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Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium
Carbon metabolism is central to photosynthetic organisms and involves the coordinated operation and regulation of numerous proteins. In cyanobacteria, proteins involved in carbon metabolism are regulated by multiple regulators including the RNA polymerase sigma factor SigE, the histidine kinases Hik...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Biochemistry and Molecular Biology
2023
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10315926/ https://www.ncbi.nlm.nih.gov/pubmed/37225018 http://dx.doi.org/10.1016/j.mcpro.2023.100582 |
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author | Huang, Chengcheng Duan, Xiaoxiao Ge, Haitao Xiao, Zhen Zheng, Limin Wang, Gaojie Dong, Jinghui Wang, Yan Zhang, Yuanya Huang, Xiahe An, Hongyu Xu, Wu Wang, Yingchun |
author_facet | Huang, Chengcheng Duan, Xiaoxiao Ge, Haitao Xiao, Zhen Zheng, Limin Wang, Gaojie Dong, Jinghui Wang, Yan Zhang, Yuanya Huang, Xiahe An, Hongyu Xu, Wu Wang, Yingchun |
author_sort | Huang, Chengcheng |
collection | PubMed |
description | Carbon metabolism is central to photosynthetic organisms and involves the coordinated operation and regulation of numerous proteins. In cyanobacteria, proteins involved in carbon metabolism are regulated by multiple regulators including the RNA polymerase sigma factor SigE, the histidine kinases Hik8, Hik31 and its plasmid-borne paralog Slr6041, and the response regulator Rre37. To understand the specificity and the cross-talk of such regulations, we simultaneously and quantitatively compared the proteomes of the gene knockout mutants for the regulators. A number of proteins showing differential expression in one or more mutants were identified, including four proteins that are unanimously upregulated or downregulated in all five mutants. These represent the important nodes of the intricate and elegant regulatory network for carbon metabolism. Moreover, serine phosphorylation of P(II), a key signaling protein sensing and regulating in vivo carbon/nitrogen (C/N) homeostasis through reversible phosphorylation, is massively increased with a concomitant significant decrease in glycogen content only in the hik8-knockout mutant, which also displays impaired dark viability. An unphosphorylatable P(II) S49A substitution restored the glycogen content and rescued the dark viability of the mutant. Together, our study not only establishes the quantitative relationship between the targets and the corresponding regulators and elucidated their specificity and cross-talk but also unveils that Hik8 regulates glycogen accumulation through negative regulation of P(II) phosphorylation, providing the first line of evidence that links the two-component system with P(II)-mediated signal transduction and implicates them in the regulation of carbon metabolism. |
format | Online Article Text |
id | pubmed-10315926 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Biochemistry and Molecular Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-103159262023-07-04 Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium Huang, Chengcheng Duan, Xiaoxiao Ge, Haitao Xiao, Zhen Zheng, Limin Wang, Gaojie Dong, Jinghui Wang, Yan Zhang, Yuanya Huang, Xiahe An, Hongyu Xu, Wu Wang, Yingchun Mol Cell Proteomics Research Carbon metabolism is central to photosynthetic organisms and involves the coordinated operation and regulation of numerous proteins. In cyanobacteria, proteins involved in carbon metabolism are regulated by multiple regulators including the RNA polymerase sigma factor SigE, the histidine kinases Hik8, Hik31 and its plasmid-borne paralog Slr6041, and the response regulator Rre37. To understand the specificity and the cross-talk of such regulations, we simultaneously and quantitatively compared the proteomes of the gene knockout mutants for the regulators. A number of proteins showing differential expression in one or more mutants were identified, including four proteins that are unanimously upregulated or downregulated in all five mutants. These represent the important nodes of the intricate and elegant regulatory network for carbon metabolism. Moreover, serine phosphorylation of P(II), a key signaling protein sensing and regulating in vivo carbon/nitrogen (C/N) homeostasis through reversible phosphorylation, is massively increased with a concomitant significant decrease in glycogen content only in the hik8-knockout mutant, which also displays impaired dark viability. An unphosphorylatable P(II) S49A substitution restored the glycogen content and rescued the dark viability of the mutant. Together, our study not only establishes the quantitative relationship between the targets and the corresponding regulators and elucidated their specificity and cross-talk but also unveils that Hik8 regulates glycogen accumulation through negative regulation of P(II) phosphorylation, providing the first line of evidence that links the two-component system with P(II)-mediated signal transduction and implicates them in the regulation of carbon metabolism. American Society for Biochemistry and Molecular Biology 2023-05-22 /pmc/articles/PMC10315926/ /pubmed/37225018 http://dx.doi.org/10.1016/j.mcpro.2023.100582 Text en © 2023 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Research Huang, Chengcheng Duan, Xiaoxiao Ge, Haitao Xiao, Zhen Zheng, Limin Wang, Gaojie Dong, Jinghui Wang, Yan Zhang, Yuanya Huang, Xiahe An, Hongyu Xu, Wu Wang, Yingchun Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium |
title | Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium |
title_full | Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium |
title_fullStr | Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium |
title_full_unstemmed | Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium |
title_short | Parallel Proteomic Comparison of Mutants With Altered Carbon Metabolism Reveals Hik8 Regulation of P(II) Phosphorylation and Glycogen Accumulation in a Cyanobacterium |
title_sort | parallel proteomic comparison of mutants with altered carbon metabolism reveals hik8 regulation of p(ii) phosphorylation and glycogen accumulation in a cyanobacterium |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10315926/ https://www.ncbi.nlm.nih.gov/pubmed/37225018 http://dx.doi.org/10.1016/j.mcpro.2023.100582 |
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