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 fromMicrocystis aeruginosaPCC 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 functionmore »
- Authors:
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Michigan State Univ., East Lansing, MI (United States). DOE Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); German Research Foundation (DFG); European Union (EU)
- OSTI Identifier:
- 1515797
- Alternate Identifier(s):
- OSTI ID: 1488747; OSTI ID: 1603658
- Grant/Contract Number:
- FG02-91ER20021; AC02-05CH11231; Di910/10-1; A70135; 731077
- 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:
- 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. https://doi.org/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. https://doi.org/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 fromMicrocystis aeruginosaPCC 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 = {Mon Jun 18 00:00:00 EDT 2018},
month = {Mon Jun 18 00:00:00 EDT 2018}
}
https://doi.org/10.1073/pnas.1806668115
Web of Science
Figures / Tables:
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