The four-celled Volvocales green alga Tetrabaena socialis exhibits weak photobehavior and high-photoprotection ability

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.

Multicellularity and increasing Reynolds number impact on the evolutionary shift in photo-induced ciliary response in Volvocales

“…(1) The eyespot’s function as a photoreceptor, which appears to be lost in Pattern 2 species, became functional again. (2) Symmetrical waveforms were observed in response to light in Pattern 1 species and independent of light in Pattern 2 species [ Tetrabaena (18) and Vitreochlamys (this study)]. Conversely, symmetrical waveforms in species with Patterns 3 and 4 have not been observed, suggesting that these organisms have lost the trait of cilia beating in symmetrical waveforms.…”

“…No obvious light response has been reported for Tetrabaena (18). Here, three closely related species, unicellular Vitreochlamys , 8–16 cells Gonium, and 16–32 cells Astrephomene , did not obviously respond to the light stimulus (Fig.…”

“…The Re for each individual was calculated according to the following formula: diameter (µm) × velocity (µm/s) / kinematic viscosity coefficient for water 10 6 (µm 2 /s). (18). Species are denoted by the first letter of genus name and the first 1-3 letters of specific name.…”

“…In Chlamydomonas reinhardtii, the ciliary waveform converts from asymmetric to symmetric in response to light, causing temporal backward swimming (14)(15)(16)(17). In Tetrabaena socialis, which has a flat shape with four cells, cilia do not change their motility even after light stimulation, and no photobehavior is observed (18). Several Volvox species temporarily reduce the ciliary beating frequency or stop ciliary movement in response to light (19).…”

Swimming ability and flagellar motility of sperm packets of the volvocine green algaPleodorina starrii

“…Volvocine green algae, ranging from unicellular Chlamydomonas [8] and four-celled Tetrabaena [9] to thousands-celled Volvox [10,11], are planktonic swimmers with flagella that have been used as model organisms to investigate the dynamics of multiple flagella. They have two equal-length flagella in one cell, and flagella in the entire colony have been shown to move collectively in many cases.…”