume = "55",
pages = "6495--6504",
journal = "Biochemistry",
issn = "0006-2960",
publisher = "American Chemical Society",
number = "47",

}

TY - JOUR

T1 - Structural Basis for the Unusual Qy Red-Shift and Enhanced Thermostability of the LH1 Complex from Thermochromatium tepidum

AU - Yu, Long-Jiang

AU - Kawakami, Tomoaki

AU - Kimura, Yukihiro

AU - Wang-Otomo, Zheng Yu

PY - 2016/11/29

Y1 - 2016/11/29

N2 - While the majority of the core light-harvesting complexes (LH1) in purple photosynthetic bacteria exhibit a Qy absorption band in the range of 870-890 nm, LH1 from the thermophilic bacterium Thermochromatium tepidum displays the Qy band at 915 nm with an enhanced thermostability. These properties are regulated by Ca2+ ions. Substitution of the Ca2+ with other divalent metal ions results in a complex with the Qy band blue-shifted to 880-890 nm and a reduced thermostability. Following the recent publication of the structure of the Ca-bound LH1-reaction center (RC) complex [Niwa, S., et al. (2014) Nature 508, 228], we have determined the crystal structures of the Sr- and Ba-substituted LH1-RC complexes with the LH1 Qy band at 888 nm. Sixteen Sr2+ and Ba2+ ions are identified in the LH1 complexes. Both Sr2+ and Ba2+ are located at the same positions, and these are clearly different from, though close to, the Ca2+-binding sites. Conformational rearrangement induced by the substitution is limited to the metal-binding sites. Unlike the Ca-LH1-RC complex, only the α-polypeptides are involved in the Sr and Ba coordinations in LH1. The difference in the thermostability between these complexes can be attributed to the different patterns of the network formed by metal binding. The Sr- and Ba-LH1-RC complexes form a single-ring network by the LH1 α-polypeptides only, in contrast to the double-ring network composed of both α- and β-polypeptides in the Ca-LH1-RC complex. On the basis of the structural information, a combined effect of hydrogen bonding, structural integrity, and charge distribution is considered to influence the spectral properties of the core antenna complex.

AB - While the majority of the core light-harvesting complexes (LH1) in purple photosynthetic bacteria exhibit a Qy absorption band in the range of 870-890 nm, LH1 from the thermophilic bacterium Thermochromatium tepidum displays the Qy band at 915 nm with an enhanced thermostability. These properties are regulated by Ca2+ ions. Substitution of the Ca2+ with other divalent metal ions results in a complex with the Qy band blue-shifted to 880-890 nm and a reduced thermostability. Following the recent publication of the structure of the Ca-bound LH1-reaction center (RC) complex [Niwa, S., et al. (2014) Nature 508, 228], we have determined the crystal structures of the Sr- and Ba-substituted LH1-RC complexes with the LH1 Qy band at 888 nm. Sixteen Sr2+ and Ba2+ ions are identified in the LH1 complexes. Both Sr2+ and Ba2+ are located at the same positions, and these are clearly different from, though close to, the Ca2+-binding sites. Conformational rearrangement induced by the substitution is limited to the metal-binding sites. Unlike the Ca-LH1-RC complex, only the α-polypeptides are involved in the Sr and Ba coordinations in LH1. The difference in the thermostability between these complexes can be attributed to the different patterns of the network formed by metal binding. The Sr- and Ba-LH1-RC complexes form a single-ring network by the LH1 α-polypeptides only, in contrast to the double-ring network composed of both α- and β-polypeptides in the Ca-LH1-RC complex. On the basis of the structural information, a combined effect of hydrogen bonding, structural integrity, and charge distribution is considered to influence the spectral properties of the core antenna complex.

UR - http://www.scopus.com/inward/record.url?scp=85000997436&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85000997436&partnerID=8YFLogxK

U2 - 10.1021/acs.biochem.6b00742

DO - 10.1021/acs.biochem.6b00742

M3 - Article

C2 - 27933779

AN - SCOPUS:85000997436

VL - 55

SP - 6495

EP - 6504

JO - Biochemistry

JF - Biochemistry

SN - 0006-2960

IS - 47

ER -