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. In this work, 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-O22–, 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:
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Institutes of Health (NIH); National Science Foundation (NSF); National Institute of General Medical Sciences (NIGMS); USDOE
- OSTI Identifier:
- 1564316
- Alternate Identifier(s):
- OSTI ID: 1561301
- Grant/Contract Number:
- R35GM122535; R35GM131760; R01DE024463; R01AI078958; R01DE023080; R35GM124908; SC0013997; DMR-1332208; GM-103485; P30 GM124165; S10 RR029205
- Resource Type:
- Journal Article: 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:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; oxygen sensor; chemoreceptor; phosphatase; signal transduction; molecular evolution
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. https://doi.org/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. 2019.
"A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species". United States. https://doi.org/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. In this work, 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-O22–, 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},
url = {https://www.osti.gov/biblio/1564316},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 30,
volume = 116,
place = {United States},
year = {Wed Jul 03 00:00:00 EDT 2019},
month = {Wed Jul 03 00:00:00 EDT 2019}
}
Web of Science
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