doi: 10.1371/journal.pone.0259138.
eCollection 2021.
The four-celled Volvocales green alga Tetrabaena socialis exhibits weak photobehavior and high-photoprotection ability
Asuka Tanno
1
2
, Ryutaro Tokutsu
3
4
, Yoko Arakaki
5
, Noriko Ueki
6
, Jun Minagawa
3
4
, Kenjiro Yoshimura
7
, Toru Hisabori
1
2
, Hisayoshi Nozaki
5
8
, Ken-Ichi Wakabayashi
1
2
Affiliations
- PMID: 34699573
- PMCID: PMC8547699
- DOI: 10.1371/journal.pone.0259138
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The four-celled Volvocales green alga Tetrabaena socialis exhibits weak photobehavior and high-photoprotection ability
Asuka Tanno et al.
PLoS One.
.
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Abstract
Photo-induced behavioral responses (photobehaviors) are crucial to the survival of motile phototrophic organisms in changing light conditions. Volvocine green algae are excellent model organisms for studying the regulatory mechanisms of photobehavior. We recently reported that unicellular Chlamydomonas reinhardtii and multicellular Volvox rousseletii exhibit similar photobehaviors, such as phototactic and photoshock responses, via different ciliary regulations. To clarify how the regulatory systems have changed during the evolution of multicellularity, we investigated the photobehaviors of four-celled Tetrabaena socialis. Surprisingly, unlike C. reinhardtii and V. rousseletii, T. socialis did not exhibit immediate photobehaviors after light illumination. Electrophysiological analysis revealed that the T. socialis eyespot does not function as a photoreceptor. Instead, T. socialis exhibited slow accumulation toward the light source in a photosynthesis-dependent manner. Our assessment of photosynthetic activities showed that T. socialis chloroplasts possess higher photoprotection abilities against strong light than C. reinhardtii. These data suggest that C. reinhardtii and T. socialis employ different strategies to avoid high-light stress (moving away rapidly and gaining photoprotection, respectively) despite their close phylogenetic relationship.
Conflict of interest statement
The authors have declared that no competing interests exist.
Figures
(A) Schematics of photobehaviors in C. reinhardtii (left) and Volvox rousseletii (right). In C. reinhardtii, two cilia beat in opposite directions to propel the cell forward. For phototaxis, the force generated by two cilia becomes unbalanced, allowing the cell to change its swimming direction. For the photoshock response, the cilia waveform changes from asymmetrical to symmetrical, allowing the cell to swim backward. In V. rousseletii, all cilia beat toward the posterior pole of the spheroid for forward swimming. For phototaxis, the beating direction of cilia in the anterior hemisphere on the light-source side reverses. The force generated by cilia between the light-source hemisphere and the opposite hemisphere becomes imbalanced, changing the swimming direction of the spheroid. For the photoshock response, the beating direction of almost all cilia in the anterior hemisphere reverses. The forces generated by the anterior hemisphere and posterior hemisphere are balanced, stopping the spheroid motion. (B) A differential-interference-contrast (top) and a bright-field (bottom) images and (C) schematics of T. socialis NIES-571 colonies. Four cells are arranged in a square. Each T. socialis cell resembles a C. reinhardtii cell, possessing two cilia and one eyespot (arrowheads in the bottom panel). Scale bars: 10 μm.
(A) Suspensions of wild-type C. reinhardtii cells and two T. socialis strains, NIES-571 and ISA2-2, were illuminated with green light (λ = 525 nm, 30 μmol photons m−2 s−1) from the right side for 15 min. (B) Polar histograms representing the percentage of cells/colonies moving in a particular direction relative to the green light illumination from the right (12 bins of 30°; n = 30 cells/colonies per strain) for 3 s following a 30-s illumination. (C) Phototactic indices (average of cosθ) calculated from (B). If all cells/colonies show positive or negative phototaxis, the value will be 1 or −1, respectively. If all cells/colonies swim in random directions, the value will be 0. Asterisk represents a significant difference from random swimming (p < 0.01; Student’s t-test). (D) Parallel indices (average of |cosθ|) calculated from (B). If all cells/colonies exhibit phototaxis (positive or negative) or swim in a completely random direction, the values would be 1 or 0.622, respectively. Asterisk represents a significant difference from random swimming (p < 0.01; Student’s t-test).
(A) Schematic image of the photoshock response in C. reinhardtii. After a flash illumination, C. reinhardtii cells change their ciliary waveform, swimming backward for a short period before returning to their normal swimming pattern. Trajectories for 6 s were traced before and after a flash illumination, and the angle (θ) between trajectories before and after the flash illumination for 1-s each was measured. (B) Representative 6-s swimming trajectories of wild-type C. reinhardtii cells and T. socialis NIES-571 and ISA2-2 colonies. Different colors indicate different cell trajectories. The yellow arrows indicate the flashlight illumination point. (C) The angles between trajectories before and after the flash illumination. Means ± S.D. (n = 10 cells/colonies) are shown. Different letters indicate significant differences (p < 0.01, one-way ANOVA and Tukey honest significance difference [HSD]).
Representative photoreceptive currents in wild-type C. reinhardtii cells (1.0 ×ばつ 107 cells/mL) and NIES-571 and ISA2-2 T. socialis colonies (2.5 ×ばつ 106 colonies/mL). The flashlight illumination is indicated with a red arrow and a broken line. The experimental setup is shown in S4 Fig.
(A) Suspensions of wild-type C. reinhardtii and T. socialis NIES-571 and ISA2-2 strains were illuminated with red light (λ = 640 nm, 30 μmol photons m−2 s−1) from the right side for 15 min. (B) Polar histograms representing the percentage of cells/colonies moving in a particular direction relative to the red light illumination (12 bins of 30°; n = 30 cells/colonies per strain) for 3 s following 30-s illumination. (C) Phototactic indices (average of cosθ) and (D) parallel indices (average of |cosθ|) calculated from (B). Values were not significantly different from random swimming (p > 0.1; Student’s t-test; see Fig 2C and 2D for details). (E, F) Time-lapse observation of T. socialis ISA2-2 photoaccumulation with (E) DCMU (or ethanol as a control) or (F) cycloheximide (CHX) (or DMSO as a control) treatments for 15 min in the dark. After the red light illumination, images of the Petri dishes were captured every 15 min.
Fv/Fm (A), NPQ (qE) (B), and φII (C) of wild-type C. reinhardtii and T. socialis NIES-571 and ISA2-2 strains were measured by a pulse-amplitude modulation chlorophyll fluorometer. Cells/colonies were illuminated under various light conditions (LL: white fluorescent light at 20 μmol photons m−2 s−1; UV fluorescent light at 20 μmol photons m−2 s−1; 470-, 530-, 660-nm LED light at 200 μmol photons m−2 s−1) for 4 h prior to the analysis. Means ± S.D. of three independent experiments are shown. In (A) and (B), different letters indicate significant differences (P < 0.01, one-way ANOVA and Tukey honest significance difference [HSD]). In (C), no significant difference between any two groups was found in each parameter (P > 0.01, one-way ANOVA and Tukey honest significance difference [HSD]).
Western blotting against whole-cell extracts (WCE) of wild-type C. reinhardtii and T. socialis NIES-571 and ISA2-2 strains using the antibody to detect C. reinhardtii LHCSR proteins (lower panel) or anti-ATPB (the beta subunit of ATP synthase) (upper panel) as a loading control. WCE were prepared after the same light/temperature treatment as Fig 6. LHCSR3-P: phosphorylated LHCSR3.
References
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- Demmig-Adams B, Adams WW, 3rd. Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Bioi 1992. p. 599–626.
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