An ATP-sensitive phosphoketolase regulates carbon fixation in cyanobacteria

Kuan Jen Lu; Chiung Wen Chang; Chun Hsiung Wang; Frederic Y.H. Chen; Irene Y. Huang; Pin Hsuan Huang; Cheng Han Yang; Hsiang Yi Wu; Wen Jin Wu; Kai Cheng Hsu; Meng Chiao Ho; Ming Daw Tsai

doi:10.1038/s42255-023-00831-w

An ATP-sensitive phosphoketolase regulates carbon fixation in cyanobacteria

Kuan Jen Lu, Chiung Wen Chang, Chun Hsiung Wang, Frederic Y.H. Chen, Irene Y. Huang, Pin Hsuan Huang, Cheng Han Yang, Hsiang Yi Wu, Wen Jin Wu, Kai Cheng Hsu, Meng Chiao Ho, Ming Daw Tsai

Research output: Contribution to journal › Article › peer-review

10 Citations (Scopus)

Abstract

Regulation of CO₂ fixation in cyanobacteria is important both for the organism and global carbon balance. Here we show that phosphoketolase in Synechococcus elongatus PCC7942 (SeXPK) possesses a distinct ATP-sensing mechanism, where a drop in ATP level allows SeXPK to divert precursors of the RuBisCO substrate away from the Calvin–Benson–Bassham cycle. Deleting the SeXPK gene increased CO₂ fixation particularly during light–dark transitions. In high-density cultures, the Δxpk strain showed a 60% increase in carbon fixation and unexpectedly resulted in sucrose secretion without any pathway engineering. Using cryo-EM analysis, we discovered that these functions were enabled by a unique allosteric regulatory site involving two subunits jointly binding two ATP, which constantly suppresses the activity of SeXPK until the ATP level drops. This magnesium-independent ATP allosteric site is present in many species across all three domains of life, where it may also play important regulatory functions.

Original language	English
Pages (from-to)	1111-1126
Number of pages	16
Journal	Nature Metabolism
Volume	5
Issue number	7
DOIs	https://doi.org/10.1038/s42255-023-00831-w
Publication status	Published - Jul 2023

ASJC Scopus subject areas

Internal Medicine
Endocrinology, Diabetes and Metabolism
Physiology (medical)
Cell Biology

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s42255-023-00831-w

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title = "An ATP-sensitive phosphoketolase regulates carbon fixation in cyanobacteria",

abstract = "Regulation of CO2 fixation in cyanobacteria is important both for the organism and global carbon balance. Here we show that phosphoketolase in Synechococcus elongatus PCC7942 (SeXPK) possesses a distinct ATP-sensing mechanism, where a drop in ATP level allows SeXPK to divert precursors of the RuBisCO substrate away from the Calvin–Benson–Bassham cycle. Deleting the SeXPK gene increased CO2 fixation particularly during light–dark transitions. In high-density cultures, the Δxpk strain showed a 60% increase in carbon fixation and unexpectedly resulted in sucrose secretion without any pathway engineering. Using cryo-EM analysis, we discovered that these functions were enabled by a unique allosteric regulatory site involving two subunits jointly binding two ATP, which constantly suppresses the activity of SeXPK until the ATP level drops. This magnesium-independent ATP allosteric site is present in many species across all three domains of life, where it may also play important regulatory functions.",

author = "Lu, {Kuan Jen} and Chang, {Chiung Wen} and Wang, {Chun Hsiung} and Chen, {Frederic Y.H.} and Huang, {Irene Y.} and Huang, {Pin Hsuan} and Yang, {Cheng Han} and Wu, {Hsiang Yi} and Wu, {Wen Jin} and Hsu, {Kai Cheng} and Ho, {Meng Chiao} and Tsai, {Ming Daw}",

note = "Funding Information: The work is supported by Academia Sinica (AS-KPQ-109-TPP2). Cryo-EM experiments were performed at the Academia Sinica Cryo-EM Facility, which is supported by Academia Sinica (AS-CFII-108-110), Taiwan Protein Project (AS-KPQ-109-TPP2) and Taiwan Cryo-EM Consortium funded by National Council of Science and Technology, grant no. NSTC 112-2740-B-006-001. The cryo-EM data were processed at the Academia Sinica Grid-computing Center supported by Academia Sinica. The authors thank Y.-M. Wu and K.-J. Lee for technical support and advice on cryo-EM sample screening and data collection. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = jul,

doi = "10.1038/s42255-023-00831-w",

language = "English",

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T1 - An ATP-sensitive phosphoketolase regulates carbon fixation in cyanobacteria

AU - Lu, Kuan Jen

AU - Chang, Chiung Wen

AU - Wang, Chun Hsiung

AU - Chen, Frederic Y.H.

AU - Huang, Irene Y.

AU - Huang, Pin Hsuan

AU - Yang, Cheng Han

AU - Wu, Hsiang Yi

AU - Wu, Wen Jin

AU - Hsu, Kai Cheng

AU - Ho, Meng Chiao

AU - Tsai, Ming Daw

N1 - Funding Information: The work is supported by Academia Sinica (AS-KPQ-109-TPP2). Cryo-EM experiments were performed at the Academia Sinica Cryo-EM Facility, which is supported by Academia Sinica (AS-CFII-108-110), Taiwan Protein Project (AS-KPQ-109-TPP2) and Taiwan Cryo-EM Consortium funded by National Council of Science and Technology, grant no. NSTC 112-2740-B-006-001. The cryo-EM data were processed at the Academia Sinica Grid-computing Center supported by Academia Sinica. The authors thank Y.-M. Wu and K.-J. Lee for technical support and advice on cryo-EM sample screening and data collection. Publisher Copyright: © 2023, The Author(s).

PY - 2023/7

Y1 - 2023/7

N2 - Regulation of CO2 fixation in cyanobacteria is important both for the organism and global carbon balance. Here we show that phosphoketolase in Synechococcus elongatus PCC7942 (SeXPK) possesses a distinct ATP-sensing mechanism, where a drop in ATP level allows SeXPK to divert precursors of the RuBisCO substrate away from the Calvin–Benson–Bassham cycle. Deleting the SeXPK gene increased CO2 fixation particularly during light–dark transitions. In high-density cultures, the Δxpk strain showed a 60% increase in carbon fixation and unexpectedly resulted in sucrose secretion without any pathway engineering. Using cryo-EM analysis, we discovered that these functions were enabled by a unique allosteric regulatory site involving two subunits jointly binding two ATP, which constantly suppresses the activity of SeXPK until the ATP level drops. This magnesium-independent ATP allosteric site is present in many species across all three domains of life, where it may also play important regulatory functions.

AB - Regulation of CO2 fixation in cyanobacteria is important both for the organism and global carbon balance. Here we show that phosphoketolase in Synechococcus elongatus PCC7942 (SeXPK) possesses a distinct ATP-sensing mechanism, where a drop in ATP level allows SeXPK to divert precursors of the RuBisCO substrate away from the Calvin–Benson–Bassham cycle. Deleting the SeXPK gene increased CO2 fixation particularly during light–dark transitions. In high-density cultures, the Δxpk strain showed a 60% increase in carbon fixation and unexpectedly resulted in sucrose secretion without any pathway engineering. Using cryo-EM analysis, we discovered that these functions were enabled by a unique allosteric regulatory site involving two subunits jointly binding two ATP, which constantly suppresses the activity of SeXPK until the ATP level drops. This magnesium-independent ATP allosteric site is present in many species across all three domains of life, where it may also play important regulatory functions.

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ER -

An ATP-sensitive phosphoketolase regulates carbon fixation in cyanobacteria

Abstract

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