Embryogenesis in Gonium and Tetrabaena

Back when I was a cocky grad student, I wrote a paper that was, in some ways, critical of the work of one of the biggest names in my field. David Kirk, who passed away last year, was among the most important figures in establishing Volvox as a model system for development, genetics, and evolution, among other things. He had published a paper that I thought was unnecessarily progressivist, and I said so in terms that, in retrospect, could have been more diplomatic. In response, Dr. Kirk, whom I had never met, sent me a very thoughtful email thanking me for pointing out some of the problems and politely disagreeing on some other points. Its tone was kind and respectful when annoyed and argumentative would have probably been justified.

In that email, he offered a bet, the stakes of which were to be a beer, that one of the things I had suggested would turn out to be wrong. The issue had to do with inversion, a process that the (mostly) spheroidal algae in the family Volvocaceae undergo during development. I have written about inversion many times on Fierce Roller; in a nutshell, these algae start their lives inside-out, with their flagella on the inside, and invert to get the flagella on the outside, where they can be used for swimming. Their relatives in the genus Gonium also undergo a process of partial inversion, changing from cup-shaped (with the flagella on the concave side) to flat or slightly cup-shaped in the other direction. Dr. Kirk had interpreted Gonium‘s partial inversion as a probable intermediate step that led to the complete inversion characteristic of the Volvocaceae. My reconstructions suggested that incomplete inversion in Gonium had evolved separately from complete inversion in the Volvocaceae, and Dr. Kirk bet me that this would turn out to be wrong.

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Why carteri?

It’s embarrassing, really. I’ve been studying Volvox and its relatives for 15 years now, and until today I couldn’t have told you who the most famous member of the group, Volvox carteri, was named for. Sure, I know Colemanosphaera is named for Annette Coleman, Volvox ferrisii for Patrick Ferris, and Volvox kirkiorum (“of the Kirks”) for David and Marilyn Kirk, but that’s because they were all named after I started studying Volvox.

But do you recall…the most famous algae of all?

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Who said we were playing?

A coauthor posted our new paper to reddit, where the comment thread blew right the hell up. I and the poster answered some of the comments and questions, but there were far too many to even read all of them. It also got some traction on Twitter and on Facebook:


There’s also a short article by Fiona MacDonald at ScienceAlert, which was reposted word-for-word without attribution (stolen, in other words) by True Viral News. Every ecosystem has its parasites. Inevitably, there was some pushback along with the wows, some thoughtful and some, well…
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New Volvocalean phylogeny

My postdoc makes fun of me for having a lousy memory. Not long ago she showed me a paper about microRNAs, and I said I hadn’t read it. She responded, “Yes you have; you blogged about it!” The other day we were discussing the use of antibiotics to prevent bacterial contamination, and I said I thought I might have done that at one time. She told me I had, it was ampicillin, and the concentration.

I’ve been blogging for nearly four years now, and I’ve published well over 400 posts. So I’ve learned that before I sink a bunch of time into writing a new blog post, it’s worth a quick search to make sure I’m not going to repeat myself. When a new paper from Takashi Nakada and colleagues popped up in my Google Scholar alerts, I didn’t immediately realize that I had already written about it. That post was mainly about a new analysis by Thomas Pröschold and colleagues, with the Nakada trees serving as a point of comparison. The new paper is worth its own post, though.

A group of researchers from Keio University have published a new analysis of evolutionary relationships among green algae in the order Volvocales. Takashi Nakada, Yudai Tsuchida, and Masaru Tomita inferred relationships using one nuclear gene and five chloroplast genes.

Nakada et al. 2019 graphical abstract

Graphical abstract from Nakada et al. 2019 showing Chlamydomonas pila as sister to the multicellular volvocine algae (Tetrabaena, Gonium, Volvox).

Previously, I focused on the monophyly of the multicellular volvocine algae, i.e. the Tetrabaenaceae, Goniaceae, and Volvocaceae (TGV). The multigene analysis shown above supports monophyly, although the support values for the critical node are not shown (meaning that the Bayesian posterior probability is <0.90 and the bootstrap proportions are <50%). Similarly, the new phylogeny doesn’t do much to resolve the backbone relationships within the Volvocaceae. There are differences from previous analyses that would be important if true, specifically in the positions of Volvox globator (the sole representative of Volvox section Volvox) and of Yamagishiella (which appears as part of an isogamous clade rather than sister to the anisogamous/oogamous Eudorina/Pleodorina/(most) Volvox clade). Neither of these differences is well supported, though, which is typical; most published phylogenies provide poor support for these relationships.

Nakada et al. 2019 Fig. 2

Figure 2 from Nakada et al. 2019. Bayesian phylogenetic tree of core-Reinhardtinia based on combined 18S-atpB-psaA-psaB-psbC-rbcL gene sequences. Corresponding posterior probabilities (≥0.90; left) and bootstrap proportions (≥50%) from maximum likelihood (middle) and neighbor-joining (right) analyses are shown next to the branches. Branch lengths and scale bars represent the expected number of nucleotide substitutions per site. Metaclades (MC; 1.00 posterior probabilities).

The main point of the new paper, though, is the close relationship between the multicellular volvocine algae and Chlamydomonas pila. The critical node for this relationship is is supported by a high Bayesian posterior probability (1.00) but crappy bootstrap values (55% for maximum likelihood and <50% for neighbor joining). The authors did do some analyses with fewer taxa to test this relationship, and those trees did have better support, but they also changed other relationships.

Correctly identifying the closest unicellular relative of the multicellular volvocine algae is critical for reconstructing the first steps in the transition to multicellular life. This is far from the first time that other species of Chlamydomonas and some of Vitreochlamys have been implicated. I’m not aware of any previous phylogeny that includes Chlamydomonas pila, but Chlamydomonas debaryana (for example) is usually closer when it is included.

I wouldn’t say that the evolutionary relationships in this group are fully settled at this point; the particulars vary among authors, depending on the gene(s) analyzed, and even depending on the method of phylogenetic inference. Even the monophyly of the multicellular species has been called into question, though I think it’s definitely too early to be confident in that conclusion. Right now it seems that Chlamydomonas pila is the best contender for the sister species to the multicellular clade, and almost certainly a closer relative to Volvox and co. than Chlamydomonas reinhardtii. As the authors point out, this makes C. pila a good candidate for whole-genome sequencing. The closer a relative to the multicellular group we can find, the better we can resolve which changes are specific to the multicellular clade.

 

Stable links:

Nakada, T., Tsuchida, Y. & Tomita, M. 2019. Improved taxon sampling and multigene phylogeny of unicellular chlamydomonads closely related to the colonial volvocalean lineage Tetrabaenaceae-Goniaceae-Volvocaceae (Volvocales, Chlorophyceae). Mol. Phylogenet. Evol. 130, 1–8. doi: 10.1016/j.ympev.2018.09.013

Undergraduate summer internships at the Danforth Center

This is an unbelievable opportunity: an NSF-funded, paid summer internship at the Donald Danforth Plant Science Center in St. Louis. Ru Zhang is at the Danforth Center. Jim Umen is at the Danforth Center. The Fourth International Volvox Conference was at the Danforth Center. If you’re an undergraduate and you think you might want to study Volvox or Chlamydomonas (or plants), this would be a great way to get started.

Danforth Internship

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Volvox newsletter

Volvox newsletter cover

As David Kirk pointed out, what we normally call the First through Fourth International Volvox Meetings are really about the fifth through eighth, as they were preceded by several meetings in the ’70s. The very first meeting was hosted by David and Marilyn Kirk at Washington University in St. Louis. Richard Starr, then at Indiana University, reported on the meeting in the first Volvox Newsletter (Dr. Starr would later move to the University of Texas, and his strains would form the beginning of the UTEX Culture Collection, which is still in operation).

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More Volvox correspondence

I previously corresponded with a science teacher in India, who wrote me with some questions about Volvox. After our initial exchange, my correspondent wrote

Can you please name if there is any unicellular colonial microorganism found?

I asked for clarification and received this reply:

I read about colonial organisms being unicellular and multicellular. Few people think Volvox as colonial organism which is unicellular while Phylum Bryozoa has colonial organisms which are multicellular. The confusion started here. What are colonial microorganisms really? If they are unicellular and multicellular why are they called as colonial then? Bacteria being unicellular which form colonies thought Can bacteria be called as colonial organism? I tried to look for the same but I have not found something solid which says bacteria can be called as colonial organisms. I want to explain colonial organisms to children and don’t want to provide wrong information.

Can you please help in understanding do colonial unicellular microorganism exist? I asked one of the microbiologist I know in here she is also not clear with the concept or probably I might have read something wrong. Need guidance.

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Mary Agard Pocock

Alexey Desnitskiy, Stuart Sym, and Pierre Durand have published a new paper in Transactions of the Royal Society of South Africa recounting the contributions of South African phycologist Mary Agard Pocock to Volvox research [full disclosure: Pierre Durand and I were labmates in Rick Michod’s lab at the University of Arizona for a time, and Alexey Desnitskiy is a friend and collaborator].

Pocock, who defended her Ph.D. in 1932, made careful observations of both sexual and asexual development in several species of Volvox that she collected in southern Africa: V. africanus, V. capensis,V. rousseletii, and V. gigas (which she originally described). For some of these species, hers are still the only detailed descriptions of their ontogeny:

Pocock studied almost all aspects of asexual and sexual development in several African Volvox species, with the exception of sexual differentiation control…Pocock’s data on embryonic inversion in V. africanus, V. capensis, V. gigas and V. rousseletii retain their importance today. Her description of inversion during asexual development in V. africanus and V. capensis remains the only detailed study of this process in these two species and her observations of embryonic inversion in V. gigas and V. rousseletii were corroborated almost 40 years later. [references omitted]

Pocock 1933 Fig. 2L-O

Figure 2L-O from Pocock 1933. Inversion in Volvox gigas.

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I was in Canada

I have been disloyal to the fierce roller. After grad school, I stepped away from Volvox for a couple of years to do a postdoc with Michael Doebeli at the University of British Columbia. I thought I was going to transition to mathematical modeling, and Dr. Doebeli and I did do a bit of that together. I also got my first exposure to next-generation sequencing in his lab. I eventually returned to the fold, but during my time in Canada I wasn’t paying much attention to the Volvox world.

As a result, I missed Jerry Coyne’s coverage of the Volvox genome, which was published in 2010, just as I was discovering Jericho Beach, enjoying cheap sushi, and struggling to understand adaptive dynamics.

What does it take to become multicellular?

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CRISPR/Cas9 mutagenesis in Volvox

Researchers in Stephen Miller’s lab at the University of Maryland, Baltimore County have successfully used CRISPR/Cas9 to knock out several developmentally important genes in Volvox carteri. CRISPR/Cas9 is a relatively new technology that allows heritable mutations to be introduced into living cells at specific locations within the genome.

This advance was announced in a new paper in The Plant Journal by José A. Ortega-Escalante, Robyn Jasper, and Stephen M. Miller (Jasper and Ortega-Escalante are listed as equal contributors). They were able to transform wild-type V. carteri with inversion-deficient and somatic-regenerator mutations, and they transformed somatic regenerator mutants with a gonidialess (no specialized reproductive cells) mutation.

I have never used CRISPR/Cas9, and I don’t know as much about it as I should, so I’m sure any explanation I gave would be riddled with errors. Here’s someone who seems to know what she’s talking about:

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