Doses (W m-2) for photosynthetically active radiation (PAR, 400-700 nm) and ultraviolet radiation A (UVA, 315-400 nm) and B (UVB, 290-315 nm) are given for the PAR and PAR+UVR treatments during the experiments. Total irradiance intensity was ± 500 µmol photons m-2 s-1 in both treatments.
1. Introduction
The phytoplankton community of open oligotrophic oceans is dominated by prokaryotic
Phytoplankton irradiance exposure is strongly influenced by physical processes in the ocean [14]. During stratification, phytoplankton can be trapped in a shallow upper mixed layer, thereby enhancing exposure to photosynthetically active radiation (PAR, 400-700 nm) and ultraviolet radiation (UVR, 280-400 nm), or can experience limiting irradiance conditions at the deep chlorophyll maximum. In seasonally stratified regions, the period of stratification is interchanged with periods of deep convective mixing that can reach below the euphotic zone. This causes a strong reduction in the daily experienced irradiance, with occasional interruptions of excessive irradiance exposure. Consequently, phytoplankton irradiance exposure in open ocean ecosystems can vary by several orders of magnitude on a time scale ranging from seconds to days. Moreover, short wavelength solar radiation (UVB, 280-315 nm) can penetrate to significant depths in clear oligotrophic waters [15,16].
High irradiance exposure may have considerable effects on photosynthesis and viability in oceanic picophytoplankton species such as
Although it has previously been reported that temperature may have a positive effect on the survival of picophytoplankton under high irradiance conditions [30], no direct assessment of the temperature-dependency of photoregulation during high PAR and UVR exposure is available for this specific phytoplankton group. A recent study showed that both prokaryotic and eukaryotic picophytoplankton may be less susceptible to the negative effects of high irradiance intensities at elevated temperatures [31]. In the prokaryotic species
In the present study, a comparative analysis of the high irradiance sensitivity of oceanic picophytoplankton was performed to study the combined effect of elevated temperatures and irradiance levels near the surface of open oligotrophic oceans. To this end, two prokaryotic and two eukaryotic strains were acclimated to 16 °C, 20 °C, and 24 °C, after which they were exposed to a single high PAR dose, with and without UVR. The response to and the recovery after high irradiance exposure was assessed by analysis of PSII fluorescence and pigmentation in order to investigate immediate photoinhibition and photoprotective processes. The results are discussed in the context of differences between oceanic picophytoplankton species and are used to unravel the importance of photoinhibition in structuring the phytoplankton community in open oligotrophic oceans.
2. Method
2.1. Culture conditions
Cultures were obtained from the Roscoff Culture Collection (RCC) and the Provasoli-Guillard National Center for Marine Algae and Microbiota (NCMA). The strains were all isolated from oligotrophic regions and are representative for low light (LL) and high light (HL) adapted species in open ocean ecosystems.
2.2. Experimental design
Cultures of
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PAR | 172 | 157 |
UVA | 8.69 | 15.3 |
UVB | 0.05 | 1.79 |
2.3. Photosystem II chlorophyll fluorescence characteristics
PSII fluorescence analyses were performed on a WATER-PAM chlorophyll fluorometer (Waltz GmbH) equipped with a WATER-FT flow-through emitter-detector unit and analyzed using WinControl software (version 2.08, Waltz GmbH) according to [40] and references therein. Prior to exposure to PAR and PAR+UVR (t = 0), 5-15 ml culture samples were dark-adapted for 20 min at 16 °C, 20 °C, or 24 °C. For analysis, the measuring light was turned on and F0 was recorded as the minimal fluorescence. During a saturating light flash, Fm° was then recorded as the maximum fluorescence in the dark-adapted state. The maximum quantum yield of PSII (Fv/Fm) was calculated as (Fm° - F0) / Fm°. After exposure (t = 10-100), the quantum yield of PSII (ΦPSII) was determined by measuring Ft as the steady state fluorescence prior to the saturating light flash and Fm’ as the maximum fluorescence in the light. ΦPSII was calculated as (Fm’ – Ft) / Fm’. From the Fv/Fm measurements at t = 0 and the ΦPSII measurements at t = 10, total non photochemical quenching (NPQ) was calculated as (Fm° - Fm’) / Fm’. Relaxation analysis was performed to estimate the contribution of slowly and rapidly relaxing non photochemical quenching. Relaxation of NPQ on a time scale of minutes is associated with photoprotective processes such as state transitions, relaxation of the xanthophyll pigment cycle or other forms of thermal dissipation [35,40,41]. Processes that relax over a longer period of time (hours) are referred to as photoinhibition, i.e. damage to the reaction centers of PSII [40,42]. To estimate photoprotection and photoinhibition, the recorded Fm’ was corrected for baseline quenching by subtracting F0 and was log transformed for further analysis. Transformed Fm’ values of the final 60 min of the ФPSII recovery curve were extrapolated to calculate the value of Fm‘ that would had been attained if only slowly relaxing quenching was present in the light (Fmr). Slow relaxing non photochemical quenching (NPQS) was then calculated as (Fm° - Fmr) / Fmr and fast relaxing non photochemical quenching (NPQF) as (Fm° / Fm’) - (Fm° - Fmr). In addition, the contribution of UVR to the decrease in quantum yield of PSII during irradiance exposure was calculated as (ΦPSII,PAR - ΦPSII,PAR+UVR ) / ΦPSII,PAR * 100 [43].
2.4. Pigment composition
Samples (25-30 ml) for untreated (t = 0), PAR treated (t = 10, 20, 40), and PAR+UVR (t = 10, 20, 40) treated cultures were filtered onto 25 mm GF/F filters (Whatman), snap frozen in liquid nitrogen, and stored at -80 °C until further analysis. Pigments were quantified using High Performance Liquid Chromatography (HPLC) as described by [44]. In short, filters were freeze-dried for 48 h and pigments were extracted in 3 ml 90% acetone (v/v, 48 h, 4 °C). Detection of pigments was carried out using a HPLC (Waters 2695 separation module, 996 photodiode array detector) equipped with a Zorbax Eclipse XDB-C8 3.5 µm column (Agilent Technologies, Inc.). Peaks were identified by retention time and diode array spectroscopy. Pigments were quantified using standards (DHI LAB products) of chlorophyll
2.5. Statistical analysis
All measurements were performed for triplicate cultures (
3. Results
3.1. Non photochemical quenching and photosystem II recovery
The spectral composition of the irradiance treatment influenced non photochemical quenching and the recovery of the quantum yield of PSII (ΦPSII) considerably in the prokaryotic strains (Figure 1, Figure 2). In both
Comparison of NPQ between the different picophytoplankton strains demonstrated significantly lower total NPQ in the prokaryotic species
3.2. Inhibition of photosystem II by ultraviolet radiation
The inhibition of ΦPSII due to UVR was affected by temperature in
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16 °C | 66.4 ± 3.9a | n/a | 24.5 ± 18.1 | 100.0 ± 0.0 |
20 °C | 55.6 ± 4.9 | 97.9 ± 3.6 | 5.3 ± 5.4 | 97.3 ± 4.7 |
24 °C | 49.5 ± 4.8a | 97.3 ± 3.8 | 13.0 ± 5.5 | 77.0 ± 20.7 |
3.3. Photoprotective pigmentation
Temperature acclimation affected the initial photoprotective pigment pool in
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t = 0 | 0.647±0.060a | 0.499±0.004a | 0.431±0.007a | 0.647±0.060b | 0.499±0.004b | 0.431±0.007b |
t = 10 | 0.644 ± 0.081 | 0.488 ± 0.019 | 0.434 ± 0.017 | 0.649 ± 0.057 | 0.488 ± 0.013 | 0.426 ± 0.017 |
t = 20 | 0.657 ± 0.066 | 0.493 ± 0.006 | 0.426 ± 0.031 | 0.655 ± 0.071 | 0.494 ± 0.002 | 0.421 ± 0.031 |
t = 40 | 0.661 ± 0.067 | 0.498 ± 0.009 | 0.424 ± 0.014 | 0.663 ± 0.053 | 0.492 ± 0.013 | 0.437 ± 0.014 |
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t = 0 | n/a | 1.062 ± 0.034 | 1.025 ± 0.023 | n/a | 1.062 ± 0.034 | 1.025 ± 0.023 |
t = 10 | n/a | 1.206 ± 0.076 | 0.976 ± 0.009 | n/a | 1.198 ± 0.039 | 0.946 ± 0.039 |
t = 20 | n/a | 1.209 ± 0.093 | 0.966 ± 0.036 | n/a | 1.189 ± 0.059 | 0.936 ± 0.032 |
t = 40 | n/a | 1.226 ± 0.088 | 0.996 ± 0.041 | n/a | 1.192 ± 0.044 | 0.974 ± 0.039 |
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t = 0 | 0.079 ± 0.030 | 0.057 ± 0.024 | 0.061 ± 0.014 | 0.079 ± 0.030 | 0.057 ± 0.024 | 0.061 ± 0.014 |
t = 10 | 0.109 ± 0.017 | 0.062 ± 0.026 | 0.084 ± 0.032 | 0.058 ± 0.004 | 0.053 ± 0.012 | 0.060 ± 0.013 |
t = 20 | 0.091 ± 0.036 | 0.052 ± 0.020 | 0.060 ± 0.009 | 0.109 ± 0.003 | 0.082 ± 0.002 | 0.105 ± 0.008 |
t = 40 | 0.106 ± 0.005 | 0.078 ± 0.006 | 0.074 ± 0.031 | 0.109 ± 0.003 | 0.079 ± 0.014 | 0.077 ± 0.020 |
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t = 0 | 0.089 ± 0.008 | 0.089 ± 0.005 | 0.106 ± 0.012 | 0.089 ± 0.008 | 0.089 ± 0.005 | 0.106 ± 0.012 |
t = 10 | 0.096 ± 0.009 | 0.095 ± 0.002 | 0.106 ± 0.013 | 0.092 ± 0.010 | 0.094 ± 0.004 | 0.103 ± 0.014 |
t = 20 | 0.093 ± 0.005 | 0.096 ± 0.007 | 0.107 ± 0.014 | 0.080 ± 0.031 | 0.093 ± 0.005 | 0.105 ± 0.014 |
t = 40 | 0.093 ± 0.009 | 0.094 ± 0.006 | 0.109 ± 0.013 | 0.090 ± 0.008 | 0.092 ± 0.005 | 0.104 ± 0.012 |
3.4. De-epoxidation of the xanthophyll cycle
In both
The effect of the spectral composition of the irradiance treatment on the de-epoxidation of the xanthophyll pigment cycle was most evident in
When the dynamics of the xanthophyll pigment cycle of both species were compared, it was shown that
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16 °C | 0.036 ± 3.75 × 10-3 | 0.029 ± 2.76 × 10-4 |
20 °C | 0.043 ± 6.01 × 10-3 | 0.030 ± 4.53 × 10-3 |
24 °C | 0.038 ± 6.33 × 10-3 | 0.034 ± 5.39 × 10-3 |
PAR+UVR | ||
16 °C | 0.033 ± 4.79 × 10-3ab | 0.021 ± 6.38 × 10-4 |
20 °C | 0.047 ± 4.08 × 10-3a | 0.023 ± 5.33 × 10-3 |
24 °C | 0.045 ± 1.12 × 10-3b | 0.031 ± 7.34 × 10-3 |
4. Discussion
Climate change is expected to mediate a rise in seawater temperature by 1.5-4.5 °C over the next century [46]. This rise in seawater temperature will lead to changes in water column stratification in open oligotrophic oceans [47,48]. The subsequent modifications in mixed layer dynamics increase the exposure of phytoplankton to high levels of photosynthetic active radiation (PAR) and ultraviolet radiation (UVR). Because temperature and irradiance conditions play an important role in the success of specific oceanic phytoplankton species [4,49,50], it is important to understand how oceanic phytoplankton will respond to elevated temperatures and whether this will affect their (photo)physiological performance. The present study focused on the temperature-dependence of photoinhibition and photoregulating processes that are essential for survival during high (dynamic) irradiance conditions.
During short periods of high irradiance exposure, both the prokaryotic picophytoplankton strains
Temperature acclimation influenced photoinhibition and related processes during high irradiance exposure in
Both low and high light adapted
In the eukaryotic picophytoplankton species
This study showed that oceanic picophytoplankton were susceptible to photoinhibition during short periods of high irradiance. The genetically defined light adaptation of
Acknowledgments
Remote access to the Roscoff Culture Collection of strains RCC407 and RCC879 was facilitated by ASSEMBLE grant number 227799 (GK). This work was supported by the Netherlands Organization for Scientific Research (NWO), grant numbers 817.01.009 (GK) and 839.08.422 (WHP).References
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