Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana

Adam Kustka, Allen J. Milligan, Haiyan Zheng, Ashley M. New, Colin Gates, Kay Bidle, John Reinfelder

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

The mechanisms of carbon concentration in marine diatoms are controversial. At low CO2, decreases in O2 evolution after inhibition of phosphoenolpyruvate carboxylases (PEPCs), and increases in PEPC transcript abundances, have been interpreted as evidence for a C4 mechanism in Thalassiosira pseudonana, but the ascertainment of which proteins are responsible for the subsequent decarboxylation and PEP regeneration steps has been elusive. We evaluated the responses of T. pseudonana to steady-state differences in CO2 availability, as well as to transient shifts to low CO2, by integrated measurements of photosynthetic parameters, transcript abundances and quantitative proteomics. On shifts to low CO2, two PEPC transcript abundances increased and then declined on timescales consistent with recoveries of Fv/Fm, non-photochemical quenching (NPQ) and maximum chlorophyll a-specific carbon fixation (Pmax), but transcripts for archetypical decarboxylation enzymes phosphoenolpyruvate carboxykinase (PEPCK) and malic enzyme (ME) did not change. Of 3688 protein abundances measured, 39 were up-regulated under low CO2, including both PEPCs and pyruvate carboxylase (PYC), whereas ME abundance did not change and PEPCK abundance declined. We propose a closed-loop biochemical model, whereby T. pseudonana produces and subsequently decarboxylates a C4 acid via PEPC2 and PYC, respectively, regenerates phosphoenolpyruvate (PEP) from pyruvate in a pyruvate phosphate dikinase-independent (but glycine decarboxylase (GDC)-dependent) manner, and recuperates photorespiratory CO2 as oxaloacetate (OAA).

Original languageEnglish (US)
Pages (from-to)507-520
Number of pages14
JournalNew Phytologist
Volume204
Issue number3
DOIs
StatePublished - Nov 1 2014

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Phosphoenolpyruvate Carboxylase
Thalassiosira
Phosphoenolpyruvate
Carbon
phosphoenolpyruvate carboxylase
carbon dioxide
Pyruvate Carboxylase
phosphoenolpyruvate carboxykinase (pyrophosphate)
Decarboxylation
metabolism
carbon
pyruvate carboxylase
Glycine Dehydrogenase (Decarboxylating)
Orthophosphate Dikinase Pyruvate
Enzymes
decarboxylation
malic enzyme
Carbon Cycle
Oxaloacetic Acid
Diatoms

All Science Journal Classification (ASJC) codes

  • Physiology
  • Plant Science

Keywords

  • C metabolism
  • Fatty acid metabolism
  • Glycine decarboxylase
  • Marine diatoms
  • Pentose phosphate pathway
  • Pyruvate carboxylase
  • Pyruvate phosphate dikinase (PPDK)
  • Quantitative proteomics

Cite this

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title = "Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana",
abstract = "The mechanisms of carbon concentration in marine diatoms are controversial. At low CO2, decreases in O2 evolution after inhibition of phosphoenolpyruvate carboxylases (PEPCs), and increases in PEPC transcript abundances, have been interpreted as evidence for a C4 mechanism in Thalassiosira pseudonana, but the ascertainment of which proteins are responsible for the subsequent decarboxylation and PEP regeneration steps has been elusive. We evaluated the responses of T. pseudonana to steady-state differences in CO2 availability, as well as to transient shifts to low CO2, by integrated measurements of photosynthetic parameters, transcript abundances and quantitative proteomics. On shifts to low CO2, two PEPC transcript abundances increased and then declined on timescales consistent with recoveries of Fv/Fm, non-photochemical quenching (NPQ) and maximum chlorophyll a-specific carbon fixation (Pmax), but transcripts for archetypical decarboxylation enzymes phosphoenolpyruvate carboxykinase (PEPCK) and malic enzyme (ME) did not change. Of 3688 protein abundances measured, 39 were up-regulated under low CO2, including both PEPCs and pyruvate carboxylase (PYC), whereas ME abundance did not change and PEPCK abundance declined. We propose a closed-loop biochemical model, whereby T. pseudonana produces and subsequently decarboxylates a C4 acid via PEPC2 and PYC, respectively, regenerates phosphoenolpyruvate (PEP) from pyruvate in a pyruvate phosphate dikinase-independent (but glycine decarboxylase (GDC)-dependent) manner, and recuperates photorespiratory CO2 as oxaloacetate (OAA).",
keywords = "C metabolism, Fatty acid metabolism, Glycine decarboxylase, Marine diatoms, Pentose phosphate pathway, Pyruvate carboxylase, Pyruvate phosphate dikinase (PPDK), Quantitative proteomics",
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Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana. / Kustka, Adam; Milligan, Allen J.; Zheng, Haiyan; New, Ashley M.; Gates, Colin; Bidle, Kay; Reinfelder, John.

In: New Phytologist, Vol. 204, No. 3, 01.11.2014, p. 507-520.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana

AU - Kustka, Adam

AU - Milligan, Allen J.

AU - Zheng, Haiyan

AU - New, Ashley M.

AU - Gates, Colin

AU - Bidle, Kay

AU - Reinfelder, John

PY - 2014/11/1

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N2 - The mechanisms of carbon concentration in marine diatoms are controversial. At low CO2, decreases in O2 evolution after inhibition of phosphoenolpyruvate carboxylases (PEPCs), and increases in PEPC transcript abundances, have been interpreted as evidence for a C4 mechanism in Thalassiosira pseudonana, but the ascertainment of which proteins are responsible for the subsequent decarboxylation and PEP regeneration steps has been elusive. We evaluated the responses of T. pseudonana to steady-state differences in CO2 availability, as well as to transient shifts to low CO2, by integrated measurements of photosynthetic parameters, transcript abundances and quantitative proteomics. On shifts to low CO2, two PEPC transcript abundances increased and then declined on timescales consistent with recoveries of Fv/Fm, non-photochemical quenching (NPQ) and maximum chlorophyll a-specific carbon fixation (Pmax), but transcripts for archetypical decarboxylation enzymes phosphoenolpyruvate carboxykinase (PEPCK) and malic enzyme (ME) did not change. Of 3688 protein abundances measured, 39 were up-regulated under low CO2, including both PEPCs and pyruvate carboxylase (PYC), whereas ME abundance did not change and PEPCK abundance declined. We propose a closed-loop biochemical model, whereby T. pseudonana produces and subsequently decarboxylates a C4 acid via PEPC2 and PYC, respectively, regenerates phosphoenolpyruvate (PEP) from pyruvate in a pyruvate phosphate dikinase-independent (but glycine decarboxylase (GDC)-dependent) manner, and recuperates photorespiratory CO2 as oxaloacetate (OAA).

AB - The mechanisms of carbon concentration in marine diatoms are controversial. At low CO2, decreases in O2 evolution after inhibition of phosphoenolpyruvate carboxylases (PEPCs), and increases in PEPC transcript abundances, have been interpreted as evidence for a C4 mechanism in Thalassiosira pseudonana, but the ascertainment of which proteins are responsible for the subsequent decarboxylation and PEP regeneration steps has been elusive. We evaluated the responses of T. pseudonana to steady-state differences in CO2 availability, as well as to transient shifts to low CO2, by integrated measurements of photosynthetic parameters, transcript abundances and quantitative proteomics. On shifts to low CO2, two PEPC transcript abundances increased and then declined on timescales consistent with recoveries of Fv/Fm, non-photochemical quenching (NPQ) and maximum chlorophyll a-specific carbon fixation (Pmax), but transcripts for archetypical decarboxylation enzymes phosphoenolpyruvate carboxykinase (PEPCK) and malic enzyme (ME) did not change. Of 3688 protein abundances measured, 39 were up-regulated under low CO2, including both PEPCs and pyruvate carboxylase (PYC), whereas ME abundance did not change and PEPCK abundance declined. We propose a closed-loop biochemical model, whereby T. pseudonana produces and subsequently decarboxylates a C4 acid via PEPC2 and PYC, respectively, regenerates phosphoenolpyruvate (PEP) from pyruvate in a pyruvate phosphate dikinase-independent (but glycine decarboxylase (GDC)-dependent) manner, and recuperates photorespiratory CO2 as oxaloacetate (OAA).

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KW - Pentose phosphate pathway

KW - Pyruvate carboxylase

KW - Pyruvate phosphate dikinase (PPDK)

KW - Quantitative proteomics

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