Plagiopyla nasuta, from the Protist Information Server.

Belongs within: Sar.
Contains: Myzozoa, Karyorelictea, Heterotrichea, Spirotricha, Armophorea, Trichostomatia, Haptoria, Dileptida, Phyllopharyngea, Colpodea, Nassophorea, Oligohymenophorea, Prostomatea.

Of macros and micros
Published 6 October 2008
Vorticella, a sessile ciliate of the intramacronucleate class Oligohymenophora. Photo from here.

Today’s featured subject is the ciliate subphylum Intramacronucleata. Ciliates, one of the most famous groups of protozoa, have been examined previously at this site. 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.

Systematics of Alveolata
    |--Miozoa [Colponemida, Protalveolata]C-S18
    |    |--+--Acavomonas [Acavomonadea, Acavomonadida]C-S18
    |    |  `--MyzozoaC-S04
    |    `--ColponemeaC-S18
    |         |--Palustrimonas Patterson & Simpson 1996AB19 [Palustrimonadida, PalustrimonadidaeC-S18]
    |         `--Colponema [Colponemidia, Colponemidae]C-S18
    |              |--C. loxodes Stein 1878FT93
    |              `--C. vietnamicaC-S18
    `--Ciliophora (see below for synonymy)C-S04
         |  i. s.: BryophyllidaeF03a
         |           |--ApobryophyllumF03a
         |           `--Bryophyllum armatusSX97
         |         Cultellothrix velhoi Foissner 2003F03b
         |         Glauconema trihymeneMCS03
         |         Metanophrys sinensisMCS03
         |         Paranophrys magnaMCS03
         |         Histobalantium marinumD86
         |         Microdiaphanosoma arcuatumFS-K03
         |         Pattersoniella vitiphilaFS-K03
         |         Pseudocyrtolophosis alpestrisFS-K03
         |         Stammeridium kahliFS-K03
         |         Triadinium Fiorentini 1890FT93
         |         Peridinopsis James-Clark 1866FT93
         |         SphaerophryaLB90
         |           |--S. magnaLB90
         |           `--S. soliformisSX97
         |         Phascolodon vorticellaAS-K07
         |         Perispira Stein 1859LT61
         |         Choenia teresG84
         |         Chilodon cucullulusG84
         |         Myrionecta rubrumC-S18
         |         Tiarina fususTP87
         |         Bursariella truncatellaTP87
         |         CampanellaG20
         |           |--C. berberinaG20
         |           `--C. umbellariaG20
         |         Valvularia bilineataG20
         |         Stegochilum fusiformeV63
         |    |--KaryorelicteaL03
         |    `--HeterotricheaL03
         `--Intramacronucleata [Hypostomata, Vestibulifera]L03
              |  i. s.: CoelosomidesD86
              |           |--C. marinaD86
              |           `--C. vermiformeD86
              |--Protocruzia Faria da Cunha & Pinto 1922AS12 [Protocruzea, ProtocruziaC-S18, Protocruziidae, Protocruziidia]
              |    `--P. adherensC-S04
              |    |  i. s.: Cariacothrix Orsi et al. 2012AS12 [CariacotricheaC-S18]
              |    |           `--C. caudataAS12
              |    |         Mesodinium [Mesodiniidae]AB19
              |    |           |--M. pulexD86
              |    |           `--M. rubrumOSS10
              |    |--SpirotrichaAB19
              |    `--LamellicorticataAB19
              |         |--ArmophoreaAB19
              |         `--Litostomatea [Filocorticata, Gymnostomatea]AB19
              |              |--TrichostomatiaL03
              |              |--HaptoriaL03
              |              |--DileptidaAB19
              |              `--Helicoprorodon [Helicoprorodontidae]AB19
              |                   `--H. barbatusD86
              `--Conthreep [Cyrtophora, Ventrata]AB19
                   |  i. s.: Askenasia Blochmann 1895AB19
                   |         Cyclotrichium [Cyclotrichiidae]AB19
                   |         Paraspathidium Noland 1937AB19
                   |         Pseudotrachelocerca [Pseudotrachelocercidae]AB19
                   |         Discotrichidae [Discotrichida]AB19
                   |           |--DiscotrichaAB19
                   |           `--LopezotereniaAB19
                      |  `--NassophoreaC-S18
                            `--Plagiopylea [Plagiopylida]L03
                                 |  i. s.: Sonderia [Sonderiidae]AS12
                                 |           |--S. schizostomaD86
                                 |           `--S. voraxD86
                                 |--Trimyema [Trimyemidae]L03
                                 |    `--T. compressumL03
                                 `--+--Lechriopyla mystaxL03
                                    `--Plagiopyla [Plagiopylidae]L03
                                         |--P. minutaBK77
                                         |--P. nasutaL03
                                         `--P. nyctotherusBK77

Ciliophora [Ciliata, Gymnostomata, Gymnostomatida, Heterokaryota, Heterotrichida, Holotricha, Kinetophragmophora, Polyhymenophora, Primociliatida, Tubulicorticata, Vorticellae]C-S04

*Type species of generic name indicated


[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

[AS-K07] Agatha, S. & M. C. Strüder-Kypke. 2007. Phylogeny of the order Choreotrichida (Ciliophora, Spirotricha, Oligotrichea) as inferred from morphology, ultrastructure, ontogenesis, and SSrRNA genes sequences. European Journal of Protistology 43 (1): 37–63.

[BK77] Barel, C. D. N., & P. G. N. Kramers. 1977. A survey of the echinoderm associates of the north-east Atlantic area. Zoologische Verhandelingen 156: 1–159.

[C-S04] Cavalier-Smith, T. 2004. Only six kingdoms of life. Proceedings of the Royal Society of London Series B—Biological Sciences 271: 1251–1262.

[C-S18] Cavalier-Smith, T. 2018. Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences. Protoplasma 255: 297–357.

[D86] Detcheva, R. 1986. Ciliata interstitiels, essentiellement des sables marins. In: Botosaneanu, L. (ed.) Stygofauna Mundi: A Faunistic, Distributional, and Ecological Synthesis of the World Fauna inhabiting Subterranean Waters (including the Marine Interstitial) pp. 21–29. E. J. Brill/Dr W. Backhuys: Leiden.

[FT93] Fensome, R. A., F. J. R. Taylor, G. Norris, W. A. S. Sarjeant, D. I. Wharton & G. L. Williams. 1993. A classification of living and fossil dinoflagellates. Micropaleontology Special Publication 7: i–viii, 1–351.

[F03a] Foissner, W. 2003a. The Myriokaryonidae fam. n., a new family of spathidiid ciliates (Ciliophora: Gymnostomatea). Acta Protozoologica 42: 113–143.

[F03b] Foissner, W. 2003b. Two remarkable soil spathidiids (Ciliophora: Haptorida), Arcuospathidium pachyoplites sp. n. and Spathidium faurefremieti nom. n. Acta Protozoologica 42: 145–159.

[FS-K03] Foissner, W., M. Strüder-Kypke, G. W. M. van der Staay, S. Y. Moon-van der Staay & J. H. P. Hackstein. 2003. Endemic ciliates (Protozoa, Ciliophora) from tank bromeliads (Bromeliaceae): a combined morphological, molecular, and ecological study. European Journal of Protistology 39 (4): 365–372.

[G20] Goldfuss, G. A. 1820. Handbuch der Naturgeschichte vol. 3. Handbuch der Zoologie pt 1. Johann Leonhard Schrag: Nürnberg.

[G84] Gruber, A. 1884. Die Protozoen des Hafens von Genua. Verhandlungen der Kaiserlichen Leopoldinisch-Carolinischen Deutschen Akademie der Naturforscher [Nova Acta Academiae Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosorum] 46 (4): 473–539, pls 7–11.

[LT61] Loeblich, A. R., Jr & H. Tappan. 1961. Remarks on the systematics of the Sarkodina (Protozoa), renamed homonyms and new and validated genera. Proceedings of the Biological Society of Washington 74: 213–234.

[LB90] Lousier, J. D., & S. S. Bamforth. 1990. Soil protozoa. In: Dindal, D. L. (ed.) Soil Biology Guide pp. 97–136. John Wiley & Sones: New York.

[L03] 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.

[MCS03] Ma, H., J. K. Choi & W. Song. 2003. An improved silver carbonate impregnation for marine ciliated protozoa. Acta Protozoologica 42: 161–164.

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

[OSS10] Orlova, T. Yu., I. V. Stonik & M. S. Selina. 2010. The diversity of HABs causative organisms on the Russian Pacific coast. In: China-Russia Bilateral Symposium: Proceedings of the China-Russia Bilateral Symposium of “Comparison on Marine Biodiversity in the Northwest Pacific Ocean”, 10–11 October 2010, Qingdao (China) pp. 66–70. Institute of Oceanology, Chinese Academy of Sciences; A. V. Zhirmunsky Institute of Marine Biology, Far East Branch of the Russian Academy of Sciences.

[SX97] Song B. & Xie P. 1997. Preliminary studies on the community structure of the planktonic protozoa from the outlet of Lake Dongting. Acta Hydrobiologica Sinica 21 (Suppl.): 60–68.

[TP87] Taylor, F. J. R., & U. Pollingher. 1987. Ecology of dinoflagellates. In: Taylor, F. J. R. (ed.) The Biology of Dinoflagellates pp. 398–529. Blackwell Scientific.

[V63] Varga, L. 1963. Weitere Untersuchungen über die aquatile Mikrofauna der Baradla-Höhle bei Aggtelek (Ungarn) (Biospeologica Hungarica, XVII). Acta Zoologica Academiae Scientiarum Hungaricae 9 (3–4): 439–458.

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.

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