The simplest integrated multicellular organism unveiled

PLoS One. 2013 Dec 11;8(12):e81641. doi: 10.1371/journal.pone.0081641. eCollection 2013.


Volvocine green algae represent the "evolutionary time machine" model lineage for studying multicellularity, because they encompass the whole range of evolutionary transition of multicellularity from unicellular Chlamydomonas to >500-celled Volvox. Multicellular volvocalean species including Gonium pectorale and Volvox carteri generally have several common morphological features to survive as integrated multicellular organisms such as "rotational asymmetry of cells" so that the cells become components of the individual and "cytoplasmic bridges between protoplasts in developing embryos" to maintain the species-specific form of the multicellular individual before secretion of new extracellular matrix (ECM). However, these morphological features have not been studied in the four-celled colonial volvocine species Tetrabaena socialis that is positioned in the most basal lineage within the colonial or multicellular volvocine greens. Here we established synchronous cultures of T. socialis and carried out immunofluorescence microscopic and ultrastructural observations to elucidate these two morphological attributes. Based on immunofluorescence microscopy, four cells of the mature T. socialis colony were identical in morphology but had rotational asymmetry in arrangement of microtubular rootlets and separation of basal bodies like G. pectorale and V. carteri. Ultrastructural observations clearly confirmed the presence of cytoplasmic bridges between protoplasts in developing embryos of T. socialis even after the formation of new flagella in each daughter protoplast within the parental ECM. Therefore, these two morphological attributes might have evolved in the common four-celled ancestor of the colonial volvocine algae and contributed to the further increase in cell number and complexity of the multicellular individuals of this model lineage. T. socialis is one of the simplest integrated multicellular organisms in which four identical cells constitute the individual.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biological Evolution*
  • Chlorophyta / classification
  • Chlorophyta / physiology
  • Chlorophyta / ultrastructure*
  • Cytoplasm / physiology
  • Cytoplasm / ultrastructure
  • Extracellular Matrix / physiology
  • Extracellular Matrix / ultrastructure
  • Flagella / physiology
  • Flagella / ultrastructure
  • Phylogeny*
  • Protoplasts / physiology
  • Protoplasts / ultrastructure
  • Species Specificity

Grants and funding

This work was supported by Grants-in-Aid for Scientific Research on JSPS Fellows (number 25-9234 to YA), Challenging Exploratory Research (number 24657045 to HN) and Scientific Research (A) (number 24247042 to HN) from MEXT/JSPS KAKENHI ( The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.