Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri

Abstract

The multicellular green alga Volvox carteri and its morphologically diverse close relatives (the volvocine algae) are well suited for the investigation of the evolution of multicellularity and development. We sequenced the 138-mega-base pair genome of V. carteri and compared its approximately 14,500 predicted proteins to those of its unicellular relative Chlamydomonas reinhardtii. Despite fundamental differences in organismal complexity and life history, the two species have similar protein-coding potentials and few species-specific protein-coding gene predictions. Volvox is enriched in volvocine-algal-specific proteins, including those associated with an expanded and highly compartmentalized extracellular matrix. Our analysis shows that increases in organismal complexity can be associated with modifications of lineage-specific proteins rather than large-scale invention of protein-coding capacity.

Fig. 1

Volvox and Chlamydomonas. (A) Adult Volvox is composed of ~2000 Chlamydomonas-like somatic cells (s) and ~16 large germline gonidia (g) (scale bar, 200 μm) (fig. S1B). (B) Chlamydomonas cell showing apical flagella (f), chloroplast (c), and eyespot (e) (scale bar, 10 μm). The microscopy used is described in (5).

Fig. 2

Comparisons of protein domains and families. (A) Total number of Pfam domains in the multicellular (green) and unicellular (blue) species: Ostreococcus tauri (ota); Micromonas pusilla (mpu); Chlamydomonas reinhardtii (cre); Volvox carteri (vca); Physcomitrella patens (ppa); Arabidopsis thaliana (ath); Thalassiosira pseudonana (tps); Phaeodactylum tricornutum (ptr); Monosiga brevicollis (mbr); Nematostella vectensis (nve); and Homo sapiens (hsa). (B) The numbers of protein families from Volvox, Chlamydomonas, and other species (5) are shown in a Venn diagram. The numbers of Volvox and Chlamydomonas members per protein family are plotted for all families (C) and for the volvocine algae–specific subset (D). In these density plots, the position of each square represents the number of family members in Volvox (x axis) and Chlamydomonas (y axis), with coloring to indicate the total number of families plotted at each position. The Pfam domains for outlier families are abbreviated as follows: a, ankyrin repeat; c, cysteine protease; g, gametolysin; h, histone; L, LRR.

Fig. 3

Diversification of key protein families with known or predicted roles in Volvox development. Unrooted maximum likelihood trees (5) are shown for pherophorins (A) and cyclins (B). Protein sequences are from Volvox (Vc, green) and Chlamydomonas (Cr, blue). Incomplete gene models were not included; Volvox-specific clades with poorly resolved branches are collapsed into triangles; bootstrap support ≥50% is indicated on branches. Red asterisks indicate pherophorins whose mRNA levels are up-regulated by a sex inducer (16).