Unorthodox

Olivia Judson on the influence of science and biology on modern life.

Sara Krulwich/The New York Times Ciliates like the paramecium have very unusual sex, a fact often unmentioned in high school biology class.

When it comes to sex and reproduction, mammals are ultra-orthodox and, frankly, rather dull. Individuals are either male or female, no one changes sex and there are never more than two sexes in a species. No mammal reproduces asexually — by budding off a small piece of itself, say, or by splitting down the middle and growing a new individual from each half. Nope: among mammals, offspring are always produced by sex. That is, an egg fuses with a sperm to produce a child that is genetically distinct from both parents.

But things can get much hairier. Take ciliates — which get my vote for Life-form of The Month: February.

Most ciliates are single-celled organisms covered with tiny hair-like structures known as cilia — which is Latin for eyelashes. The cilia are used for a variety of activities, including swimming and feeding. Some ciliates even use them to scuttle across surfaces.

Behind the cilia, however, ciliates are a diverse and ancient group. Their lineage split off from the one that we evolved from more than a billion years ago; their closest relations are the apicomplexans (a group of single-celled parasites that includes Plasmodium, the bug that causes malaria) and the dinoflagellates (which I profiled in January).

Ciliates live in all kinds of places, from the guts of cockroaches to the waters around Antarctica, and they have a range of lifestyles. Some are filter feeders, sieving particles of food from the water like microscopic blue whales. Others are active predators, harpooning their prey (usually bacteria, or other ciliates) and killing them with poisons.

And if you’re a fact jock, you’ll like this detail. Almost all organisms on the planet read their DNA with the same language, so that if you put a jellyfish gene into a pig, you get exactly the same product in both organisms. Ciliates, however, don’t play strictly by the rules: they have repeatedly evolved small variations on the normal way of reading genes. (They also, mysteriously, have rather a lot of genes: some have as many as 30,000, which is several thousand more than we have.)

Although ciliates sound obscure, they’ve been hugely important in scientific research. Last year, for example, three scientists won a Nobel prize for their discoveries in the ciliate Tetrahymena. (The discoveries concerned telomeres — the bits of DNA that cap off chromosomes — and telomerase — the enzyme that keeps telomeres in good shape. Both are thought to be important in aging.) And if you did biology at school, a ciliate may already have batted its eyelashes at you: the lozenge-shaped paramecium often gets put under the classroom microscope for everyone to draw. Usually, though, no one mentions it’s a representative of one of the most sexually unorthodox groups on Earth.

Ciliate sex is peculiar in several ways. For one thing, reproduction and sex do not happen together. When a ciliate reproduces, it does so asexually, typically by splitting in half and growing a complete new individual from each piece. So: where there was one individual, there are now two.

In and of itself, asexual reproduction is not especially strange — many organisms, from aphids to sea anemones, do it at least from time to time. The weird stuff happens when ciliates get sexual.

In ciliate sex, two individuals arrive, and two individuals leave: no eggs are fertilized, no offspring are produced. But by the time the two individuals go their separate ways, a massive change will have come over both of them: they will both have acquired a new genetic identity.

Here’s what happens. Each ciliate has something called a micronucleus; this contains two complete versions of its genome. During sex, the micronucleus divides in such a way that each individual keeps one version of its genome for itself; it then gives an exact copy of this version to its partner. Afterwards, each individual fuses the two genomes (the one it kept and the one it got) to make a new micronucleus.

This has three odd consequences. The first is that, by the end of sex, the two individuals have become genetically identical. It’s as if you and your mate began coitus as yourselves and finished as identical twins. The second odd consequence is that, partway through its life, a ciliate can radically alter its genetic make-up; genetically speaking, the transformation is so extreme that it’s as if you changed into one of your children. Talk about being reborn.

Which brings me to the third odd consequence: after sex, the organism undergoes a profound remodeling.

Ciliates have evolved a curious system by which the micronucleus is reserved for sex: the DNA there is not involved in the day-to-day running of the cell. Instead, the job of running the cell is done by something known as the macronucleus. (After sex, the old macronucleus is destroyed, and a new one is built.)

The macronucleus is made from the micronucleus, but it is not at all the same in content. In extreme cases — such as that of Oxytricha trifallax — less than 5 percent of the DNA in the micronucleus is used by the macronucleus. The rest is cut out and thrown away.

Why? It’s not clear. However, what we do know is this: like many organisms, ciliates have a lot of DNA that does not encode genes. It’s this other DNA that gets removed from the macronucleus: the macronucleus is a genes-only sort of place. But why the micronucleus has all this extra “stuff”, and what function it serves, is something of a mystery. (Part of the answer is that the micronucleus has accumulated huge numbers of genetic parasites — DNA segments that simply proliferate themselves. To what extent these can also serve their host is an interesting question. Recent results suggest that at least some of these “parasitic” sequences play an important part in building the macronucleus.)

As if that wasn’t enough strangeness, here’s one other peculiar detail. Many ciliates have more than two sexes (or “mating types”) and some — Stylonychia mytilus, for example — have as many as 100. This doesn’t mean that 100 individuals have to gather for sex to take place. Rather, it means that you can mate with anyone not of the same mating type as yourself. In principle, it gives you more choice: with more mating types, more individuals are eligible mates. In my next life . . . .

For a summary of ciliate biology, see pages 138-139 of Margulis, L. and Schwartz, K. V. 1998. “Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth.” Third Edition. Freeman.

I took my estimate of the time that the ciliate lineage separated from the one that (eventually) produced us from Wright, A. D. G. and Lynn, D. H. 1997. “Maximum ages of ciliate lineages estimated using a small subunit rRNA molecular clock: crown eukaryotes date back to the paleoproterozoic.” Archiv für Protistenkunde 148: 329-341.

For ciliates living in the guts of cockroaches, see Ricard, G. et al. 2008. “Macronuclear genome structure of the ciliate Nyctotherus ovalis: single-gene chromosomes and tiny introns.” BMC Genomics 9: 587. For ciliates living in the oceans around Antarctica, see la Terza, A. et al. 2007. “Adaptive evolution of the heat-shock response in the Antarctic psychrophilic ciliate, Euplotes focardii: hints from a comparative determination of the hsp70 gene structure.” Antarctic Science 19: 239-244. For the various feeding habits of ciliates, see Verni, F. and Gualtieri, P. 1997. “Feeding behaviour in ciliated protists.” Micron 28: 487-504.

For an estimate of 30,000 genes in some ciliate species, see Zagulski, M. et al. 2004. “High coding density on the largest Paramecium tetraurelia somatic chromosome.” Current Biology 14: 1397-1404. Note that the 30,000 figure refers only to protein-coding genes in the macronucleus. Ciliates are famous for using non-canonical genetic codes for reading their genes; see, for example, the discussion in Eisen, J. A. et al. 2006. “Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote.” PLoS Biology 4: e286. See also Salas-Marco, J. et al. 2006. “Distinct paths to stop codon reassignment by the variant-code organisms Tetrahymena and Euplotes.” Molecular and Cellular Biology 26: 438-447. For details of the Nobel prize, see here.

The details of ciliate sex, and the behavior of the micronucleus and the macronucleus, differ slightly from one species to the next; my description is taken from the aforementioned Margulis and Schwartz, and also from Jönsson, F., Postberg, J. and Lipps, H. J. 2009. “The unusual way to make a genetically active nucleus.” DNA and Cell Biology 28: 71-78. For the throwing out of large quantities of DNA from the macronucleus of Oxytricha trifallax, see Doak, T. G. et al. 2003. “Sequencing the Oxytricha trifallax macronuclear genome: a pilot project.” Trends in Genetics 19: 603-607. For an overview of some of the remodeling that goes on in ciliates more generally, see Prescott, D. M. 2000. “Genome gymnastics: unique modes of DNA evolution and processing in ciliates.” Nature Reviews Genetics 1: 191-198. For certain genetic parasites having a useful role in building the macronucleus, see Nowacki, M. et al. 2009. “A functional role for transposases in a large eukaryotic genome.” Science 324: 935-938.

For ciliates having more than two sexes, see Phadke, S. S. and Zufall, R. A. 2009. “Rapid diversification of mating systems in ciliates.” Biological Journal of the Linnean Society 98: 187-197. It is from this paper that I took the number of 100 sexes for Stylonychia mytilus. Note that it is not clear what leads to some species having large numbers of sexes, while others have just two.

Many thanks to Austin Burt and Jonathan Swire for insights, comments and suggestions.