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Title: Structural and functional insights into the unique CBS–CP12 fusion protein family in cyanobacteria

Abstract

Cyanobacteria are important photosynthetic organisms inhabiting a range of dynamic environments. This phylum is distinctive among photosynthetic organisms in containing genes encoding uncharacterized cystathionine β-synthase (CBS)–chloroplast protein (CP12) fusion proteins. These consist of two domains, each recognized as stand-alone photosynthetic regulators with different functions described in cyanobacteria (CP12) and plants (CP12 and CBSX). Here we show that CBS–CP12 fusion proteins are encoded in distinct gene neighborhoods, several unrelated to photosynthesis. Most frequently, CBS–CP12 genes are in a gene cluster with thioredoxin A (TrxA), which is prevalent in bloom-forming, marine symbiotic, and benthic mat cyanobacteria. Focusing on a CBS–CP12 from Microcystis aeruginosa PCC 7806 encoded in a gene cluster with TrxA, we reveal that the domain fusion led to the formation of a hexameric protein. We show that the CP12 domain is essential for hexamerization and contains an ordered, previously structurally uncharacterized N-terminal region. We provide evidence that CBS–CP12, while combining properties of both regulatory domains, behaves different from CP12 and plant CBSX. It does not form a ternary complex with phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase. Instead, CBS–CP12 decreases the activity of PRK in an AMP-dependent manner. We propose that the novel domain architecture and oligomeric state of CBS–CP12 expand itsmore » regulatory function beyond those of CP12 in cyanobacteria.« less

Authors:
; ; ; ; ; ; ; ; ORCiD logo; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1515797
Alternate Identifier(s):
OSTI ID: 1488747
Grant/Contract Number:  
FG02-91ER20021; AC02-05CH11231
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: 115 Journal Issue: 27; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; crystal structure; hexamer; redox; Microcystis aeruginosa

Citation Formats

Hackenberg, Claudia, Hakanpää, Johanna, Cai, Fei, Antonyuk, Svetlana, Eigner, Caroline, Meissner, Sven, Laitaoja, Mikko, Jänis, Janne, Kerfeld, Cheryl A., Dittmann, Elke, and Lamzin, Victor S. Structural and functional insights into the unique CBS–CP12 fusion protein family in cyanobacteria. United States: N. p., 2018. Web. doi:10.1073/pnas.1806668115.
Hackenberg, Claudia, Hakanpää, Johanna, Cai, Fei, Antonyuk, Svetlana, Eigner, Caroline, Meissner, Sven, Laitaoja, Mikko, Jänis, Janne, Kerfeld, Cheryl A., Dittmann, Elke, & Lamzin, Victor S. Structural and functional insights into the unique CBS–CP12 fusion protein family in cyanobacteria. United States. doi:10.1073/pnas.1806668115.
Hackenberg, Claudia, Hakanpää, Johanna, Cai, Fei, Antonyuk, Svetlana, Eigner, Caroline, Meissner, Sven, Laitaoja, Mikko, Jänis, Janne, Kerfeld, Cheryl A., Dittmann, Elke, and Lamzin, Victor S. Mon . "Structural and functional insights into the unique CBS–CP12 fusion protein family in cyanobacteria". United States. doi:10.1073/pnas.1806668115.
@article{osti_1515797,
title = {Structural and functional insights into the unique CBS–CP12 fusion protein family in cyanobacteria},
author = {Hackenberg, Claudia and Hakanpää, Johanna and Cai, Fei and Antonyuk, Svetlana and Eigner, Caroline and Meissner, Sven and Laitaoja, Mikko and Jänis, Janne and Kerfeld, Cheryl A. and Dittmann, Elke and Lamzin, Victor S.},
abstractNote = {Cyanobacteria are important photosynthetic organisms inhabiting a range of dynamic environments. This phylum is distinctive among photosynthetic organisms in containing genes encoding uncharacterized cystathionine β-synthase (CBS)–chloroplast protein (CP12) fusion proteins. These consist of two domains, each recognized as stand-alone photosynthetic regulators with different functions described in cyanobacteria (CP12) and plants (CP12 and CBSX). Here we show that CBS–CP12 fusion proteins are encoded in distinct gene neighborhoods, several unrelated to photosynthesis. Most frequently, CBS–CP12 genes are in a gene cluster with thioredoxin A (TrxA), which is prevalent in bloom-forming, marine symbiotic, and benthic mat cyanobacteria. Focusing on a CBS–CP12 from Microcystis aeruginosa PCC 7806 encoded in a gene cluster with TrxA, we reveal that the domain fusion led to the formation of a hexameric protein. We show that the CP12 domain is essential for hexamerization and contains an ordered, previously structurally uncharacterized N-terminal region. We provide evidence that CBS–CP12, while combining properties of both regulatory domains, behaves different from CP12 and plant CBSX. It does not form a ternary complex with phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase. Instead, CBS–CP12 decreases the activity of PRK in an AMP-dependent manner. We propose that the novel domain architecture and oligomeric state of CBS–CP12 expand its regulatory function beyond those of CP12 in cyanobacteria.},
doi = {10.1073/pnas.1806668115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 27,
volume = 115,
place = {United States},
year = {2018},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1806668115

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Cited by: 4 works
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Figures / Tables:

Fig. 1. Fig. 1.: CBS–CP12 variants and gene neighborhood conservation. (A) Domain organization of the five CBS–CP12 variants. CBS–CP12-N/C contains both cysteine pairs in the CP12 domain, CBS–CP12-N only the N-terminal pair, and CBS–CP12-0 lacks both cysteine pairs. CBS–CP12-N-tr contains a truncated CP12 domain with the N-terminal cysteine pair, and CBS–CP12-tr possessesmore » only a short CP12 domain without cysteine pairs. The distribution of the five CBS–CP12 variants within the cyanobacterial phylum is displayed in SI Appendix, Fig. S1. (B) Selected list of gene neighborhoods of CBS–CP12 genes in different cyanobacteria. Note that a CBS–CP12 gene is also copresent in the hydrogenase gene cluster of Synechococcus sp. PCC 7002. (C) Conservation of 12 gene cluster types featuring a CBS–CP12 and a TrxA gene. Note that one gene cluster type occurs in bloom-forming and marine symbiotic cyanobacteria (M. aeruginosa PCC 7806 and Prochloron P2 Fiji).« less

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    Works referencing / citing this record:

    Structural and functional insights into the unique CBS–CP12 fusion protein family in cyanobacteria
    text, January 2018

    • Hackenberg, Claudia; Hakanpää, Johanna; Cai, Fei
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.