The mechanism of photosystem-II inactivation during sulphur deprivation-induced H2 production in Chlamydomonas reinhardtii

Valéria Nagy, André Vidal-Meireles, Anna Podmaniczki, K. Szentmihályi, G. Rákhely, Laura Zsigmond, László Kovács, Szilvia Z. Tóth

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Sulphur limitation may restrain cell growth and viability. In the green alga Chlamydomonas reinhardtii, sulphur limitation may induce H2 production lasting for several days, which can be exploited as a renewable energy source. Sulphur limitation causes a large number of physiological changes, including the inactivation of photosystem II (PSII), leading to the establishment of hypoxia, essential for the increase in hydrogenase expression and activity. The inactivation of PSII has long been assumed to be caused by the sulphur-limited turnover of its reaction center protein PsbA. Here we reinvestigated this issue in detail and show that: (i) upon transferring Chlamydomonas cells to sulphur-free media, the cellular sulphur content decreases only by about 25%; (ii) as demonstrated by lincomycin treatments, PsbA has a significant turnover, and other photosynthetic subunits, namely RbcL and CP43, are degraded more rapidly than PsbA. On the other hand, sulphur limitation imposes oxidative stress early on, most probably involving the formation of singlet oxygen in PSII, which leads to an increase in the expression of GDP-L-galactose phosphorylase, playing an essential role in ascorbate biosynthesis. When accumulated to the millimolar concentration range, ascorbate may inactivate the oxygen-evolving complex and provide electrons to PSII, albeit at a low rate. In the absence of a functional donor side and sufficient electron transport, PSII reaction centers are inactivated and degraded. We therefore demonstrate that the inactivation of PSII is a complex and multistep process, which may serve to mitigate the damaging effects of sulphur limitation.

Original languageEnglish
Pages (from-to)548-561
Number of pages14
JournalPlant Journal
Volume94
Issue number3
DOIs
Publication statusPublished - May 1 2018

Fingerprint

Chlamydomonas reinhardtii
hydrogen production
Photosystem II Protein Complex
Sulfur
photosystem II
inactivation
sulfur
Renewable Energy
Lincomycin
oxygen evolving complex
Chlamydomonas
Hydrogenase
Phosphorylases
lincomycin
Singlet Oxygen
Chlorophyta
singlet oxygen
phosphorylase
renewable energy sources
Electron Transport

Keywords

  • ascorbate
  • Chlamydomonas reinhardtii
  • hydrogen production
  • photosystem II
  • PsbA
  • sulphur

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

The mechanism of photosystem-II inactivation during sulphur deprivation-induced H2 production in Chlamydomonas reinhardtii. / Nagy, Valéria; Vidal-Meireles, André; Podmaniczki, Anna; Szentmihályi, K.; Rákhely, G.; Zsigmond, Laura; Kovács, László; Tóth, Szilvia Z.

In: Plant Journal, Vol. 94, No. 3, 01.05.2018, p. 548-561.

Research output: Contribution to journalArticle

Nagy, Valéria ; Vidal-Meireles, André ; Podmaniczki, Anna ; Szentmihályi, K. ; Rákhely, G. ; Zsigmond, Laura ; Kovács, László ; Tóth, Szilvia Z. / The mechanism of photosystem-II inactivation during sulphur deprivation-induced H2 production in Chlamydomonas reinhardtii. In: Plant Journal. 2018 ; Vol. 94, No. 3. pp. 548-561.
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T1 - The mechanism of photosystem-II inactivation during sulphur deprivation-induced H2 production in Chlamydomonas reinhardtii

AU - Nagy, Valéria

AU - Vidal-Meireles, André

AU - Podmaniczki, Anna

AU - Szentmihályi, K.

AU - Rákhely, G.

AU - Zsigmond, Laura

AU - Kovács, László

AU - Tóth, Szilvia Z.

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N2 - Sulphur limitation may restrain cell growth and viability. In the green alga Chlamydomonas reinhardtii, sulphur limitation may induce H2 production lasting for several days, which can be exploited as a renewable energy source. Sulphur limitation causes a large number of physiological changes, including the inactivation of photosystem II (PSII), leading to the establishment of hypoxia, essential for the increase in hydrogenase expression and activity. The inactivation of PSII has long been assumed to be caused by the sulphur-limited turnover of its reaction center protein PsbA. Here we reinvestigated this issue in detail and show that: (i) upon transferring Chlamydomonas cells to sulphur-free media, the cellular sulphur content decreases only by about 25%; (ii) as demonstrated by lincomycin treatments, PsbA has a significant turnover, and other photosynthetic subunits, namely RbcL and CP43, are degraded more rapidly than PsbA. On the other hand, sulphur limitation imposes oxidative stress early on, most probably involving the formation of singlet oxygen in PSII, which leads to an increase in the expression of GDP-L-galactose phosphorylase, playing an essential role in ascorbate biosynthesis. When accumulated to the millimolar concentration range, ascorbate may inactivate the oxygen-evolving complex and provide electrons to PSII, albeit at a low rate. In the absence of a functional donor side and sufficient electron transport, PSII reaction centers are inactivated and degraded. We therefore demonstrate that the inactivation of PSII is a complex and multistep process, which may serve to mitigate the damaging effects of sulphur limitation.

AB - Sulphur limitation may restrain cell growth and viability. In the green alga Chlamydomonas reinhardtii, sulphur limitation may induce H2 production lasting for several days, which can be exploited as a renewable energy source. Sulphur limitation causes a large number of physiological changes, including the inactivation of photosystem II (PSII), leading to the establishment of hypoxia, essential for the increase in hydrogenase expression and activity. The inactivation of PSII has long been assumed to be caused by the sulphur-limited turnover of its reaction center protein PsbA. Here we reinvestigated this issue in detail and show that: (i) upon transferring Chlamydomonas cells to sulphur-free media, the cellular sulphur content decreases only by about 25%; (ii) as demonstrated by lincomycin treatments, PsbA has a significant turnover, and other photosynthetic subunits, namely RbcL and CP43, are degraded more rapidly than PsbA. On the other hand, sulphur limitation imposes oxidative stress early on, most probably involving the formation of singlet oxygen in PSII, which leads to an increase in the expression of GDP-L-galactose phosphorylase, playing an essential role in ascorbate biosynthesis. When accumulated to the millimolar concentration range, ascorbate may inactivate the oxygen-evolving complex and provide electrons to PSII, albeit at a low rate. In the absence of a functional donor side and sufficient electron transport, PSII reaction centers are inactivated and degraded. We therefore demonstrate that the inactivation of PSII is a complex and multistep process, which may serve to mitigate the damaging effects of sulphur limitation.

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