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Arrest of cytoplasmic streaming induces algal proliferation in green paramecia.

Takahashi T, Shirai Y, Kosaka T, Hosoya H - PLoS ONE (2007)

Bottom Line: Here, we found that cytoplasmic streaming was arrested in dividing green paramecia and the endosymbiotic algae proliferated only during the arrest of cytoplasmic streaming.Interestingly, arrest of cytoplasmic streaming with pressure or a microtubule drug also induced proliferation of endosymbiotic algae independently of host cell cycle.Furthermore, confocal microscopic observation revealed that a division septum was formed in the constricted area of a dividing paramecium, producing arrest of cytoplasmic streaming.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Biological Science, Hiroshima University, Higashi-Hiroshima, Hiroshima, Japan.

ABSTRACT
A green ciliate Paramecium bursaria, bearing several hundreds of endosymbiotic algae, demonstrates rotational microtubule-based cytoplasmic streaming, in which cytoplasmic granules and endosymbiotic algae flow in a constant direction. However, its physiological significance is still unknown. We investigated physiological roles of cytoplasmic streaming in P. bursaria through host cell cycle using video-microscopy. Here, we found that cytoplasmic streaming was arrested in dividing green paramecia and the endosymbiotic algae proliferated only during the arrest of cytoplasmic streaming. Interestingly, arrest of cytoplasmic streaming with pressure or a microtubule drug also induced proliferation of endosymbiotic algae independently of host cell cycle. Thus, cytoplasmic streaming may control the algal proliferation in P. bursaria. Furthermore, confocal microscopic observation revealed that a division septum was formed in the constricted area of a dividing paramecium, producing arrest of cytoplasmic streaming. This is a first report to suggest that cytoplasmic streaming controls proliferation of eukaryotic cells.

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(A) Cytoplasmic streaming in P. bursaria.Upper (10-second intervals) and Lower panels (30-second intervals); P. bursaria having carmine particles (arrowheads) in the cytoplasm at interphase (stage 1) and dividing phase (stage 2), respectively. Scale bar, 20 µm. (B) A relation between cytoplasmic streaming and the number of endosymbionts. A bar graph shows the number of endosymbionts (±S.D.) at each phase of host cell cycle (stage 1–4). The endosymbionts were classified into a unicellular cell (purple), 2 (green) and 4 autospores (white). A table shows whether cytoplasmic streaming occurs or not, and the total number of endosymbionts. * and ** mean statistical differences with Student's t-test, *P<0.005 and **P<0.001.
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pone-0001352-g001: (A) Cytoplasmic streaming in P. bursaria.Upper (10-second intervals) and Lower panels (30-second intervals); P. bursaria having carmine particles (arrowheads) in the cytoplasm at interphase (stage 1) and dividing phase (stage 2), respectively. Scale bar, 20 µm. (B) A relation between cytoplasmic streaming and the number of endosymbionts. A bar graph shows the number of endosymbionts (±S.D.) at each phase of host cell cycle (stage 1–4). The endosymbionts were classified into a unicellular cell (purple), 2 (green) and 4 autospores (white). A table shows whether cytoplasmic streaming occurs or not, and the total number of endosymbionts. * and ** mean statistical differences with Student's t-test, *P<0.005 and **P<0.001.

Mentions: Cytoplasmic streaming in Paramecium bursaria (green and algae-free) was observed in vivo. P. bursaria at interphase demonstrates dynamically rotational microtubule-based cytoplasmic streaming [3], in which some cytoplasmic granules and endosymbionts flow in a constant direction (Fig. 1A, upper; Movie S1). Interestingly, we found that dividing host cells almost arrested cytoplasmic streaming (Fig. 1A, lower; Movie S1). The arrest of cytoplasmic streaming continued until about 30 min after host cell division (data not shown). When a paramecium initiated cytokinesis (Stage 2, Fig. 1B), endosymbionts also initiated cytokinesis, producing 2–4 autospores. In Stage 3, the total number of endosymbionts increased twice as much as that at interphase (Stage 1). When a paramecium completed cell division and cytoplasmic streaming recovered (Stage 4), the number of endosymbionts returned almost the same as that at interphase.


Arrest of cytoplasmic streaming induces algal proliferation in green paramecia.

Takahashi T, Shirai Y, Kosaka T, Hosoya H - PLoS ONE (2007)

(A) Cytoplasmic streaming in P. bursaria.Upper (10-second intervals) and Lower panels (30-second intervals); P. bursaria having carmine particles (arrowheads) in the cytoplasm at interphase (stage 1) and dividing phase (stage 2), respectively. Scale bar, 20 µm. (B) A relation between cytoplasmic streaming and the number of endosymbionts. A bar graph shows the number of endosymbionts (±S.D.) at each phase of host cell cycle (stage 1–4). The endosymbionts were classified into a unicellular cell (purple), 2 (green) and 4 autospores (white). A table shows whether cytoplasmic streaming occurs or not, and the total number of endosymbionts. * and ** mean statistical differences with Student's t-test, *P<0.005 and **P<0.001.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2131778&req=5

pone-0001352-g001: (A) Cytoplasmic streaming in P. bursaria.Upper (10-second intervals) and Lower panels (30-second intervals); P. bursaria having carmine particles (arrowheads) in the cytoplasm at interphase (stage 1) and dividing phase (stage 2), respectively. Scale bar, 20 µm. (B) A relation between cytoplasmic streaming and the number of endosymbionts. A bar graph shows the number of endosymbionts (±S.D.) at each phase of host cell cycle (stage 1–4). The endosymbionts were classified into a unicellular cell (purple), 2 (green) and 4 autospores (white). A table shows whether cytoplasmic streaming occurs or not, and the total number of endosymbionts. * and ** mean statistical differences with Student's t-test, *P<0.005 and **P<0.001.
Mentions: Cytoplasmic streaming in Paramecium bursaria (green and algae-free) was observed in vivo. P. bursaria at interphase demonstrates dynamically rotational microtubule-based cytoplasmic streaming [3], in which some cytoplasmic granules and endosymbionts flow in a constant direction (Fig. 1A, upper; Movie S1). Interestingly, we found that dividing host cells almost arrested cytoplasmic streaming (Fig. 1A, lower; Movie S1). The arrest of cytoplasmic streaming continued until about 30 min after host cell division (data not shown). When a paramecium initiated cytokinesis (Stage 2, Fig. 1B), endosymbionts also initiated cytokinesis, producing 2–4 autospores. In Stage 3, the total number of endosymbionts increased twice as much as that at interphase (Stage 1). When a paramecium completed cell division and cytoplasmic streaming recovered (Stage 4), the number of endosymbionts returned almost the same as that at interphase.

Bottom Line: Here, we found that cytoplasmic streaming was arrested in dividing green paramecia and the endosymbiotic algae proliferated only during the arrest of cytoplasmic streaming.Interestingly, arrest of cytoplasmic streaming with pressure or a microtubule drug also induced proliferation of endosymbiotic algae independently of host cell cycle.Furthermore, confocal microscopic observation revealed that a division septum was formed in the constricted area of a dividing paramecium, producing arrest of cytoplasmic streaming.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Biological Science, Hiroshima University, Higashi-Hiroshima, Hiroshima, Japan.

ABSTRACT
A green ciliate Paramecium bursaria, bearing several hundreds of endosymbiotic algae, demonstrates rotational microtubule-based cytoplasmic streaming, in which cytoplasmic granules and endosymbiotic algae flow in a constant direction. However, its physiological significance is still unknown. We investigated physiological roles of cytoplasmic streaming in P. bursaria through host cell cycle using video-microscopy. Here, we found that cytoplasmic streaming was arrested in dividing green paramecia and the endosymbiotic algae proliferated only during the arrest of cytoplasmic streaming. Interestingly, arrest of cytoplasmic streaming with pressure or a microtubule drug also induced proliferation of endosymbiotic algae independently of host cell cycle. Thus, cytoplasmic streaming may control the algal proliferation in P. bursaria. Furthermore, confocal microscopic observation revealed that a division septum was formed in the constricted area of a dividing paramecium, producing arrest of cytoplasmic streaming. This is a first report to suggest that cytoplasmic streaming controls proliferation of eukaryotic cells.

Show MeSH