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Title: A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species

Abstract

Many bacteria contain cytoplasmic chemoreceptors that lack sensor domains. Here, we demonstrate that such cytoplasmic receptors found in 8 different bacterial and archaeal phyla genetically couple to metalloproteins related to β-lactamases and nitric oxide reductases. We show that this oxygen-binding di-iron protein (ODP) acts as a sensor for chemotactic responses to both iron and oxygen in the human pathogen Treponema denticola ( Td ). The ODP di-iron site binds oxygen at high affinity to reversibly form an unusually stable μ-peroxo adduct. Crystal structures of ODP from Td and the thermophile Thermotoga maritima ( Tm ) in the Fe[III] 2 -O 2 2− , Zn[II], and apo states display differences in subunit association, conformation, and metal coordination that indicate potential mechanisms for sensing. In reconstituted systems, iron-peroxo ODP destabilizes the phosphorylated form of the receptor-coupled histidine kinase CheA, thereby providing a biochemical link between oxygen sensing and chemotaxis in diverse prokaryotes, including anaerobes of ancient origin.

Authors:
; ; ; ; ; ; ; ORCiD logo; ; ORCiD logo;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1564316
Grant/Contract Number:  
SC0013997
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 30; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Muok, Alise R., Deng, Yijie, Gumerov, Vadim M., Chong, Jenna E., DeRosa, Jennifer R., Kurniyati, Kurni, Coleman, Rachael E., Lancaster, Kyle M., Li, Chunhao, Zhulin, Igor B., and Crane, Brian R. A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species. United States: N. p., 2019. Web. doi:10.1073/pnas.1904234116.
Muok, Alise R., Deng, Yijie, Gumerov, Vadim M., Chong, Jenna E., DeRosa, Jennifer R., Kurniyati, Kurni, Coleman, Rachael E., Lancaster, Kyle M., Li, Chunhao, Zhulin, Igor B., & Crane, Brian R. A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species. United States. doi:10.1073/pnas.1904234116.
Muok, Alise R., Deng, Yijie, Gumerov, Vadim M., Chong, Jenna E., DeRosa, Jennifer R., Kurniyati, Kurni, Coleman, Rachael E., Lancaster, Kyle M., Li, Chunhao, Zhulin, Igor B., and Crane, Brian R. Wed . "A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species". United States. doi:10.1073/pnas.1904234116.
@article{osti_1564316,
title = {A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species},
author = {Muok, Alise R. and Deng, Yijie and Gumerov, Vadim M. and Chong, Jenna E. and DeRosa, Jennifer R. and Kurniyati, Kurni and Coleman, Rachael E. and Lancaster, Kyle M. and Li, Chunhao and Zhulin, Igor B. and Crane, Brian R.},
abstractNote = {Many bacteria contain cytoplasmic chemoreceptors that lack sensor domains. Here, we demonstrate that such cytoplasmic receptors found in 8 different bacterial and archaeal phyla genetically couple to metalloproteins related to β-lactamases and nitric oxide reductases. We show that this oxygen-binding di-iron protein (ODP) acts as a sensor for chemotactic responses to both iron and oxygen in the human pathogen Treponema denticola ( Td ). The ODP di-iron site binds oxygen at high affinity to reversibly form an unusually stable μ-peroxo adduct. Crystal structures of ODP from Td and the thermophile Thermotoga maritima ( Tm ) in the Fe[III] 2 -O 2 2− , Zn[II], and apo states display differences in subunit association, conformation, and metal coordination that indicate potential mechanisms for sensing. In reconstituted systems, iron-peroxo ODP destabilizes the phosphorylated form of the receptor-coupled histidine kinase CheA, thereby providing a biochemical link between oxygen sensing and chemotaxis in diverse prokaryotes, including anaerobes of ancient origin.},
doi = {10.1073/pnas.1904234116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 30,
volume = 116,
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
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DOI: 10.1073/pnas.1904234116

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