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Plant function and evolutionary biology
RESEARCH ARTICLE

New insights into the effect of NdhO levels on cyanobacterial cell death triggered by high temperature

Jiaohong Zhao A , Yuanyuan Jiang A , Yuhao Tian A , Jun Mao A , Lanzhen Wei A B and Weimin Ma https://orcid.org/0000-0003-4964-415X A B
+ Author Affiliations
- Author Affiliations

A Shanghai Key laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, 100 Guilin Road, Shanghai 200234, China.

B Corresponding author. Email: wma@shnu.edu.cn; weilz@shnu.edu.cn

Functional Plant Biology - https://doi.org/10.1071/FP21097
Submitted: 1 April 2021  Accepted: 5 August 2021   Published online: 25 August 2021

Abstract

NdhO, a regulatory oxygenic photosynthesis-specific subunit, is close to the ferredoxin-binding site of cyanobacterial NDH-1, and its levels are negatively associated with the rates of cyclic electron transfer around PSI mediated by NDH-1 (NDH-CET). However, the effect of NdhO levels on cyanobacterial cell death triggered by high temperature remains elusive. Here, our results uncovered a synergistic effect of NdhO levels on the cell death and reactive oxygen species (ROS) accumulation when cyanobacterial cells grown at 30°C for 1 day were transferred to 45°C for 2 days. Such synergistic effect was found to be closely associated with the activities of NDH-CET and CO2 assimilation during high temperature. Collectively, we propose that the effect of NdhO levels on the cyanobacterial cell bleaching and cell death triggered by high temperature is a result of influencing production of ROS by NDH-CET, which is considered to be vital to balance the ATP/NADPH ratio and improve the Calvin-Benson cycle.

Keywords: NdhO, high temperature, cyclic electron transfer, CO2 fixation, reactive oxygen species, cell death, Synechocystis.


References

Allen MM (1968) Simple conditions for growth of unicellular blue-green algae on plates. Journal of Phycology 4, 1–4.
Simple conditions for growth of unicellular blue-green algae on plates.Crossref | GoogleScholarGoogle Scholar | 27067764PubMed |

Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 16654194PubMed |

Bassham JA (1964) Kinetic studies of the photosynthetic carbon reduction cycle. Annual Review of Plant Physiology 15, 101–120.
Kinetic studies of the photosynthetic carbon reduction cycle.Crossref | GoogleScholarGoogle Scholar |

Battchikova N, Wei L, Du L, Bersanini L, Aro EM, Ma W (2011) Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH:plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803. The Journal of Biological Chemistry 286, 36992–37001.
Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH:plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 21880717PubMed |

Beckmann K, Messinger J, Badger MR, Wydrzynski T, Hillier W (2009) On-line mass spectrometry: membrane inlet sampling. Photosynthesis Research 102, 511–522.
On-line mass spectrometry: membrane inlet sampling.Crossref | GoogleScholarGoogle Scholar | 19653116PubMed |

Bernát G, Appel J, Ogawa T, Rögner M (2011) Distinct roles of multiple NDH-1 complexes in the cyanobacterial electron transport network as revealed by kinetic analysis of P700+ reduction in various Ndh-deficient mutants of Synechocystis sp. strain PCC6803. Journal of Bacteriology 193, 292–295.
Distinct roles of multiple NDH-1 complexes in the cyanobacterial electron transport network as revealed by kinetic analysis of P700+ reduction in various Ndh-deficient mutants of Synechocystis sp. strain PCC6803.Crossref | GoogleScholarGoogle Scholar | 21036997PubMed |

Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science 4, 273
Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops.Crossref | GoogleScholarGoogle Scholar | 23914193PubMed |

Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036.
Archean molecular fossils and the early rise of eukaryotes.Crossref | GoogleScholarGoogle Scholar | 10446042PubMed |

Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. The EMBO Journal 17, 868–876.
Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes.Crossref | GoogleScholarGoogle Scholar | 9463365PubMed |

Catling DC, Glein CR, Zahnle KJ, McKay CP (2005) Why O2 is required by complex life on habitable planets and the concept of planetary “oxygenation time”. Astrobiology 5, 415–438.
Why O2 is required by complex life on habitable planets and the concept of planetary “oxygenation time”.Crossref | GoogleScholarGoogle Scholar | 15941384PubMed |

Červený J, Sinetova MA, Zavřel T, Los DA (2015) Mechanisms of high temperature resistance of Synechocystis sp. PCC 6803: an impact of histidine kinase 34. Life (Basel, Switzerland) 5, 676–699.
Mechanisms of high temperature resistance of Synechocystis sp. PCC 6803: an impact of histidine kinase 34.Crossref | GoogleScholarGoogle Scholar |

Dai H, Zhang L, Zhang J, Mi H, Ogawa T, Ma W (2013) Identification of a cyanobacterial CRR6 protein, Slr1097, required for efficient assembly of NDH-1 complexes in Synechocystis sp. PCC 6803. The Plant Journal 75, 858–866.
Identification of a cyanobacterial CRR6 protein, Slr1097, required for efficient assembly of NDH-1 complexes in Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 23725563PubMed |

Deng Y, Ye J, Mi H (2003) Effects of low CO2 on NAD(P)H dehydrogenase, a mediator of cyclic electron transport around photosystem I in the cyanobacterium Synechocystis PCC6803. Plant & Cell Physiology 44, 534–540.
Effects of low CO2 on NAD(P)H dehydrogenase, a mediator of cyclic electron transport around photosystem I in the cyanobacterium Synechocystis PCC6803.Crossref | GoogleScholarGoogle Scholar |

Gao F, Zhao J, Wang X, Qin S, Wei L, Ma W (2016a) NdhV is a subunit of NADPH dehydrogenase essential for cyclic electron transport in Synechocystis sp. strain PCC 6803. Plant Physiology 170, 752–760.
NdhV is a subunit of NADPH dehydrogenase essential for cyclic electron transport in Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar | 26644505PubMed |

Gao F, Zhao J, Chen L, Battchikova N, Ran Z, Aro EM, Ogawa T, Ma W (2016b) The NDH-1L-PSI supercomplex is important for efficient cyclic electron transport in cyanobacteria. Plant Physiology 172, 1451–1464.
The NDH-1L-PSI supercomplex is important for efficient cyclic electron transport in cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 27621424PubMed |

Ifuku K, Endo T, Shikanai T, Aro EM (2011) Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant & Cell Physiology 52, 1560–1568.
Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits.Crossref | GoogleScholarGoogle Scholar |

Inoue N, Taira Y, Emi T, Yamane Y, Kashino Y, Koike H, Satoh K (2001) Acclimation to the growth temperature and the high-temperature effects on photosystem II and plasma membranes in a mesophilic cyanobacterium, Synechocystis sp. PCC6803. Plant & Cell Physiology 42, 1140–1148.
Acclimation to the growth temperature and the high-temperature effects on photosystem II and plasma membranes in a mesophilic cyanobacterium, Synechocystis sp. PCC6803.Crossref | GoogleScholarGoogle Scholar |

Keston AS, Brandt R (1965) The fluorometric analysis of ultramicro quantities of hydrogen peroxide. Analytical Biochemistry 11, 1–5.
The fluorometric analysis of ultramicro quantities of hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar | 14328641PubMed |

Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiology 155, 70–78.
The importance of energy balance in improving photosynthetic productivity.Crossref | GoogleScholarGoogle Scholar | 21078862PubMed |

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 5432063PubMed |

Laughlin TG, Bayne AN, Trempe JF, Savage DF, Davies KM (2019) Structure of the complex I-like molecule NDH of oxygenic photosynthesis. Nature 566, 411–414.
Structure of the complex I-like molecule NDH of oxygenic photosynthesis.Crossref | GoogleScholarGoogle Scholar | 30742075PubMed |

Li Q, Liang Z, Ge F, Xu Y, Yang L, Zeng H (2014) Alleviating CTAC and Flu combined pollution damage in Chlorella vulgaris by exogenous nitric oxide. Chemosphere 96, 39–45.
Alleviating CTAC and Flu combined pollution damage in Chlorella vulgaris by exogenous nitric oxide.Crossref | GoogleScholarGoogle Scholar | 24001670PubMed |

Ma W, Mi H (2005) Expression and activity of type 1 NAD(P)H dehydrogenase at different growth phases of the cyanobacterium, Synechocystis PCC 6803. Physiologia Plantarum 125, 135–140.
Expression and activity of type 1 NAD(P)H dehydrogenase at different growth phases of the cyanobacterium, Synechocystis PCC 6803.Crossref | GoogleScholarGoogle Scholar |

Ma W, Ogawa T (2015) Oxygenic photosynthesis-specific subunits of cyanobacterial NADPH dehydrogenases. IUBMB Life 67, 3–8.
Oxygenic photosynthesis-specific subunits of cyanobacterial NADPH dehydrogenases.Crossref | GoogleScholarGoogle Scholar | 25564967PubMed |

Ma W, Wei L, Wang Q (2008) The response of electron transport mediated by active NADPH dehydrogenase complexes to heat stress in the cyanobacterium Synechocystis 6803. Science in China. Series C, Life Sciences 51, 1082–1087.
The response of electron transport mediated by active NADPH dehydrogenase complexes to heat stress in the cyanobacterium Synechocystis 6803.Crossref | GoogleScholarGoogle Scholar | 19093081PubMed |

Markelova AG, Vladimirova MG, Kuptsova ES (2000) A comparison of cytochemical methods for the rapid evaluation of microalgal viability. Russian Journal of Plant Physiology 47, 815–819.
A comparison of cytochemical methods for the rapid evaluation of microalgal viability.Crossref | GoogleScholarGoogle Scholar |

Mi H, Endo T, Ogawa T, Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant & Cell Physiology 36, 661–668.
Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar |

Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429, 579–582.
Cyclic electron flow around photosystem I is essential for photosynthesis.Crossref | GoogleScholarGoogle Scholar | 15175756PubMed |

Murata N, Nishiyama Y (2018) ATP is a driving force in the repair of photosystem II during photoinhibition. Plant, Cell & Environment 41, 285–299.
ATP is a driving force in the repair of photosystem II during photoinhibition.Crossref | GoogleScholarGoogle Scholar |

Ogawa T (1991) A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proceedings of the National Academy of Sciences of the United States of America 88, 4275–4279.
A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803.Crossref | GoogleScholarGoogle Scholar | 1903537PubMed |

Ormerod MG (1990) Analysis of DNA. In Ormerod MG(Eds), Flow cytometry. A practical approach, Oxford University Press, Oxford, pp. 69–87.

Pan X, Cao D, Xie F, Xu F, Su X, Mi H, Zhang X, Li M (2020) Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase. Nature Communications 11, 610
Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase.Crossref | GoogleScholarGoogle Scholar | 32001694PubMed |

Peltier G, Cournac L (2002) Chlororespiration. Annual Review of Plant Biology 53, 523–550.
Chlororespiration.Crossref | GoogleScholarGoogle Scholar | 12227339PubMed |

Peltier G, Aro EM, Shikanai T (2016) NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annual Review of Plant Biology 67, 55–80.
NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis.Crossref | GoogleScholarGoogle Scholar | 26735062PubMed |

Peng L, Yamamoto H, Shikanai T (2011) Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. Biochimica et Biophysica Acta 1807, 945–953.
Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex.Crossref | GoogleScholarGoogle Scholar | 21029720PubMed |

Ran Z, Zhao J, Tong G, Gao F, Wei L, Ma W (2019) Ssl3451 is important for accumulation of NDH-1 assembly intermediates in the cytoplasm of Synechocystis sp. strain PCC 6803. Plant & Cell Physiology 60, 1374–1385.
Ssl3451 is important for accumulation of NDH-1 assembly intermediates in the cytoplasm of Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar |

Rastogi RP, Singh SP, Häder DP, Sinha RP (2010) Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2′,7′-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937. Biochemical and Biophysical Research Communications 397, 603–607.
Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2′,7′-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937.Crossref | GoogleScholarGoogle Scholar | 20570649PubMed |

Raymond J, Segrè D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311, 1764–1767.
The effect of oxygen on biochemical networks and the evolution of complex life.Crossref | GoogleScholarGoogle Scholar | 16556842PubMed |

Sacksteder CA, Kanazawa A, Jacoby ME, Kramer DM (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged. Proceedings of the National Academy of Sciences of the United States of America 97, 14283–14288.
The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged.Crossref | GoogleScholarGoogle Scholar | 11121034PubMed |

Schuller JM, Birrell JA, Tanaka H, Konuma T, Wulfhorst H, Cox N, Schuller SK, Thiemann J, Lubitz W, Sétif P, Ikegami T, Engel BD, Kurisu G, Nowaczyk MM (2019) Structural adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer. Science 363, 257–260.
Structural adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer.Crossref | GoogleScholarGoogle Scholar | 30573545PubMed |

Schuller JM, Saura P, Thiemann J, Schuller SK, Gamiz-Hernandez AP, Kurisu G, Nowaczyk MM, Kaila VRI (2020) Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I. Nature Communications 11, 494
Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I.Crossref | GoogleScholarGoogle Scholar | 31980611PubMed |

Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annual Review of Plant Biology 58, 199–217.
Cyclic electron transport around photosystem I: genetic approaches.Crossref | GoogleScholarGoogle Scholar | 17201689PubMed |

Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proceedings of the National Academy of Sciences of the United States of America 95, 9705–9709.
Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I.Crossref | GoogleScholarGoogle Scholar | 9689145PubMed |

Ueno M, Sae-Tang P, Kusama Y, Hihara Y, Matsuda M, Hasunuma T, Nishiyama Y (2016) Moderate heat stress stimulates repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803. Plant & Cell Physiology 57, 2417–2426.
Moderate heat stress stimulates repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar |

Wang HL, Postier BL, Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. The Journal of Biological Chemistry 279, 5739–5751.
Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator.Crossref | GoogleScholarGoogle Scholar | 14612435PubMed |

Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye JY, Mi H (2006) Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiology 141, 465–474.
Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress.Crossref | GoogleScholarGoogle Scholar | 16428601PubMed |

Wang X, Gao F, Zhang J, Zhao J, Ogawa T, Ma W (2016) A cytoplasmic protein Ssl3829 is important for NDH-1 hydrophilic arm assembly in Synechocystis sp. strain PCC 6803. Plant Physiology 171, 864–877.
A cytoplasmic protein Ssl3829 is important for NDH-1 hydrophilic arm assembly in Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar | 27208268PubMed |

Zhang J, Gao F, Zhao J, Ogawa T, Wang Q, Ma W (2014) NdhP is an exclusive subunit of large complex of NADPH dehydrogenase essential to stabilize the complex in Synechocystis sp. strain PCC 6803. The Journal of Biological Chemistry 289, 18770–18781.
NdhP is an exclusive subunit of large complex of NADPH dehydrogenase essential to stabilize the complex in Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar | 24847053PubMed |

Zhang H, Zhang S, Peng Y, Li Y, Chen Z, Xu H, Yu Z, Zheng W, Zheng T (2015) Effects of marine actinomycete on the removal of a toxicity alga Phaeocystis globose in eutrophication waters. Frontiers in Microbiology 6, 474
Effects of marine actinomycete on the removal of a toxicity alga Phaeocystis globose in eutrophication waters.Crossref | GoogleScholarGoogle Scholar | 26042109PubMed |

Zhang C, Shuai J, Ran Z, Zhao J, Wu Z, Liao R, Wu J, Ma W, Lei M (2020) Structural insights into NDH-1 mediated cyclic electron transfer. Nature Communications 11, 888
Structural insights into NDH-1 mediated cyclic electron transfer.Crossref | GoogleScholarGoogle Scholar | 32060291PubMed |

Zhao J, Gao F, Qiu Z, Wang Q, Ma W (2014a) Deletion of an electron donor-binding subunit of the NDH-1 complex, NdhS, results in a heat-sensitive growth phenotype in Synechocystis sp. PCC 6803. Chinese Science Bulletin 59, 4484–4490.
Deletion of an electron donor-binding subunit of the NDH-1 complex, NdhS, results in a heat-sensitive growth phenotype in Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar |

Zhao J, Gao F, Zhang J, Ogawa T, Ma W (2014b) NdhO, a subunit of NADPH dehydrogenase, destabilizes medium size complex of the enzyme in Synechocystis sp. strain PCC 6803. The Journal of Biological Chemistry 289, 26669–26676.
NdhO, a subunit of NADPH dehydrogenase, destabilizes medium size complex of the enzyme in Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar | 25107904PubMed |

Zhao J, Rong W, Gao F, Ogawa T, Ma W (2015) Subunit Q is required to stabilize the large complex of NADPH dehydrogenase in Synechocystis sp. strain PCC 6803. Plant Physiology 168, 443–451.
Subunit Q is required to stabilize the large complex of NADPH dehydrogenase in Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar | 25873552PubMed |

Zhao J, Gao F, Fan DY, Chow WS, Ma W (2018) NDH-1 is important for photosystem I function of Synechocystis sp. strain PCC 6803 under environmental stress conditions. Frontiers in Plant Science 8, 2183
NDH-1 is important for photosystem I function of Synechocystis sp. strain PCC 6803 under environmental stress conditions.Crossref | GoogleScholarGoogle Scholar | 29387069PubMed |

Zhou S, Shao Y, Gao N, Li L, Deng J, Zhu M, Zhu S (2014) Effect of chlorine dioxide on cyanobacterial cell integrity, toxin degradation and disinfection by-product formation. The Science of the Total Environment 482–483, 208–213.
Effect of chlorine dioxide on cyanobacterial cell integrity, toxin degradation and disinfection by-product formation.Crossref | GoogleScholarGoogle Scholar | 24651056PubMed |