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Juggling Lightning: How Chlorella ohadii handles extreme energy inputs without damage

Abstract

The green alga Chlorella ohadii was isolated from a desert biological soil crust, one of the harshest environments on Earth. When grown under optimal laboratory settings it shows the fastest growth rate ever reported for a photosynthetic eukaryote and a complete resistance to photodamage even under unnaturally high light intensities. Here we examined the energy distribution along the photosynthetic pathway under four light and carbon regimes. This was performed using various methodologies such as membrane inlet mass spectrometer with stable O2 isotopes, variable fluorescence, electrochromic shift and fluorescence assessment of NADPH level, as well as the use of specific inhibitors. We show that the preceding illumination and CO2 level during growth strongly affect the energy dissipation strategies employed by the cell. For example, plastid terminal oxidase (PTOX) plays an important role in energy dissipation, particularly in high light- and low-CO2-grown cells. Of particular note is the reliance on PSII cyclic electron flow as an effective and flexible dissipation mechanism in all conditions tested. The energy management observed here may be unique to C. ohadii, as it is the only known organism to cope with such conditions. However, the strategies demonstrated may provide an insight into the processes necessary for photosynthesis under high-light conditions.

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Acknowledgements

This research was supported by the Israel Science Foundation Grants to IY and AK and from the Israeli Ministry for Science and Technology to AK. We thank Dr. Haim Treves for many fruitful discussions and Dr. Judy Lieman-Hurwitz for technical assistance.

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Correspondence to Aaron Kaplan.

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Figure S1

: QA reoxidation achieved at 4 minutes of dark acclimation. C. ohadii cultures grown in LC/LL were placed in measurement apparatus and kept in dark for 15 minutes. Then they were exposed to HL (2000 μmol photons m-2 s-1 red light) for 4 minutes, followed by an additional 15 minute of dark. PAM saturating pulses were obtained 4 and 15 minutes into each dark phase to test for differences in QA reoxidation between these times. In both F0 (dark bars) and Fm (light bars) parameters, no significant difference is found between 4 and 14 minutes of the first dark phase (LL Dark 4, LL Dark 14), or between 4 and 15 minute of the second dark phase (HL Dark 4, HL Dark 15) (lowest P value was 0.067). Error bars are ± standard error, n=3 (TIF 181 kb)

Figure S2: ECS at prolonged light-off

. Normally, ΔΨ/ΔpH ratio is derived from the ration between the minimum level and the steady-state dark level. However, in this organism these two value are very close, probably indicating that this analysis is not suitable here. A similar image is derived in LC cultures (TIF 315 kb)

Table S1: Parameters derived from MIMS measurements

. Average values of ≥4 measurements in each condition. Standard error of the mean given in parentheses. Please note that these are raw results, results shown in Fig. 2 are normalized to dark respiration (TIF 278 kb)

Table S2: Parameters derived from OJIP analysis

of fast fluorescence rise kinetics. a) Average values of 4 measurements in each condition. b) Results of students T-test between relevant pairs of treatments, values below 0.05 emphasized in bold. Please note that for both LL conditions, nOG treatment has hardly any effect. (TIF 688 kb)

(TIF 418 kb)

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Kedem, I., Milrad, Y., Kaplan, A. et al. Juggling Lightning: How Chlorella ohadii handles extreme energy inputs without damage. Photosynth Res 147, 329–344 (2021). https://doi.org/10.1007/s11120-020-00809-9

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  • DOI: https://doi.org/10.1007/s11120-020-00809-9

Keywords

  • Energy dissipation
  • PTOX
  • Fluorescence
  • Oxygen evolution
  • High illumination
  • BSC