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

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.

doi:10.1073/pnas.1904234116

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

Journal Article · 03 July 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1904234116 · OSTI ID:1564316

Muok, Alise R.; Deng, Yijie; Gumerov, Vadim M.; Chong, Jenna E.; DeRosa, Jennifer R.; Kurniyati, Kurni; Coleman, Rachael E.;

; Li, Chunhao;

; Crane, Brian R.

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-O₂^2–, 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.

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Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); National Institute of General Medical Sciences (NIGMS); USDOE

Grant/Contract Number:: SC0013997

OSTI ID:: 1564316

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 30 Vol. 116; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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