A hemoprotein with a zinc-mirror heme site ties heme availability to carbon metabolism in cyanobacteria

Grosjean, Nicolas; Yee, Estella F.; Kumaran, Desigan; Chopra, Kriti; Abernathy, Macon; Biswas, Sandeep; Byrnes, James; Kreitler, Dale F.; Cheng, Jan-Fang; Ghosh, Agnidipta; Almo, Steven C.; Iwai, Masakazu; Niyogi, Krishna K.; Pakrasi, Himadri B.; Sarangi, Ritimukta; van Dam, Hubertus; Yang, Lin; Blaby, Ian K.; Blaby-Haas, Crysten E.

doi:10.1038/s41467-024-47486-z

Title: A hemoprotein with a zinc-mirror heme site ties heme availability to carbon metabolism in cyanobacteria

Journal Article · 11 April 2024 · Nature Communications

DOI: https://doi.org/10.1038/s41467-024-47486-z · OSTI ID:2331231

;

; Kumaran, Desigan;

; Abernathy, Macon;

; Byrnes, James; Kreitler, Dale F.;

;

; Almo, Steven C.; Iwai, Masakazu;

;

Heme has a critical role in the chemical framework of the cell as an essential protein cofactor and signaling molecule that controls diverse processes and molecular interactions. Using a phylogenomics-based approach and complementary structural techniques, we identify a family of dimeric hemoproteins comprising a domain of unknown function DUF2470. The heme iron is axially coordinated by two zinc-bound histidine residues, forming a distinct two-fold symmetric zinc-histidine-iron-histidine-zinc site. Together with structure-guided in vitro and in vivo experiments, we further demonstrate the existence of a functional link between heme binding by Dri1 (Domain related to iron 1, formerly ssr1698) and post-translational regulation of succinate dehydrogenase in the cyanobacterium Synechocystis, suggesting an iron-dependent regulatory link between photosynthesis and respiration. Given the ubiquity of proteins containing homologous domains and connections to heme metabolism across eukaryotes and prokaryotes, we propose that DRI (Domain Related to Iron; formerly DUF2470) functions at the molecular level as a heme-dependent regulatory domain.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Advanced Scientific Computing Research (ASCR); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: SC0012704; AC02-05CH11231; AC02-76SF00515; FG02-99ER20350

OSTI ID:: 2331231

Alternate ID(s):: OSTI ID: 2336838; OSTI ID: 2341819; OSTI ID: 2370371; OSTI ID: 2440004

Report Number(s):: BNL--225348-2024-JAAM

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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