Clues to the evolution of multicellularity from Tetrabaena


One development I’m excited to see among the Volvox community is an increased focus on Tetrabaena, one of the smallest and simplest of the colonial volvocine algae. The one species in this genus, Tetrabaena socialis, was classified as Gonium until 1994, when Hisayoshi Nozaki and Motomi Itoh revised it not only to a new genus but a new family, the Tetrabaenaceae.

Nozaki & Itoh 1994 Fig. 10

Figure 10 from Nozaki & Itoh 1994. Summary of the phylogenetic relationships within the colonial Volvocales inferred from cladistic analysis based on morphological data.

Their classification was based on morphological characters, but the backbone relationships, Tetrabaenaceae sister to Goniaceae + Volvocaceae, have subsequently been supported in several independent analyses using genetic data.

In 2013, very much to my surprise, Yoko Arakaki and colleagues showed that the (typically) four cells of Tetrabaena are connected by cytoplasmic bridges (this means that some of the ancestral character state reconstructions I did in grad school need to be revised). Their detailed analyses of Tetrabaena morphology and development are a valuable resource for comparative studies.

Now, in addition to the morphological data, we also have complete sequences for both organelle genomes (mitochondria and chloroplast) and for the nuclear genome. Jonathan Featherston and colleagues published the organelle genomes in 2016, and their new paper in Molecular Biology and Evolution describes the nuclear genome.

Studying Tetrabaena is critical for understanding the evolution of multicellularity. As one of the most distant relatives of Volvox within the colonial volvocine algae, any trait that Tetrabaena has in common with Volvox was probably present in their most recent common ancestor, in other words in the earliest multicellular species. For example, unlike the unicellular Chlamydomonas reinhardtiiTetrabaena and Volvox both have circular mitochondrial genomes:

Featherston et al. 2016 Fig. 5

Figure 5 from Featherston et al. 2016. Mitochondrial DNA conformations for various Reinhardtinia lineages.

Thus it seems likely that the earliest multicellular volvocine algae had circular mitochondrial genomes, and that the linear conformation in Pandorina evolved later.

Similarly, Featherston and colleagues have now used comparisons among nuclear genomes to infer changes related to the evolution of multicellularity.

Featherston et al. 2018 Fig. 1

Figure 1 from Featherston et al. 2018. Traits relevant to the current investigation and phylogenetic relationships of volvocine algae. The four species represented are those with sequenced nuclear genomes.

The Tetrabaena nuclear genome is similar in size and gene content to those of unicellular Chlamydomonas, colonial (undifferentiated) Gonium, and multicellular (differentiated) Volvox, around 120 megabases. This is not a huge surprise, since we already knew that the Gonium and Volvox  genomes were not much larger than that of Chlamydomonas, but it emphasizes once again that the evolution of multicellularity, at least in the volvocine algae, did not happen through large-scale changes in gene content.

Featherston Table 1

Table 1 from Featherston et al. 2018. Summary Statistics of sequenced volvocine genomes. *For this analysis Volvox carteri version 1 data were used. ** Including alternative splice variants.

That’s not to say, though, that there are no differences in gene content among the genomes. Of particular interest are genes and gene families that are present in GoniumVolvox, and Tetrabaena but absent from Chlamydomonas. If these were gained in the multicellular lineage, rather than lost in the Chlamydomonas lineage, they are good candidates for being related to multicellularity. Featherston and colleagues identified 131 gene families that originated, and 27 that expanded, in the multicellular lineage. Among these, genes related to developmental processes were overrepresented, including DNA repair, protein kinase activity, cell adhesion and extracellular functions.

One obvious place to look for changes related to the evolution of multicellularity is genes related to control of the cell cycle. For example, Erik Hanschen and colleagues have previously shown that alterations to one cell cycle gene, retinoblastoma, are sufficient to cause a multicellular phenotype in Chlamydomonas. Accordingly, Featherston and colleagues examined cell cycle genes in Tetrabaena. One such gene, cyclin D1, was already known to have undergone duplications in the lineage including Gonium and Volvox: each has four copies, compared to one in ChlamydomonasTetrabaena turns out to have three copies of cyclin D1, suggesting that this expansion occurred near the origin of multicellularity.

It’s very difficult to identify the genetic changes that actually underlie the evolution of multicellularity. VolvoxGonium, and Tetrabaena last shared a common ancestor about 200-250 million years ago, and there’s no doubt that all three lineages have evolved substantially since then. Sorting out which of the many, many differences are actually causative is a daunting task. Genome comparisons such as this one can give us clues to where to look. Right now, cell cycle genes are implicated by both plausible function and comparative analyses. Confirming causal roles of particular changes, though, will require functional analyses like that of retinoblastoma.

 

Stable links:

Arakaki, Y., Kawai-Toyooka, H., Hamamura, Y., Higashiyama, T., Noga, A., Hirono, M., Olson, B.J.S.C., and Nozaki, H. 2013. The simplest integrated multicellular organism unveiled. PLoS One, 8: e81641. doi: 10.1371/journal.pone.0081641

Featherston, J., Arakaki, Y., Hanschen, E.R., Ferris, P.J., Michod, R.E., Olson, B.J.S.C., Nozaki, H., and Durand, P.M. 2018. The 4-celled Tetrabaena socialis nuclear genome reveals the essential components for genetic control of cell number at the origin of multicellularity in the volvocine lineage. Mol. Biol. Evol. doi: 10.1093/molbev/msx332

Featherston, J., Arakaki, Y., Nozaki, H., Durand, P.M. and Smith, D.R. 2016. Inflated organelle genomes and a circular-mapping mtDNA probably existed at the origin of coloniality in volvocine green algae. Eur. J. Phycol., 51: 1–9. doi: 10.1080/09670262.2016.1198830

Nozaki, H. and Itoh, M. 1994. Phylogenetic relationships within the colonial Volvocales (Chlorophyta) inferred from cladistic analysis based on morphological data. J. Phycol., 30: 353–365. doi: 10.1111/j.0022-3646.1994.00353.x

EDIT: fixed doi link for Featherston et al. 2018 (2018-02-06)

Comments

  1. jazzlet says

    Thank you. There is no way I’d read all the relevant papers, but I am interested in this, as in so much else, which is why summaries (not the correct word, but near enough) like yours are so helpful.

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