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Playing Roulette with Seven Sexes

Have you ever watched “Seven Brides for Seven Brothers”? There are these seven brothers and, well you get the idea… But that was complicated enough with the two sexes that we boring old humans have – what if you had seven? That’s the exotic situation that the ciliate Tetrahymena finds itself in.

Tetrahymena [from Robinson R (2006) Ciliate Genome Sequence Reveals Unique Features of a Model Eukaryote. PLoS Biology 4(9):e304.]
We can only speculate as to how these creatures handle their private lives, but thanks to a paper just published in PLOS Biology we now know how they decide which of the seven sexes to be.

PLOS Biology recently published another example of ciliate madness – the bizarre 16,000 chromosomes of Oxytricha. Each generation that creature makes a “working copy” of its genome by a massive cut’n’paste job that results in almost one chromosome per gene. Tetrahymena does a similar thing, though not as spectacularly (a mere 225 chromosomes as published in another PLOS Biology paper), and that’s where the sex decision is taken.

Marcella Cervantes, Eduardo Orias and colleagues now show how this happens, and it involves playing genomic roulette. Each generation two little Tetrahymena of different sex get together, turn up the Barry White, and cook up an unholy blend of their germline genomes. The offspring then makes its working copy (somatic) genome, and it’s around this time that it spins the wheel of fortune to decide what sex it’s going to be.

For an accessible account of how the authors actually went about their study, read Richard Robinson’s excellent Synopsis. However, I’m just going to cut to the chase and tell you how the funky roulette bit happens. While the baby Tetrahymena is rearranging the rest of its genome, one little bit of this genome is particularly busy. This region consists of a tight cluster of six back-to-back gene pairs (the authors use a strain that only has six sexes, just to make things inconvenient for bloggers and synopsis writers).

This array of genes is the roulette wheel. Each “number” comprises a pair of incomplete genes that should encode membrane-spanning proteins; the six pairs are clearly related to each other yet distinct, suggesting that they might do subtly different versions of the same job.

The relationship between Tetrahymena germline and somatic sex loci and their encoded proteins. Dotted lines indicate relationships between genes, rather than actual recombination events.
The relationship between Tetrahymena germline and somatic sex loci and their encoded proteins. Dotted lines indicate relationships between genes, rather than actual recombination events.

The fact that they’re incomplete is crucial. Comparing this germline array with the corresponding region of the “working copy” (somatic) genome reveals just how the game plays out. In each sex all but one of the gene pairs is deleted, leaving just one pair to determine the sex.  And the genomic cut’n’paste that does this neatly splices that remaining gene pair onto sequences at each end of the array, thereby completing the previously truncated genes and allowing them to be transcribed fruitfully. The selection of the remaining gene pair, and therefore of the sex, appears to be left entirely to chance, ensuring a good mix of sexes in the population.

Although this study stops with the identification of the genomic shenanigans, the assumption is presumably that these sex-specific pairs of transmembrane proteins somehow allow the sexes to recognise each other, or at least to avoid mating with the same sex. Even with their help, Tetrahymena dating must be a complicated business indeed.

Cervantes, M., Hamilton, E., Xiong, J., Lawson, M., Yuan, D., Hadjithomas, M., Miao, W., & Orias, E. (2013). Selecting One of Several Mating Types through Gene Segment Joining and Deletion in Tetrahymena thermophila PLoS Biology, 11 (3) DOI: 10.1371/journal.pbio.1001518

Robinson, R. (2013). Mating type determination in Tetrahymena: Last man standing PLOS Biology, 11 (3) DOI: 10.1371/journal.pbio.1001522

  1. Thanks for a nice summary of the paper and links to other interesting cilate work. One of the interesting points of this work is the apparent necessary coupling of a poor environment (starvation) and sex. To my mind, this suggests that much of the randomness of the gender draw is related to maintaining as much variation as possible, that is to reduce linkage to genes that in one circumstance will be useful but in another not. I don’t follow the genetic logic at this reading to understand whether this actually results from the mechanisms found but it seems to be a possibility.

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