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Cited by 59Light effects on plantsProtist diversity and phylogenyMicro and Nano Robotics

How 5000 independent rowers coordinate their strokes in order to row into the sunlight: phototaxis in the multicellular green alga Volvox

Open access
Ueki, Noriko, Matsunaga, Shigeru, Inouye, Isao, Hallmann, Armin·2010·BMC Biology
DOI 10.1186/1741-7007-8-103PMC PMC2920248
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Abstract

BACKGROUND: The evolution of multicellular motile organisms from unicellular ancestors required the utilization of previously evolved tactic behavior in a multicellular context. Volvocine green algae are uniquely suited for studying tactic responses during the transition to multicellularity because they range in complexity from unicellular to multicellular genera. Phototactic responses are essential for these flagellates because they need to orientate themselves to receive sufficient light for photosynthesis, but how does a multicellular organism accomplish phototaxis without any known direct communication among cells? Several aspects of the photoresponse have previously been analyzed in volvocine algae, particularly in the unicellular alga Chlamydomonas. RESULTS: In this study, the phototactic behavior in the spheroidal, multicellular volvocine green alga Volvox rousseletii (Volvocales, Chlorophyta) was analyzed. In response to light stimuli, not only did the flagella waveform and beat frequency change, but the effective stroke was reversed. Moreover, there was a photoresponse gradient from the anterior to the posterior pole of the spheroid, and only cells of the anterior hemisphere showed an effective response. The latter caused a reverse of the fluid flow that was confined to the anterior hemisphere. The responsiveness to light is consistent with an anterior-to-posterior size gradient of eyespots. At the posterior pole, the eyespots are tiny or absent, making the corresponding cells appear to be blind. Pulsed light stimulation of an immobilized spheroid was used to simulate the light fluctuation experienced by a rotating spheroid during phototaxis. The results demonstrated that in free-swimming spheroids, only those cells of the anterior hemisphere that face toward the light source reverse the beating direction in the presence of illumination; this behavior results in phototactic turning. Moreover, positive phototaxis is facilitated by gravitational forces. Under our conditions, V. rousseletii spheroids showed no negative phototaxis. CONCLUSIONS: On the basis of our results, we developed a mechanistic model that predicts the phototactic behavior in V. rousseletii. The model involves photoresponses, periodically changing light conditions, morphological polarity, rotation of the spheroid, two modes of flagellar beating, and the impact of gravity. Our results also indicate how recently evolved multicellular organisms adapted the phototactic capabilities of their unicellular ancestors to multicellular life.

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  • The single-celled Chlamydomonas, the multicellular Volvox or the larvae of the annelid Platynereis all orient very quickly and precisely along the light vector, usually within a few helical turns.

    “The single-celled Chlamydomonas [26], the multicellular Volvox [35] or the larvae of the annelid Platynereis [8] all orient very quickly and precisely along the light vector, usually within a few helical turns.”

    From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [35]

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1 of the 111 references couldn’t be matched to a known paper.

Research works printed but not linked: 2

  1. Rüffer U Nultsch W Flagellar coordination in Chlamydomonas cells held on micropipettes Cell Motil Cytoskeleton 1998 41 297 307 9858155
  2. Yoshimura K Shingyoji C Takahashi K Conversion of beating mode in Chlamydomonas flagella induced by electric stimulation Cell Motil Cytoskeleton 1997 36 236 245 9067619

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Authors
Ueki, N., Matsunaga, S., Inouye, I., & Hallmann, A.
Affiliations
  • Bielefeld University (DE)
  • University of Tsukuba (JP)
Corresponding author
Hallmann, Armin
ORCID
Venue
BMC Biology
Publisher
Springer Science and Business Media LLC
Published
2010-07-27
Volume
8
Issue
1
Pages
103-103
ISSN
1741-7007 (ISSN-L)
DOI
10.1186/1741-7007-8-103
PMC
PMC2920248
OpenAlex
W2088959313
Cited by
59
References
111
Citations by year
2026: 4 · 2025: 4 · 2024: 4 · 2023: 8 · 2022: 1 · 2021: 5 · 2020: 5 · 2019: 2 · 2018: 3 · 2017: 2 · 2016: 5 · 2015: 1 · 2014: 5 · 2013: 2 · 2012: 3
FWCI
3.85
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion, other-oa)
  • PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion, public-domain)
Funders
  • Toyobo Biotechnology Foundation
  • Japan Society for the Promotion of Science
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
  • Physical Sciences › Physics and Astronomy › Condensed Matter Physics › Micro and Nano Robotics
Keywords
phototaxis, evolution of multicellularity, eyespots, flagellar beating, stroke reversal, anterior-posterior polarity, cell-to-cell communication
MeSH terms
Flagella, Light, Movement, Photic Stimulation, Phylogeny, Volvox

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