Of Macros and Micros

Vorticella, a sessile ciliate of the intramacronucleate class Oligohymenophora. Photo from here.

Today's Taxon of the Week is the ciliate subphylum Intramacronucleata. Ciliates, one of the most famous groups of protozoa, have been touched on previously at the Catalogue of Organisms. They are certainly one of those groups of organisms that get progressively cooler the further one looks. Admittedly, there are few groups of organisms to which that wouldn't apply.

Intramacronucleata is the largest of the two primary subdivisions within the ciliates recognised in the recent years, and includes most well-known ciliates such as George (Paramecium) and George (Tetrahymena), as well as the Georges (Spirotricha) discussed at the post linked to above (names due to an ex-partner of mine who decided that Paramecium was far too unwieldy a word, and henceforth all microbes should be known as George). The other subphylum goes by the even more unwieldy moniker of Postciliodesmatophora (Lynn, 2003). The name refers to one of the more intriguing features of ciliates, the macronucleus. Ciliate cells always contain at least two nuclei, the reproductive micronucleus and the transcriptional macronucleus. Depending on species and life-cycle stage, a ciliate may have between one and twenty micronuclei, and from one to several hundred macronuclei (McGrath et al., 2006). The vast majority of transcription happens from chromosomes contained in the macronuclei. However, when conjugation (sexual reproduction) occurs, the macronuclei break down and only the micronucleus is propagated. Two conjugating ciliates each generate a pair of haploid micronuclei, one of which they donate to the other. The donor and recipient micronuclei then fuse to form the new diploid micronucleus, which gives rise to the daughter cells' macronuclei. (In the post linked to above, I originally said that the macronuclei break down during cell division, but I was wrong. It only happens in conjugation).


Reproductive cycles in ciliates. Diagram from here.

Despite being derived from the micronucleus, the macronucleus is genetically very different from its progenitor. As well as being replicated, the original genome is subjected to an intense processing programme (described in detail by McGrath et al., 2006). The fewer standard chromosomes contained in the micronucleus are fragmented into a larger number of much smaller chromosomes, each of which is usually present in a large number of chromosomes. The most extreme examples are found among the spirotrichs, some of which start with 120 micronuclear chromosomes which they divide up into as many as 24,000 macronuclear chromosomes. Each of these macronuclear chromosomes may comprise only a single gene, and there may be up to 15,000 copies of each one. New telomeres are generated and tacked onto each of the newly-produced chromosomes. Non-functional sections of DNA in the original micronuclear genome such as repetitive elements, introns and transposons (up to 95% of the original sequence) are brutally excised from the daughter chromosomes, which are stitched back together to form unbroken transcriptional templates.

Intramacronucleata get their name because the microtubules involved in macronuclear division form within the nuclear envelope, while the Postciliodesmatophora include one class (the Heterotrichea) in which the microtubules form outside the macronucleus, and one (the Karyorelictea) in which the macronuclei do not undergo division. While micronuclei divide like respectable nuclei by a process of mitosis, macronuclei are anarchists to the core and divide by a poorly-understood process called amitosis. Amitosis differs from mitosis in that there is no mitotic spindle. As a result, the division of chromosomes between amitotically-produced nuclei is not necessarily even, and in some species of ciliate one daughter nucleus will regularly contain more than twice as many chromosomes as the other. This may explain why ciliate macronuclei may contain such a ridiculous number of copies of each chromosome. When one also factors in that macronuclei are not necessarily evenly distributed during cell division, individual ciliates can vary significantly in their functional genetic makeup even if they descend asexually from the same ancestral cell.


Trichodina, another member of the Oligohymenophora, and a parasite of fish. Image from here.

There is an intriguing paradox at work as a result of all this. Because of their unique disconnect between the products of reproduction and the functional template, one can't help wondering if ciliates are, to some extent, able to dodge the consequences of natural selection. Does the ruthless excision of non-functional sequences prior to transcription mean that the ciliate genome may accumulate more such sequences than it could normally? The uneven assortment of chromosomes during amitosis means that not every macronucleus will necessarily contain all alleles present in the micronucleus. Does this mean that deleterious mutations can persist in the micronucleus even if they would impair function in the macronucleus? Zufall et al. (2006) demonstrated that ciliates showed significantly higher rates of genetic evolution than other eukaryotes, and suggested that such potential persistance of deleterious alleles increased the chance of compensatory mutations appearing in the genome before selection took its toll. As Zufall et al. put it, ciliates were therefore free to "explore protein space" to a higher degree than was possible for other eukaryote groups.

REFERENCES

Lynn, D. H. 2003. Morphology or molecules: How do we identify the major lineages of ciliates (phylum Ciliophora)? European Journal of Protistology 39 (4): 356-364.

McGrath, C. L., R. A. Zufall & L. A. Katz. 2006. Ciliate genome evolution. In Genomics and Evolution of Microbial Eukaryotes (L. A. Katz & D. Bhattacharya, eds.) pp. 64-77. Oxford University Press.

Zufall, R. A., C. L. McGrath, S. V. Muse & L. A. Katz. 2006. Genome architecture drives protein evolution in ciliates. Molecular Biology and Evolution 23 (9): 1681-1687.