Eukarya |--+--Fungi | `--Metazoa |--Amoebozoa `--+--Rhizaria |--Metamonada `--o--Plantae `--o--Chromista `--Alveolata |--Ciliophora `--Miozoa |--Dinozoa | `--Dinoflagellata `--Apicomplexa
Alveolata is a high-order group of Eukarya whose principal members include (a) the Ciliophora (e.g., Paramecium), (b) a large group of revolting parasites called the Apicomplexa or Sporozoa (e.g. Plasmodium, the organism responsible for malaria), and (c) the dinoflagellates, a hugely successful group of marine photosynthetic and heterotrophic organisms. In addition, the Haplosporidia may fall within the Alveolata. For the moment, however, we will leave them out of the mix.
Despite their considerable success, the Alveolata are apparently a taxon of relicts. They are united by the presence of small vesicles (alveoli) in, or just under, the plasma membrane. The function of the alveoli is unknown, although they are believed to form part of a complete inner membrane system. The usual speculation is that they function in ion transport and in structural stabilization of the cell membrane. The outer membrane is pierced by micropores of unknown function. Siddall et al. (2001). The internal membrane systems may be present, but dictyosomes are often reduced. The implication, we assume, is that the alveoli are taking up the transport function normally assumed by the Golgi apparatus. The Microscope site adds: "Flagella when present (whether as flagella or cilia) typically with at least one cross-striated fibrous root". We take this character to be primitive for Eukarya. The Alveolata share with their sister clade, Chromista, an interesting flagellar accessory known as the mastigoneme, which is described at the glossary entry. The Alveolata also go in for other strange, and sometimes unique, organelles, but these are not synapomorphies of the whole taxon, and we will take them up as need be. All of the Alveolata prefer oxygen-rich environments and engage in oxidative metabolism using mitochondria of the usual, tubulocristate kind.
But that's about the extent of their similarities. The three alveolate taxa otherwise seem very different. The ciliates are free-living heterotrophs, most of which inhabit soils. The dinoflagellates are marine (benthic or planktonic) photosynthetic autotrophs and/or heterotrophs. The Apicomplexa are all obligate parasites. Nevertheless, these three disparate strands consistently braid together in both molecular and morphological tests. We are therefore forced to the conclusion that we're looking at a relict taxon, in which only isolated fragments remain of an originally continuous spectrum of diversity.
In this context, the recent work of Siddall et al. (2001) is particularly welcome. The Siddall group addressed the molecular phylogeny of three, very similar, alveolate genera with debatable affinities: Colpodella, Perkinsus, and Parvilucifera. The thought was that these forms might represent missing links between the three major alveolate taxa.
The basic structure of these forms is shown in the figure from Siddall et al. (2001). The essential structures are not really very different from the karyomastigont structure which has been proposed as the basal organelle arrangement of the Eukarya. We see a complex anterior microtubular array from which the flagella emerge. There are fibrous sheets radiating from the "mastigont" as well, although these are not as closely integrated with the flagellae as in Metamonada. Instead of only a posterior flagellar/feeding groove, we see both posterior and lateral grooves. At least one flagellum bears mastigonemes. The nucleus is no longer bound into the mastigont. The internal, alveolar membrane system is present, with micropores associated with the alveoli. When displayed in this manner, the system is curiously reminiscent of the polar filament coils of the Microsporidia -- a similarity which may not be coincidental if a secondary membrane system should turn out to be basal to Metabiotiformes. Extrusomes (another apparent synapomorphy of Metabiotiformes) are present and take the form of elongate, somewhat club-shaped sacs terminating anteriorly. These are quite similar to the rhoptries of the Apicomplexa. Similarly, all genera have some sort of anterior conoid-like structure associated with predation or intracellular insertion in the Apicomplexa.
Siddall's theoretical approach to molecular work is outstanding. It is constrained by morphological data and gives appropriate attention to the morphological implications. Therefore his results ought to have rather higher credibility than many such studies -- particularly here, where morphology will probably not be sufficient to resolve phylogeny. The Siddall group also wisely uses two completely different gene sequences: for actin and for SSU rRNA. They do not find a unique solution, but their results tend to yield a phylogeny along the lines shown in the image.
The Siddall group's execution of this particular study has, however, been heavily criticized for various technical errors. See, e.g., Cavalier-Smith & Chao (2004). These criticisms are almost certainly correct with respect to Colpodella. Nonetheless, the differences between the ultimate results of Siddall and Cavalier-Smith are not particularly earth-shattering at the level of resolution relevant here. Neither Siddall nor Cavalier-Smith were ultimately able to say with any confidence just where Colpodella lies. The answer to that question may well depend on which species and isolate one studies. Perkinsus and Parvilucifera are Dinozoa in both studies. The apparent disagreement comes only from the usual (we were about to say "pig-headed", but exerted our usual iron self-discipline just in time) refusal of protistologists to adopt reasonable phylogenetic definitions.
Curiously, none of the three genera turns out to be a definite apicomplexan. Parvilucifera and Perkinsus are Dinozoa. Colpodella turns out to be "a paraphyletic mess hovering about the base of Miozoa" [phrasing courtesy of C. Taylor, 2004]. Since none of these genera show any obvious synapomorphies with the three main alveolate clades, Siddall et al. propose that these three collectively exemplify the basal type of all Alveolata. From our previous discussion, this observation may be limited just to the Miozoa. Still, it looks to be a pretty good bet for that group. Other than micropores and alveoli, the basic structure looks not so different from, for example, an oxymonad.
In the fullness of time, we hope to get more deeply into this particularly weird corner of phylospace. Certainly there is much more here than just green dinoflagellates and evil, parasitic sporozoans. As in human society, there are any number of odd characters who are impossible to categorize -- as well as an unsettling number of evil, parasitic green dinoflagellates and beneficial sporozoans.
ATW041031. Text public domain. No rights reserved. Revised ATW041104. This section has benefited considerably from the thoughtful comments of Christopher Taylor, Univ. of Auckland who, of course, is not responsible for any thoughtless errors we have made in applying them.
The Ciliophora are the ciliates, including the ubiquitous Paramecium of high school biology texts. They may have a fossil history going back into the Precambrian, if chitinozoans are, as suspected, ciliophoran coverings. Ciliophora are both very common and quite diverse. Most are free-living aquatic predators. They may be benthic or planktonic and, at times, Ciliophora may account for a very large fraction of standing plankton biomass.
The Ciliophora are characterized, reasonably enough, by the presence of cilia. Generally speaking, cilia are simply short flagella. At some stage of life, ciliophorans have numerous cilia covering some substantial fraction of the cell membrane. The cilia often occur in rows (kineties), which helps to explain how hundreds of separate cilia can be coordinated in locomotion. The ciliary bases are attached to the pellicle, a peripheral cytoskeleton. In addition, Ciliophora have an epiplasm composed of a fibrous mesh.
The plasma membrane has both a permanent cytostome ("mouth") and a permanent cytoproct ("anus"). The cytoproct is a feeding groove presumably derived from the old posterior flagellar groove. The more exterior portion of the cytostome is underlain by a fibrous network, as was the ancestral flagellar groove. The groove terminates in a region which packages the food particles into digestive vacuoles and pinches them off into the cytoplasm. The kineties around the cytostome are arranged to funnel particles deeper into the feeding groove. Also associated with the plasma membrane are extrusomes, which rapidly eject short threadlike structures (as do the possibly homologous micronemes of Apicomplexa). These extrusomes function in predation, defense, and in forming cysts in various Ciliophora.
The cytoplasm contains, in addition to digestive vacuoles, contractile vacuoles which probably function in the control of osmotic pressures. They can open to the medium and presumably discharge excess internal water or ions.
There are two types of nuclei, micronuclei and macronuclei, either of which may be present singly or in several copies. The micronuclei are diploid, with condensed chromatin. They appear to function largely in reproduction. Sexual reproduction is common and, in some species, required for long-term survival. During sexual reproduction a cytoplasmic bridge is constructed between the two cells, and micronuclei are exchanged over this bridge. In this process, the macronuclei simply break down. The macronuclei appear to contain multiple copies of particular genes needed for day-to-day metabolic functions.
ATW041031 Text public domain. No rights reserved. Revised ATW041104.
Miozoa (= Myzozoa)
Miozoa was originally erected by Cavalier-Smith to unite Apicomplexa and Dinozoa. It seems that he is no longer happy with that name and has attempted to substitute "Myzozoa" = "sucking life." And so it does on occasion, but that's no reason to arbitrarily unseat the senior name. Consequently we retain the older name -- at least until our usual cowardice in such matters results in the more usual fawning capitulation to taxonomic fashion. Cavalier-Smith & Chao (2004: 194) characterize the taxon as "[p]redominantly haploid, typically uninucleate alveolates with zygotic meiosis; lacking separate macronuclei; ancestrally and typically with two centrioles and cilia only; anterior cilium often with simple hairs. Trichocysts typically with a dense basal rod that is square in cross section and a less dense distal region composed of hollow twisted tubules. When trichocysts are present cortical alveoli are typically inflated and morphologically discrete, often with internal plates; when trichocysts are absent they are typically highly compressed and often fused into an inner membrane complex. Myzocystosis [sic --> myzocytosis] and/or rhoptries and micronemes are very widespread, and possibly even ancestral." This is somewhat unhelpful since it is largely a description of the alternative character states of Dinozoa and Apicomplexa. In fact, of all of the characters mentioned which we can clearly identify, all are either plesiomorphic ("ancestral" -- not unique to Miozoa) or are apomorphies of included taxa (only apply to some Miozoa). No synapomorphies are identified.
ATW041031 Text public domain. No rights reserved. Revised ATW041104.
Dinozoa was originally created by Cavalier-Smith to contain the dinoflagellates and the "Protalveolata". The latter are an artificial group of misfits, such as the three genera studied by Siddall et al. (2001). Since Miozoa is indisputably a crown group, it only makes sense to treat Dinozoa and Apicomplexa as the corresponding stem groups. Thus Dinozoa = dinoflagellates > sporozoans. There is no room for a "Protalveolata," even if such a group existed. As matters stand, Perkinsus and Parvilucifera are dinozoans. Most other well-known dinozoans are traditional dinoflagellates, and these are discussed elsewhere. A variety of other strange and wonderful creatures also inhabit this phylospace which we will have to get to another day.
ATW041031 Text public domain. No rights reserved. Revised ATW041104.
Apicomplexa (= Sporozoa)
The Apicomplexa are common parasites of insects, vertebrates, and almost everything else. They are characterized by a particularly fiendish parasitic tool-kit called the apical complex (hence, of course, the name). Added to this, apicomplexans have a thick, triple outer layer which is very flexible, but nearly impervious to biological, and even to most chemical, agents. In some cases it is possible to clean out the entire cytoplasm with detergents and still recover -- more or less intact -- the reinforced membrane structure.
The outer layer of the apicomplexan cell is an ordinary(?) plasma membrane. However, this membrane is buttressed by an inner, double membrane made up of flattened alveoli sutured together. Finally, the whole business is reinforced with the cellular equivalent of rebar -- longitudinal bundles of microtubules running from the apical complex back towards the posterior end of the cell. These are cross-linked in some fashion.
The membrane is broken only by a simple cytostome consisting of an invagination of the plasma membrane. It is very similar in structure to the flagellar grooves that are occur in many other protist groups.
The components of the apical complex (rhoptries, micronemes, polar rings, the conoid, and subpellicular microtubules) are described in the appropriate glossary entries. We defer further discussion to a time when we can go beyond brief summaries. Apicomplexans have life cycles which are complex. In fact they would seem almost comical were it not for the fact that they are so efficient, and so often deadly to the host species. The basic life cycle may be said to start when an infective stage, or sporozoite, enters a host cell, and then divides repeatedly to form numerous merozonts. Some of the merozonts transform into reproductive cells, or gamonts. Gamonts join together in pairs and form a gamontocyst. Within the gamontocyst, the gamonts divide to form numerous gametes. Pairs of gametes then fuse to form zygotes, which give rise by meiosis to new sporozoites.
Motile forms of Apicomplexa crawl along the substratum in a non-amoeboid fashion known as gliding motility, which is poorly understood. Many apicomplexan species have flagellated gametes.
<==Alveolata | i. s.: Platyophrya vorax |--Myzozoa (see below for synonymy) | |--Colponema [Colponemida, Colponemidae] | | `--C. loxodes Stein 1878 | `--+--Algovora Cavalier-Smith & Chao 2004 [Algovorida, Algovoridae] | | |--*A. pugnax Cavalier-Smith & Chao 2004 | | `--A. turpis (Simpson & Patterson 1996) [=Colpodella turpis] | `--+--Voromonadida | | |--Voromonas Cavalier-Smith & Chao 2004 [Voromonadidae] | | | `--*V. pontica (Mylnikov 2000) [=Colpodella pontica] | | `--Alphamonas Aléxéieff 1918 [Alphamonadidae] | | `--*A. edax (Klebs 1892) (see below for synonymy) | `--+--Apicomplexa | | | i. s.: Isospora belli | | |--Sporozoa | | `--Apicomonadea [Apicomonada] | | |--Colpodella Cienkowski 1865 [incl. Spiromonas Perty 1852; Colpodellida] | | | |--C. angusta (Patterson & Zölfell 1991) (see below for synonymy) | | | |--C. edax [=Spiromonas edax] | | | |--C. gonderi (Foissner & Foissner 1984) [=Spiromonas gonderi] | | | |--C. pugnax Kent 1880 | | | |--C. tetrahymenae Cavalier-Smith & Chao 2004 | | | `--C. vorax (Kent 1880-1881) [=Dinomonas vorax; incl. Alphamonas coprocola] | | `--Acrocoelus [Acrocoelida] | `--+--Chilovora Cavalier-Smith & Chao 2004 [Chilovorida, Chilovoridae] | | `--*C. perforans (Hollande 1938) (see below for synonymy) | `--+--Perkinsea [Perkinsemorphina, Perkinsozoa] | | |--Perkinsus [Perkinsida] | | | |--P. atlanticus | | | `--P. marinus [=Dermocystidium marinum] | | |--Rastrimonadida | | | |--Rastrimonas Brugerolle 2003 [=Cryptophagus Brugerolle 2002 (preoc.)] | | | | `--*R. subtilis (Brugerolle 2002) [=Cryptophagus subtilis] | | | `--Parvilucifera Norén, Moestrup & Rehnstam-Holm 1999 | | | `--*P. infectans Norén, Moestrup & Rehnstam-Holm 1999 | | `--Phagodinium [Phagodinida] | `--+--Dinoflagellata | `--Ellobiopsea [Ellobiophyceae, Ellobiopsa] | |--Ellobiopsis Caullery 1910 | |--Thalassomyces Niezabitowski 1913 | |--Amallocystis Fage 1936 | |--Ellobiocystis Coutière 1911 | |--Parallobiopsis Collin 1913 | |--Rhizellobiopsis Hovasse 1926 | `--Staphylocystis Coutière 1911 `--Ciliophora [Ciliata, Gymnostomatida, Heterokaryota, Kinetophragmophora, Polyhymenophora, Tubulicorticata] | i. s.: Sathrophilus muscorum | Bryophyllidae | |--Apobryophyllum | `--Bryophyllum armatus | Cultellothrix velhoi Foissner 2003 | Fabrea salina | Glauconema trihymene | Metanophrys sinensis | Paranophrys magna | Parauronema virginianum | Pseudocohnilembus | |--P. hargisi | `--P. persalinus | Radiophrya hoplites | Vaginicola | |--V. ampulla | |--V. attenuata | `--V. ceratophylli | Carchesium limneticum | Histobalantium marinum | Sonderia | |--S. schizostoma | `--S. vorax | Thigmotrichida | |--Boveria subcylindrica [incl. B. cylindica Koehler 1924] | |--Hemispeira asteriasi | `--Hemispeiropsis antedonis (Cuénot 1891) [=Trichodina antedonis; incl. H. comatulae König 1894] | Caenomorpha | |--C. levanderi | `--C. uniserialis | Cyrtolophosis | |--C. elongata | `--C. mucicola | Drepanomonas revoluta | Leptopharynx costatus | Microdiaphanosoma arcuatum | Microthorax pusillus | Pattersoniella vitiphila | Plagiocampa rouxi | Pseudocyrtolophosis alpestris | Stammeridium kahli | Spirodinium Fiorentini 1890 | Triadinium Fiorentini 1890 | Peridinopsis James-Clark 1866 | Cothurnia oblonga | Opercularia | |--O. coarctata | `--O. protecta | Ophrydium crassicaule | Sphaerophrya soliformis | Tintinnidium fluviatile |--Intramacronucleata `--Postciliodesmatophora |--Karyorelictea `--Heterotrichea
*Alphamonas edax (Klebs 1892) [=Bodo edax, Colpodella edax; incl. Nephromonas hyalina Droop 1953]
*Chilovora perforans (Hollande 1938) [=Bodo perforans, Colpodella perforans, Spiromonas perforans]
Colpodella angusta (Patterson & Zölfell 1991) [=Dingensia angusta, Heteromita angusta, Spiromonas angusta]
Myzozoa [Colponemea, Dinozoa, Miozoa, Myzomonadea, Perkinsemorpha, Protalveolata, Spiromonadaceae, Spiromonadida, Spiromonadidae, Spiromonadidomorphina]
* Type species of generic name indicated
Amann, R. I., W. Ludwig & K.-H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews 59 (1): 143-169.
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.
Brugerolle, G. 2003. Apicomplexan parasite Cryptophagus renamed Rastrimonas gen. nov. European Journal of Protistology 39 (1): 101.
Cavalier-Smith, T. 1999. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. Journal of Eukaryotic Microbiology 46 (4): 347-366.
Cavalier-Smith, T. 2003. Protist phylogeny and the high-level classification of Protozoa. European Journal of Protistology 39 (4): 338-348.
Cavalier-Smith, T. 2004. Only six kingdoms of life. Proceedings of the Royal Society of London Series B – Biological Sciences 271: 1251-1262.
Cavalier-Smith, T., & E. E. Chao. 2004. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.) European Journal of Protistology 40: 185–212.
Curds, C. R. 1979. Group phenomena in the phylum Protozoa. In Biology and Systematics of Colonial Organisms (G. Larwood & B. R. Rosen, eds.) pp. 29-37. Academic Press: London.
Curds, C. R., & J. M. Vandyke. 1966. The feeding habits and growth rates of some freshwater ciliates found in activated-sludge plants. Journal of Applied Ecology 3: 127-137.
Detcheva, R. 1986. Ciliata interstitiels, essentiellement des sables marins. In Stygofauna Mundi: A Faunistic, Distributional, and Ecological Synthesis of the World Fauna inhabiting Subterranean Waters (including the Marine Interstitial) (L. Botosaneanu, ed.) pp. 21-29. E. J. Brill / Dr. W. Backhuys: Leiden.
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.
Foissner, W. 2003a. The Myriokaryonidae fam. n., a new family of spathidiid ciliates (Ciliophora: Gymnostomatea). Acta Protozoologica 42: 113-143.
Foissner, W. 2003b. Two remarkable soil spathidiids (Ciliophora: Haptorida), Arcuospathidium pachyoplites sp. n. and Spathidium faurefremieti nom. n. Acta Protozoologica 42: 145-159.
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.
Hackstein, J. H. P., A. Akhmanova, F. Voncken, A. van Hoek, T. van Alen, B. Boxma, S. Y. Moon-van der Staay, G. van der Staay, J. Leunissen, M. Huynen, J. Rosenberg & M. Veenhuis. 2001. Hydrogenosomes: Convergent adaptations of mitochondria to anaerobic environments. Zoology 104: 290-302.
Krylov, M. V. 1992. The origin of heteroxeny in Sporozoa. Parazitologiya 26 (5): 361-368.
Leander, B. S., R. E. Clopton & P. J. Keeling. 2003. Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and β-tubulin. International Journal of Systematic and Evolutionary Microbiology 53: 345-354.
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.
Ma, H., J. K. Choi & W. Song. 2003. An improved silver carbonate impregnation for marine ciliated protozoa. Acta Protozoologica 42: 161-164.
Nichols, G. L. 2000. Food-borne protozoa. British Medical Bulletin 56 (1): 209-235.
Norén, F., Ø. Moestrup & A.-S. Rehnstam-Holm. 1999. Parvilucifera infectans Norén et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): A parasitic flagellate capable of killing toxic microalgae. European Journal of Protistology 35: 233-254.
Okamoto, N., & I. Inouye. 2005. The katablepharids are a distant sister group of the Cryptophyta: A proposal for Katablepharidophyta divisio nova / Kathablepharida phylum novum based on SSU rDNA and beta-tubulin phylogeny. Protist 156: 163-179.
Saldarriaga, J. F., M. L. McEwan, N. M. Fast, F. J. R. Taylor & P. J. Keeling. 2003. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology 53: 355-365.
Siddall, M. E., K. S. Reece, T. A. Nerad & E. M. Burreson. 2001. Molecular determination of the phylogenetic position of a species in the genus Colpodella (Alveolata). American Museum Novitates 3314, 10pp.
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.
ATW041102. Text and image public domain. No rights reserved. Revised ATW041104. Phylogeny and some references Christopher 01:23, 11 October 2009 (UTC).