Photosynthetic acclimation to chilling in the widespread chilling-tolerant cyanobacterium Nostoc commune

DOI: https://doi.org/10.21203/rs.3.rs-1965680/v1

Abstract

Nostoc commune (N. commune) is a widespread chilling-tolerant cyanobacterium, whereas its photosynthetic acclimation to chilling remains largely unknown. Here, its photosynthetic responses to chilling were investigated. During 24 h exposure to chilling temperature (4 ºC), this cyanobacterium exhibited photosystem II (PSII) photoinhibition, as evident by the significant decrease in both the PSII maximum quantum yield Fv/Fm and the PSII core protein D1 abundance. However its photosystem I (PSI) maintained stable, both the maximum photo-oxidizable P700 and the PSI core protein PsaA/B abundance remained largely unchanged after chilling. Chilling activated the non-photochemical quenching to maintain energy balance of intersystem electron transport in N. commune, its quantum yield of regulated energy dissipation in PSII (Y(NPQ)) significantly rose by 41%, so that its PSII excitation pressure (1-qP) remained stable. Furthermore, the significant stimulation of cyclic electron flow (CEF) was observed upon the transfer to chilling and subsequent recovery in N. commune, and its photodamage in the presence of chloramphenicol was similar to that in the presence of methyl viologen, suggesting that CEF contributed to the PSII repair under chilling stress. The present data provide novel insight into photosynthetic acclimation to chilling, which benefit the survival of N. commune in cold habitats or during over-wintering periods and could be used as a reference for the design of robust photosynthetic cell factory.

Introduction

Cyanobacteria are the ancient photosynthetic oxygenic prokaryotic organisms and also known to be the ancestor of plant chloroplast. They are the important primary producer in biosphere (Potts 2000; Flombaum et al. 2013), whereas some key environmental factors limit their global distribution and productivity, such as chilling temperature. Low temperature is a mechanic stress, can increase the rigidify of lipid membrane and slow enzymatic reactions, thereby resulting in photosystem II (PSII) damage or photosystem I (PSI) photoinhibition corresponding by the production of excess reactive oxygen species (Gombos et al. 1992; Tasaka et al. 1996; Sonoike 1998, 2011). Cyanobacteria have evolved diverse cold adaptability to withstand chilling stress, such as the induction of fatty acid desaturase to increase the fluidity of membrane (Wada et al. 1990; Sakamoto et al. 1997; Kis et al. 1998), the synthesis of specific regulatory proteins stabilizing photosynthetic complex (Zak and Pakrasi 2000; Li et al. 2012), the accumulation of RNA binding proteins, the evolution of multi-functional genes, the integration of light-temperature signals and so on (Murata et al. 2010; Tan et al. 2011; Sinetova and Los 2016; Oren et al. 2019; Xu et al. 2021; Gao et al. 2021). Whereas if considering the diversity of cyanobacteria, chilling-resistance mechanisms are far from been fully understood.

Nostoc commune (N. commune) is a well-known desiccation-tolerant terrestrial cyanobacterium, widely distributed from arid or semi-arid lands to extremely cold Antarctica, and also acts as an excellent species for studying chilling-tolerance (Lipman, 1941; Potts 2000; Novis et al. 2007; Sand-Jensen and Jespersen 2012). It is a typical colonial cyanobacterium with a gelatinous polysaccharide sheath, and its thick extracellular polysaccharides played crucial roles in its desiccation and freezing tolerance (Tamaru et al. 2005). Since its productivity is largely determined by photosynthesis, much attention was paid to its photosynthetic responses to multiple and rapidly changing stresses. N. commune cells can actively deactivate photosynthetic systems on sensing water loss to avoid photodamage in the forthcoming desiccation (Hirai et al. 2004; Fukuda et al. 2008), and then quickly recover its photosynthetic activity during rewetting (Satoh et al. 2002; Chen et al. 2011). Its photosynthetic apparatus can also respond flexibly to daily diurnal light fluctuation by the stimulation of non-photochemical quenching at noon (Chen et al. 2011). However, little document reported the strategy of its photosynthetic apparatus to resist chilling stress.

Therefore, in the present study, the photosynthetic activity of N. commune under chilling stress and subsequent recovery were examined in order to explore its potential chilling-tolerance mechanism, which could deepen our understanding of survival strategies of this widespread cyanobacterium in cold habitats or during over-wintering periods.

Materials And Methods

Materials and chilling treatments

Colonies of N. commune were freshly collected on the campus of Hubei Normal University, Huangshi, China (115.07o E, 30.23o N). Unless otherwise stated, the fresh colonies were dried for more than 1 week at 25 ºC under dim light (5-10 μmol photons m-2 s-1). Samples were rewetted in BG110 under 50 μmol photons m-2 s-1 at 25 ºC for 12 h and then subjected to chilling stress and subsequent recovery. 

The N. commune colonies immersed in BG110 medium were placed in a cool room at 4 ºC for 24 h and then allowed to recover under a temperature of 25 ºC for another 24 h, and the light intensity maintained 50 μmol photons m-2 s-1 all the time.

Chlorophyll fluorescence measurements

The Chl fluorescence measurement were determined using a Dual-PAM-100 (Heinz Walz, USA). The Fv/Fm values were determined after dark adaptation for 15 min. All the PSII photosynthetic measurements in the light were determined under a photon flux density (PFD) of 50 μmol m-2 s-1 after 5 min light adaptation. The fluorescence parameters were calculated as follows: Fv/Fm=(Fm-Fo)/Fm, Fv'/Fm'=(Fm'-Fo')/Fm', qP=(Fm'-Fs)/(Fm'-Fo'), Y(II)=(Fm'-Fs)/Fm', Y(NO)=Fs/Fm, Y(NPQ)=Fs/Fm'-Fs/Fm, rETR=Y(II)×0.84×0.5×PFD (Genty et al. 1989; Campbell et al. 1998; Klughammer and Schreiber 2008); where Fo is the minimum fluorescence in the dark-adapted state, Fs is steady-state fluorescence in light, and Fo' is the light-adapted state constant fluorescence yield evaluated following a far-red illumination, Fm and Fm' are maximum fluorescence values upon illumination by a pulse (700 ms) of saturating light (4000 µmol photons m-2 s-1) in the dark-adapted state and light-adapted state respectively according to Campbell et al. (1998). The fragmented N. commune samples with the same thickness and physiological state were used to compare control and treatment in terms of relative values (their Fo and Fv/Fm values were 0.1 ± 0.02 and 0.35 ± 0.05 respectively).

P700 redox kinetics assay

The P700 redox state was measured by Dual PAM-100 with a dual wavelength (830/875 nm) unit, following the method of Klughammer and Schreiber (1994). The maximum photo-oxidizable P700 (Pm) was determined after a saturation pulse, was given after preillumination with far-red light. At a defined optical property, the amplitude of Pm depends on the maximum amount of photo-oxidizable P700, which is a parameter for representing the quantity of efficient PSI complex. 

The P700+ dark-reduction kinetics was used to determine the cyclic electron flow (CEF), 20 μM 3-(3,4-dichlorophenyl)- 1,1-dimethylurea DCMU was added to the samples prior to measurements (Dai et al. 2013). The P700 was oxidized by far-red light with a maximum at 720 nm from LED lamp for 10 s, and the subsequent re-reduction of P700+ in the dark was monitored. The P700+ reduction rate constants (s−1) were determined from the calculated electron transfer rate.

Western blot assay

Western blot assay was performed according to the methods described previously (Chen et al. 2019). The N. commune samples were pulverized in liquid N2 and suspended in ice-cold isolation buffer containing 50 mM Mes-NaOH (pH 6.5), 25% glycerol, 10 mM MgCl2, 5 mM CaCl2, and 1 mM phenylmethylsulfonyl fluoride. Cells were ruptured with a ultrasonic cell disruptor (Scientz-IID, Ningbo, China) in an ice bath for 10 min at 30% of its peak amplitude. Cell debris and unbroken cells were removed by centrifugation at 4000 g and 4 ºC for 10 min. Total thylakoid membrane proteins and cytosolic soluble proteins were obtained by centrifugation at 40,000 g and 4 ºC for 60 min. The resulting thylakoids were resuspended in isolation buffer and used for Western blot analysis. SDS-PAGE and Western blotting were performed using standard methods. Briefly, equal amounts of proteins (10 μg) were loaded, separated by 12% SDS-PAGE, transferred to PVDF membrane (sigma, USA), detected with D1- and PsaA/B-specific primary antibodies, and visualized with goat anti-rabbit alkaline phosphatase antibody with nitroblue tetrazolium and 5-bromo-4-chloro-3-indolylphosphate (Amresco) as the substrates. The target proteins were detected and visualized by chemiluminescence (bio-rad ChemiDoc XRS, BioRad, USA).

Statistical analysis

Statistical calculations are performed using SPSS. The significant differences between these two groups were compared by t-test. One-way analysis of variance (ANOVA) and Tukey honestly significant difference (HSD) test were conducted to test the statistical significance of the differences between means of various treatments.

Results

PSII and PSI activities under chilling stress in N. commune

Responses of PSII and PSI activities to chilling stress are shown in Fig.1A. During the exposure to chilling temperature (4 ºC), the PSII maximun quantum yield Fv/Fm showed a slight rise within 4 h, then gradually decreased, and significantly reduced by 35% at 24 h compared with the initial values (Turkey HSD, P < 0.05), but 

the maximum photo-oxidizable P700 Pm, as an indicator of the quantity of efficient PSI complex, did not decrease and maintained stable (Fig. 1). During the following recovery at 25 ºC, Fv/Fm exhibited a rapid increase, up to the levels of the initial values, Pm also remained stable (Fig. 1A＆B). 

To explore the underlying mechanism, we further carried out western blot assay for photosystem core proteins of N. commune. In agreement with the physiological results, after exposed to chilling stress (4 ºC) for 24 h, the abundance of PSII core protein D1 in N. commune obviously decreased but the abundance of PSI core protein PsaA remained stable, and during the following recovery experiments (25 ºC) for 24 h, the D1 abundance recovered approximately to the initial levels whereas the PsaA/B abundance also remained stable. These results showed that PSII was sensitive to chilling stress whereas PSI was chilling-tolerant in N. commune.

The PSII excitation pressure maintained stable under chilling stress in N. commune

Effects of chilling stress on the chlorophyll fluorescence parameters Fv'/Fm',1-qP and rETR(II) in N. commune were indicated in Fig. 2. During the 24 h exposure to chilling stress, both the light-adapted maximum quantum yield of PSII Fv'/Fm' and the relative electron transport rate around PSII rETR(II) continuously decreased, up to 65% of the original values, and returned to the initial values during the following recovery at 25 ºC. However, the parameter 1-qP, as an indicator of the excitation pressure in PSII or the proportion of closed PSII reaction centers, maintained stable during the chilling treatment and the subsequent recovery at 25 ºC.

non-photochemical quenching increased under chilling stress in N. commune

Effects of chilling stress on light energy distribution in PSII were illustrated in Fig. 3. Since the effective quantum yield of PSII Y(II) is the product of the light-adapted maximum quantum yield of PSII Fv'/Fm' multiplied by the photochemical quenching coefficient qP, when exposed to chilling stress for 24 h, qP maintained stable, so the decrease in Y(II) by 35% was only due to the loss of Fv'/Fm' which was also reduced by 35% (Fig. 2＆3). During chilling stress at 4 ºC, the quantum yield of non-regulated energy dissipation in PSII (Y(NO), reflecting the inability to protect itself against damage by excess light energy, gradually increased by 16% at 24 h, the quantum yield of regulated energy dissipation in PSII Y(NPQ) was stimulated, significantly rose by 41% at 24 h compared to the initial values. During the recovery, Y(II) rapidly increased, Y(NO) and Y(NPQ) fell down quickly, reaching the original levels (Fig. 3).

Cyclic electron flow was stimulated upon the transfer to chilling stress and subsequent recovery in N. commune

Responses of cyclic electron flow (CEF) in N. commune to chilling stress at 4 ºC and subsequent recovery at 25 ºC were assayed in Fig. 4. When the samples was transferred to chilling stress at 4 ºC, the cyclic electron flow was significantly stimulated, its cyclic electron transfer rate of 2.03±0.39 s−1 at 0.5 h rose by 46% compared to the initial values (1.39±0.10 s−1), then cyclic electron flow gradually decreased, reaching 50% of the original values at 24 h. Once the chilling-treated samples were transferred to the optimum temperature condition at 25 ºC, its cyclic electron flow was sharply stimulated again, its cyclic electron transfer rate of 1.40±0.39 s−1 at 0.5 h reached nearly two-fold that of chilling-treated cells (0.7±0.10 s−1), then gradually increased within 4 h, and then maintain relative stable levels, specifically its cyclic electron transfer rate reached 126-137% of the initial values (Fig. 3 A-B).

A similar reduction of PSII activity was induced by methyl viologen and chloramphenicol under chilling stress in N. commune

We further examined the decrease of PSII activity in the presence of methyl viologen (MV) or chloramphenicol (CMP) during chilling stress as shown in Fig. 5. CMP is the protein translation inhibitor and can interrupt PSII repair cycle, and MV accepts electrons from the PSI acceptor side and can block the cyclic electron flow around PSI (Yu et al. 1993). After 24 h exposure to chilling stress at 4 ºC, the Fv/Fm value decreased to 69% of the initial values, whereas Fv/Fm further decreased to 48% of the initial values in the presence of chloramphenicol, implying the PSII repair contributed to 21% of the PSII activity during chilling stress. When the samples were exposed to MV during chilling stress, its PSII activity showed a similar reduction in Fv/Fm values (21%), suggesting that cyclic electron flow may contribute to the PSII repair under chilling stress in N. commune.

Discussion

PSII photoinhibition and PSI stability under chilling stress 

PSII photoinhibition usually occurs under strong light due to photodamage of PSII exceed the repair of PSII (Andersson and Aro 2001), while other environmental stresses such as chilling stress could not influence photodamage of PSII but suppress the repair of PSII, which also lead to photoinhibiton (Allakhverdiev and Murata 2004). The PSII repair process is largely limited by de novo-synthesis of the PSII core protein D1, and chilling stress has been reported to be able to suppress the de novo-synthesis of the D1 protein and the processing of the precursor to the mature D1 protein (Aro et al. 1993; Kanervo et al. 1997; Li et al. 2018). This is supported by our results that both the Fv/Fm values and the D1 abundance decreased under chilling stress in N. commune (Fig. 1). On the other hand, PSII photoinhibition can exert protective effects on photosynthetic apparatus, especially PSI. The partly destroy of PSII reaction centre caused the decrease of relative linear electron transport rate (Fig. 2C). It means less electrons flow into PSI, which was beneficial for the formation of more oxidation state of PSI so as to be able to protect PSI from photodamage (Tjus et al. 1998; Huang et al. 2010). So, PSII photoinhibition could be a protective acclimation response to resist chilling stress in N. commune.

PSI photoinhibition is another damage target of chilling stress on photosynthetic organisms (Terashima et al. 1994; Sonoike et al. 1995; Tjus et al. 1998; Zak et al. 2000; Huang et al. 2010). Upon PSI photoinhibition, the reaction center subunits of PSI were degraded like PSII photoinhibition, whereas the recovery of damaged PSI is much slower than that of PSII, so PSI photoinhibition could be more dangerous than PSII inhibition, and even could be a lethal event for photosynthetic organisms (Sonoike 2011; Shimakawa and Miyake 2019). For example, in chilling-sensitive cyanobacterium Synechocystis sp. PCC 6803, low-temperature conditions resulted in the decrease of its PSI activity and increased degradation of its PSI reaction center proteins PsaA/B, and this cyanobacterium loses its ability to reinitiate growth during chilling stress (Zak et al. 2000; Yin et al. 2007). Unlike Synechocystis sp. PCC 6803, N. commune is a chilling-tolerant species, which can grow during winter or even in extremely cold Antarctica (Potts 2000; Novis et al. 2007), its PSI activity and its core proteins PsaA/B remained largely unchanged under chilling stress (Fig. 1). Since PSI stability was subjected to the oxidized P700 state (Sonoike 2011; Shimakawa and Miyake 2019), there are at least two protective mechanisms involved in PSI stability under chilling stress in N commune, including stimulation of cyclic electron transport which pull electrons from PSI acceptor side, and the PSII photoinhibiton which caused less electron flow into PSI (Fig 2＆4; Sonoike 2011; Shimakawa and Miyake 2019). Therefore, PSI stability could be a key strategy for the survival of N. commune during overwinter or in cold habitats. 

Tuning of energy distribution in PSII under chilling stress 

A balance between energy supply and energy consumption is required in all the photosynthetic organisms, but the energy balance could be affected by environment stress, such as chilling stress (Huner et al. 1996; Ivanov et al 2008). Since carbon metabolism is more susceptible to temperatures down-shift in the light than the photochemical reactions, chilling temperatures could usually result in the energy imbalance, which can be sensed through PS II excitation pressure1-qP (Huner et al. 1996; Huner et al. 1998). The increase of the excitation pressure was observed in the cyanobacterium Anabaena sp. Strain PCC 7120 in response to temperature down-shift in the light (Ehira et al. 2005). By contrast, in N. commune, the PS II excitation pressure was insensitive to chilling stress under low light (50 μmol m-2 s-1) (Fig. 2). The capacity to keep PS II reaction centers open under chilling stress in N. commune could be attributed to the activation of some photoprotective mechanisms, as indicated by the increase of non-photochemical quenching Y(NPQ) (Fig. 2). The underlying NPQ-related mechanisms may be state transition or orange carotenoid protein mediated photoprotection, which have been reported to dynamically regulate photosystem II excitation in response to rapid environment changes (Wilson et al. 2006; Derks et al. 2015; Kirilovsky 2007, 2014). For this chilling-tolerant cyanobacterium N. commune, fine tuning of PSII energy distribution should be another strategy to resist chilling stress.

Cyclic electron flow around PSI contributed to the repair of PSII under chilling stress

Cyclic electron flow around PSI play an essential role in the protection of PSII inhibition in response to various environmental changes and stresses (Yamori and Shikanai, 2016). Specifically, CEF can generate the proton motive force across the thylakoid membrane and promote the production of ATP, which could drive the repair of PSII and help to alleviate photoinhibition of PSII (Murata and Nishiyama 2018). In higher plants, such as Arabidopsis and some tropical tree species, cyclic electron transport was significantly stimulated by the temporal chilling under low light (Cruz et al. 2005; Huang et al. 2011), which was also observed in the cyanobacterium N. commune colonies (Fig. 4). After 24 h exposure to chilling stress, the photodamage in the presence of the PSII repair inhibitor chloramphenicol was similar to that in the presence of the cyclic electron flow inhibitor MV, indicating that the cyclic electron flow contributed to the PSII repair under chilling stress in N. commune (Fig. 5). Stimulation of cyclic electron flow during the subsequent recovery after chilling-induced PSII photoinhibition was observed in the mature leaves of Dalbergia odorifera (Huang et al. 2010). Similarly, in N. commune, upon the transfer from chilling stress to optimal temperature conditions, CEF was strongly stimulated again, accompanied by the rapid recovery of photodamaged PSII (Fig1, 4). These results indicated that the CEF was an important drive force for the PSII repair under chilling stress and subsequent recovery in both higher plants and this chilling-tolerant cyanobacterium N. commune.

 In conclusion, PSII photoinhibition and PSI stability as well as the stimulation of NPQ and CEF could be beneficial for the robust photosynthesis under chilling stress. If considered from the perspective of synthetic biology, N. commune was a typical representative for chilling-tolerant cyanobacteria, its photosynthetic acclimation characteristics under chilling stress could be used as a reference for the design of photosynthetic cell factory.

Declarations

Acknowledgements  

This work was supported by the Natural Science Foundation of China (No. 32100310), the Scientific Research Project of Hubei Education Department (No. D20202501), the Open Foundation of Hubei Key Laboratory of Edible Wild Plants Conservation & Utilization (EWPL202003 and EWPL201905).

Compliance with ethical standards

Conflict of interest 

The authors declare that they have no conflict of interest.

Research involving with human and animal participants 

This article does not contain any studies with human or animal subjects performed by any of the authors.

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