The Model Tetrahymenidans

Ciliates have long been one of the most (if not the most) confidently recognised groups of unicellular eukaryotes owing to their distinctive array of features, in particular locomotion by means of more or less dense tracts of small cilia that often run the length of the organism. And of all ciliates, perhaps none have been more extensively studied than species of the genus Tetrahymena such as T. thermophila. Being easily cultured in the laboratory, Tetrahymena species have become model organisms for the study of a great many genetic and cellular systems such as cell division and gene function. At least two Nobel prizes have been awarded for work based on Tetrahymena that established the functions of telomeres and ribozymes. But Tetrahymena is just one genus of larger group of ciliates, the Tetrahymenida.

Tetrahymena thermophila, from Robinson 2006.

In general, tetrahymenidans are more or less 'typical'-looking ciliates with an ovoid body form and a well-developed 'mouth' at one end. The name Tetrahymena, meaning 'four membranes', refers to the presence of four membrane-like structures inside the oral cavity, a larger, ciliated undulating membrane on the left and three membranelles (formed from polykinetids, complex arrays of cilia and associated basal bodies and fibrils). Most tetrahymenidans possess some variation of this arrangement with the exception of Curimostoma, a genus of parasites of freshwater flatworms and molluscs that lack oral structures (Lynn & Small 2002). Life cycles may contain a number of morphologically differentiated stages. A more mobile theront stage will seek out food sources then transform into a feeding trophont. Mature trophonts may divide asexually or reproduce through conjugation. Cellular multiplication often involves successive divisions so a single parent cell may give rise to four daughter cells. In a number of species, resistant resting cysts may form under adverse conditions.

Glaucoma scintillans, another well-studied tetrahymenidan, copyright Proyecto Agua.

Tetrahymenidans are also ecologically diverse, occupying a range of freshwater habitats. They may be free-living, feeding on bacteria, or they may be parasitic or histophagous, feeding on the tissues of invertebrates. Some species may switch between one or the other depending on circumstances. A few Tetrahymena species have even been cultured in the laboratory axenically: that is, absorbing nutrients directly from a culture broth without requiring a bacterial food supply. Recently, the first confirmed case of a tetrahymenidan containing endosymbiotic algae was described by Pitsch et al. (2016). The species Tetrahymena utriculariae inhabits the bladders of the carnivorous bladderwort Utricularia reflexa. Endosymbiotic green algae provide it with oxygen, allowing the ciliate to survive within the anoxic environment of the bladders.

REFERENCES

Lynn, D. H., & E. B. Small. 2002. Phylum Ciliophora Doflein, 1901. In: Lee, J. J., G. F. Leedale & P. Bradbury (eds) An Illustrated Guide to the Protozoa: Organisms traditionally referred to as Protozoa, or newly discovered groups 2^nd ed. vol. 1 pp. 371–656. Society of Protozoologists: Lawrence (Kansas).

Pitsch, G., L. Adamec, S. Dirren, F. Nitsche, K. Šimek, D. Sirová & T. Posch. 2016. The green Tetrahymena utriculariae n. sp. (Ciliophora, Oligohymenophorea) with its endosymbiotic algae (Micractinium sp.), living in traps of a carnivorous aquatic plant. Journal of Eukaryotic Microbiology 64: 322–335.

Let's You and Me Enter Syzygy

Finally, you and your beloved are together. For the two of you, there are no others; all the world is yours alone. You gaze into each other's eyes, and then you pull your beloved into an embrace. Your lips touch in a passionate kiss. Your arms and legs intertwine in a firm hold. As you press so close to one another, it almost feels like you can no longer tell where the dividing line is between you. The excitement builds, and then... the two of you explode, each dissolving into a cascading avalanche of twitching gobbets of flesh.

Life cycle of Lecudina, from Clopton (2002).

This, roughly, is syzygy, a key event in the life cycle of many of the invertebrate-gut-parasitising protists known as eugregarines. Originally, the term 'syzygy' referred to the conjunction of two heavenly bodies, and provides a very poetic label for the process by which two of these unicellular organisms conjoin, rotating around one another as they produce and outer membrane to contain themselves within a single gametocyst. Once within the gametocyst, each divides into numerous gametes (which are produced through straight mitotic division, as eugregarines are haploid at maturity rather than diploid like ourselves). The resulting gametes will then be released from the gametocyst to fuse with one another in the production of diploid zygotes. Each zygote encloses itself in a resistant oocyst, in which state it may be passed out of the host's digestive system and be swallowed by a new host. While within the oocyst, the zygote divides to produce a number of new haploid individuals. Once the oocyst is in a suitable host, the new eugregarines are released, ready to feed and hopefully to eventually find a syzygy of their own.

Mature individuals of Blabericola in association, copyright R. E. Clopton.

Eugregarines have been referred to at this site before. As described in that post, they are part of the group of protists known as gregarines. Eugregarines differ from the other two major subgroups of gregarines, the archigregarines and neogregarines, in that they do not include an extensive asexually reproducing phase in their life cycle in addition to the sexual phase. All known eugregarines are parasites of invertebrates: their hosts include arthropods, molluscs, annelids and tunicates. Most eugregarines parasitise only a single host species over the course of their life cycle. The only known exception is members of the family Porosporidae, which are believed to spend part of their life cycle in a crustacean, and part in a mollusc. However, the porosporid life cycle has only been observed in its entirety once in 1940, when H. F. Prytherch fed infective spores from an oyster to crabs. It has been suggested that Prytherch may have conflated two separate parasites, with the eugregarine infection observed in the crabs after feeding them the spores actually representing a pre-existing infection that they had been carrying before the start of the experiment (Clopton 2002).

Individual of Schneideria quadrinotatus, from Clopton (2002); scale bar = 100 µm. Offhand, I can't be the only one who can't help seeing the nuclei in these sort of drawings as eyes. And for some reason, they always seem to look a bit wistful.

The eugregarines are usually divided between three suborders. Two of these, the Septatorina and Aseptatorina, include the great majority of species and are distinguished (as their names suggest) by the presence or absence of septae dividing the cell into sections. The third suborder includes the single small genus Siedlickia, parasites of marine annelids, which differs from other eugregarines in that it does not go through syzygy; instead, reproductive cells are budded directly off the mature feeding cells. The relationships between the three suborders are largely unknown; the Aseptatorina in particular seems to be defined largely by plesiomorphies. Clopton (2009) argued for a marine ancestry of eugregarines as a whole, and that the radiation of the septate eugregarines had been driven by adaptations of the gametocyst allowing their transmission in freshwater and terrestrial habitats. However, both the aseptate and septate eugregarines include parasites of marine, freshwater and terrestrial hosts. The fact that Clopton did not refer in 2009 to the marine members of the Septatorina (in the Porosporidae and various families of the Gregarinoidea) is somewhat bemusing as he himself had reviewed them some years earlier in his 2002 chapter on the eugregarines for The Illustrated Guide to the Protozoa. It is possible that he simply assumed the marine species to sit outside the terrestrial-freshwater clade, but it would have been nice for hime to say so.

Multiple syzygy in Hyalospora roscoviana, from Clopton (2002). The one in front doesn't look like it was quite expecting this.

Ignorance of the marine eugregarines does seem to be a theme, though: they're definitely less well-studied than the parasites of terrestrial species. Not that the latter can claim to have been exhaustively studied either: as noted by Clopton (2002), while over 1600 species of eugregarine have been described, only a fraction (much less than one percent) of potential hosts have been investigated for their presence. As almost every investigation of a new host results in the description of new parasite species, it is possible that the total number of eugregarine species out there ranks in the millions. Eugregarines are morphologically and behaviourally diverse. Attachment to the cells of the host's intestinal lining is via a structure called the epimerite, which may be a simple nubbin or may be a complex branching, fingered, collared or dart-like structure. When not attached to the host cell, most eugregarines move by gliding, but the worm-like Selenidiidae move by nondirectional swinging or thrashing. Many taxa are all distinguished by the characteristics of their syzygy. They may connect end to end, or they may lie top-to-tail. Members of the septate superfamily Gregarinoidea form associations some time before entering actual syzygy, so they are often found connected (whereas other taxa that do not become conjoined until the point of syzygy are more often found as isolated cells). Syzygy is most often between two individuals, but some Gregarinoidea regularly form associations of three or more. At least one species, Hirmocystis polymorpha, has been found in head-to-tail chains of up to twelve individuals. Whether such polygamous associations lead to all the individuals involved combining to form one gametocyst, or whether some form of competition occurs to whittle them down to a single victorious pair, is something I haven't yet discovered.

REFERENCES

Clopton, R. E. 2002. Order Eugregarinorida Léger, 1900. In: Lee, J. J., G. Leedale, D. Patterson & P. C. Bradbury (eds) Illustrated Guide to the Protozoa, 2nd ed., vol. 1 pp. 205–288. Society of Protozoologists: Lawrence (Kansas).

Clopton, R. E. 2009. Phylogenetic relationships, evolution, and systematic revision of the septate gregarines (Apicomplexa: Eugregarinorida: Septatorina). Comp. Parasitol. 76 (2): 167–190.

Ceratium...er...Neoceratium...er...Tripos humilis

The dinoflagellate formerly known as Ceratium humile, from here.

Ceratium has long been a popular choice as a representative dinoflagellate genus for textbooks, because as micro-organisms go, they're fairly specky. The theca of Ceratium is characterised by protruding horns, with an elongate anterior horn and one to three posterior horns. The posterior horns may be directed back from the theca, or they may curve around towards the front to produce an anchor-like shape. These horns increase the cell's buoyancy, though they do make them fairly slow swimmers. The concept of Ceratium has been fairly stable since the early 1800s, but Gómez et al. (2010) found when conducting a molecular analysis of a number of 'Ceratium' species that there was a deep divide between freshwater and marine Ceratium species. As well as the molecular divide, there is also a morphological difference: freshwater species have six plates around the cingulum (the groove around the theca body in which sits one of the flagella), while marine species have five cingular plates. As a result, Gómez et al. proposed dividing the two clades between two genera, with the name Ceratium being restricted to the freshwater species. The marine species were all transferred into a new genus Neoceratium. However, Gómez (2013) later recognised that there were a number of older generic names floating about that had been given to marine taxa, and the marine species were moved again into a resurrected genus Tripos. Among the taxa affected by this double transfer was the species shown in the photo above, now known as Tripos humilis.

There are a large number of anchor-shaped Tripos species, and distinguishing them is apparently a difficult process. Tripos humilis has the anterior part of the theca in front of the cingulum (excluding the anterior horn) fairly low, the upper surface of the theca (i.e. the side away from the origin of the flagella) strongly convex, and the right-hand posterior horn much longer than the left, with the right horn tending to converge towards the anterior horn while the left horn diverges (Subrahmanyan 1968). The cingulum is also distinctly angled relative to the posterior margin of the theca. While other Tripos species are found in a range of habitats, T. humilis appears to be a more specifically tropical species. It is found pantropically, though seemingly nowhere abundantly.

Chain of Tripos, from here.

Dinoflagellates can sometimes form long chains when dividing individuals don't fully separate but continue to multiply. In Ceratium and Tripos species, the members of a chain remain connected through the apical horns. Chaining individuals may be somewhat morphologically distinct from isolated individuals; in T. humilis, the horns of chained individuals are relatively much shorter. Chains are apparently commoner when dinoflagellates form 'red tides' or algal blooms, and one suggested function is that a chain is able to swim faster overall than an individual, improving the dinoflagellates' ability to compete when moving to occupy suitable places in the water column for light or food.

REFERENCES

Gómez, F. 2013. Reinstatement of the dinoflagellate genus Tripos to replace Neoceratium, marine species of Ceratium (Dinophyceae, Alveolata). CICIMAR Oceánides 28(1): 1-22.

Gómez, F., D. Moreira & P. López-García. 2010. Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 161: 35-54.

Subrahmanyan, R. 1968. The Dinophyceae of the Indian Seas. Part I. Genus Ceratium Schrank. Marine Biological Association of India, Memoir 2: 1-129.

Glenodinium and the Horseshoe of Light

Yes, it's another dinoflagellate. The subject of the above photo (from here) is Glenodinium pulvisculus. Glenodinium is a genus of photosynthetic, mostly freshwater dinoflagellates in the family Glenodiniaceae, diagnosed by Fensome et al. (1983) by the possession of four apical plates and six postcingular plates (see near the top of this post for a brief explanation of these terms). Fensome et al. included two genera in this family, Glenodinium and Glenodiniopsis. Glenodinium has a horseshoe-shaped eyespot, but Glenodiniopsis does not. The eye-spot presumably functions in phototaxis, though it is worth noting that Glenodiniopsis is positively phototactic even without one (Highfill & Pfiester 1992).

Glenodiniopsis uliginosa, from here.

The identity of Glenodinium has been somewhat confused over the years, due in part to confusion over the identity of its type species, G. cinctum (Loeblich 1980). As a result, many of the references to Glenodinium in the literature refer to unrelated species, while true Glenodinium appears relatively little-studied. One species of Glenodiniopsis, G. steinii, has fared a little better, and its ultrastructure was described in detail by Highfill & Pfiester (1992). Among the more interesting details they noted was that instead of the multiple chloroplasts this species had originally been described as having, it really possesses a single chloroplast but one with multiple lobes, so that if it is viewed in cross-section the lobes might appear as individual plastids.

REFERENCES

Fensome, R. A., F. J. R. Taylor, G. Norris, W. A. S. Sarjeant, D. I. Wharton & G. L. Williams. 1983. A classification of living and fossil dinoflagellates. Micropaleontology Special Publication 7.

Highfill, J. F., & L. A. Pfiester. 1992. The ultrastructure of Glenodiniopsis steinii (Dinophyceae). American Journal of Botany 79 (10): 1162-1170.

Loeblich, A. R., III. 1980. Dinoflagellate nomenclature. Taxon 29 (2-3): 321-324.

The State of Peridinium

As I've said on many an occasion before, dinoflagellates are complicated. Obscenely complicated. So when my search for a random post topic brought up the dinoflagellate genus Peridinium, I approached it with a certain amount of dread. If you're not familiar with dinoflagellates, the diagram at the top of this post will explain a lot of the terminology I'm about to use.

Specimen of Peridinium cf. cinctum, photographed by Kate Howell. Peridinium cinctum is the type species of Peridinium.

Peridinium is a genus that has been used in the past to cover a wide range of freshwater and marine dinoflagellates. For a long time, the standard diagnosis of Peridinium was that it contained species with four apical plates (the ring of plates at the front of the cell when it is moving), seven precingular plates (the ring of plates in front of the cingulum), five postcingular plates and two antapical plates (Carty 2008). However, the genus has been divided by differences in the shape and arrangements of the plates making up the theca into a number of species groups, and more recent studies have concurred that these species groups are not all closely related to each other. While support remains low in most phylogenetic studies of dinoflagellates, and many species remain to be analysed, indications are that all of the marine species and many of the freshwater species are not true Peridinium (Horiguchi & Takano 2006; Logares et al. 2007). As it currently stands, the probably monophyletic Peridinium sensu stricto includes two species groups, the P. cinctum and P. willei groups, and is exclusively freshwater. As well as the characters mentioned above, true Peridinium species have three apical intercalary plates between the apical and precingular plates, five cingular plates, and ridges on all the plates forming an areolate pattern. They are also united by a distinct combination of which plates in the front section of the organism break off when the theca is shed during cell division (Craveiro et al. 2009). The two species groups differ in the exact arrangement of the plates anterior to the cingulum: in the P. willei group they are symmetrical relative to the dorsal-ventral axis, vs asymmetrical in the P. cinctum group. Slightly surprisingly, though the presence or absence of an apical pore was one of the first characters used to subdivide the genus Peridinium, Peridinium sensu stricto includes both species with (such as P. bipes) and without (such as P. cinctum and P. willei).

SEM image of Peridinium gatunense, by Pawel Owsiany.

Peridinium species are photosynthetic, with a much-lobed chloroplast that ramifies through the cell. One species, identified by Hickel & Pollingher (1988) as P. gatunense, has been intensely studied as the creator of annual blooms in Lake Kinneret in Israel.

REFERENCES

Carty, S. 2008. Parvodinium gen. nov. for the Umbonatum Group of Peridinium (Dinophyceae). Ohio Journal of Science 108 (5): 103-107.

Craveiro, S. C., A. J. Calado, N. Daugbjerg & Ø. Moestrup. 2009. Ultrastructure and LSU rDNA-based revision of Peridinium group Palatinum (Dinophyceae) with the description of Palatinus gen. nov. Journal of Phycology 45: 1175-1194.

Hickel, B., & U. Pollingher. 1988 Identification of the bloom-forming Peridinium from Lake Kinneret (Israel) as P. gatunense (Dinophyceae). British Phycological Journal 23 (2): 115-119.

Horiguchi, T., & Y. Takano. 2006. Serial replacement of a diatom endosymbiont in the marine dinoflagellate Peridinium quinquecorne (Peridiniales, Dinophyceae). Phycological Research 54: 193-200.

Logares, R., K. Shalchian-Tabrizi, A. Boltovskoy & K. Rengefors. 2007. Extensive dinoflagellate phylogenies indicate infrequent marine–freshwater transitions. Molecular Phylogenetics and Evolution 45 (3): 887-903.

Taxon of the Week: Protoperidinium grande

I can't really award anyone the prize for identifying yesterday's image; identifying it as a "dinoflagellate" doesn't really cut the mustard considering how many thousands of dinoflagellate species are known.


Protoperidinium grande. From Steidinger & Williams (1970).

Many references describe dinoflagellates as photosynthetic; this is wrong, in the same way as describing mosquitoes as feeding on blood is wrong. In terms of number of species, there are probably more non-photosynthetic than photosynthetic dinoflagellates. Protoperidinium is a genus of more than 200 species of mostly non-photosynthetic marine dinoflagellates, many of which possess a single apical horn and two antapical horns as seen in the photo above. Features distinguishing P. grande include the reticulate theca and the compressed cingular area (the cingulum is the groove around the midline; one of the dinoflagellate's two flagella wraps around the cingulum). Unlike some other Protoperidinium species, P. grande does not produce resting cysts; as a result, it is found only in warmer waters around the world. As non-photosynthetic heterotrophs, Protoperidinium species obtain their nutrition by feeding on other micro-organisms such as diatoms, cyanobacteria or other dinoflagellates. Rather than directly engulfing their prey in the way of an amoeba, Protoperidinium extend a large pseudopodial extension called a pallium from their theca's antapical pole to envelop it. The food organism is digested by the pallium, which is then withdrawn back into the dinoflagellate theca carrying a load of nutrients with it. This feeding behaviour was first 'discovered' in the late 1990s, but ironically it had actually been illustrated as long ago as 1895 with later researchers failing to recognise earlier records for what they were (Jacobson 1999*).

*Jacobson's comment on this re-discovery are worth repeating: "the brilliant, detailed observations of Kofoid and Swezy, Schütt, and Biecheler remain a humbling reminder to those of us working in a highly capitalized, high-tech environment that important work can arise from a simple light microscope, coupled with patience, luck and the appropriate search image".


Protoperidinium depressum feeding on diatoms. Figure from Jacobson (1999).

Until relatively recently, Protoperidinium species were included in the genus Peridinium along with a number of freshwater dinoflagellates. The taxonomy of Recent dinoflagellates* has traditionally been dominated by a small number of what might be termed 'super-genera' of hundreds of species that between them encompass the great majority of living taxa. It is probably not surprising that phylogenetic analyses have suggested that many of these super-genera are polyphyletic, but most of those analyses have tended to return very poorly supported results and attempts to subdivide the super-genera have not been entirely successful. The division of Peridinium is one of the more successful examples, based on ecology (Peridinium sensu stricto is freshwater, Protoperidinium is marine), fine details of the arrangement of plates in the theca (Peridinium has five plates around the cingulum; Protoperidinium has four) and the features of cysts produced in some species (Dale, 1978). Molecular analyses have supported the monophyly of Protoperidinium (Yamaguchi & Horiguchi, 2005). The division on ecological grounds has been a common pattern in studies on protists; molecular analyses of a number of other micro-eukaryotic groups such as myxozoans have also produced results that contradict traditional morphological classifications but correlate strongly with ecological features.

*The taxonomy of fossil dinoflagellates is an entirely separate pot of evil.

REFERENCES

Dale, B. 1978. Acritarchous cysts of Peridinium faeroense Paulsen: implications for dinoflagellate systematics. Palynology 2: 187-193.

Jacobson, D. M. 1999. A brief history of dinoflagellate feeding research. Journal of Eukaryotic Microbiology 46 (4): 376-381.

Steidinger, K. A., & J. Williams. 1970. Dinoflagellates. Memoirs of the Hourglass Cruises 2: 1-251.

Yamaguchi, A., & T. Horiguchi. 2005. Molecular phylogenetic study of the heterotrophic dinoflagellate genus Protoperidinium (Dinophyceae) inferred from small subunit rRNA gene sequences. Phycological Research 53 (1): 30-42.

The Schizosphere (Taxon of the Week: Schizosphaerella)

Micrographs of Schizosphaerella from Perch-Nielsen (1989).

The dead are all around us. Large parts of the world's surface are made up by the remains of long-gone marine organisms who left their shells and skeletons, initially constructed for protection from predators and the elements, to form gigantic sedimentary graveyards. Over time, as with everything else, the identities of these unwitting benefactors have changed as new groups supplant the old.

During the Jurassic period, the predominant groups of biomineralising plankton were the calcareous coccoliths and Schizosphaerella (radiolarians were present but only important under certain conditions, planktic foraminiferans would not appear until the Cretaceous, while diatoms appeared in the Jurassic but remained marginalised until during the Cenozoic - Erba, 2004). Of these two, Schizosphaerella was particularly significant; at times, it accounted for nearly 100% of plankton-derived carbonate deposition (Mailliot et al., 2007). Schizosphaerella left its remains from the late Triassic to the end of the Jurassic in the form of globular to bell-shaped resting cysts, five to 30 μm in diameter, known as schizospheres. These are composed of two roughly hemispherical plates joined by a simple hinge. The two recognised species, S. punctulata and S. astraea, are distinguished by the presence or absence, respectively, of a subperipheral groove around the hinge and by the lattice arrangement of the elongate radiating elements that make up the wall (Perch-Nielsen, 1989). The nature of the Schizosphaerella organism during the active parts of its life cycle (assuming that the fossils are cysts) are unknown, as are its relationships to other organisms. The most common suggestion is that it represents some form of dinoflagellate - calcareous cysts are definitely produced by dinoflagellates of the subfamily Calciodinelloideae. However, Streng et al. (2004) have pointed out that the two-plated hinge arrangement of Schizosphaerella is unlike that known for any dinoflagellate, whose cysts normally open through an archeopyle at one end. That micropalaeontology is littered with examples of taxa of uncertain relationships (becoming more so the further back one goes in time) should come as no surprise to anyone - after all, it is often difficult enough to work out the relationships of modern unicellular organisms on morphological grounds, and doing so is often dependent on features of cell ultrastructure that are unlikely to be preserved in fossils.

Mention should also be made of the nannofossil Stomiosphaera minutissima which was described as having a calcareous cell wall of two layers - a thin inner layer and an outer layer composed of radiating fibres. 'Stomiosphaera' was shown by Aubry et al. (1988) to be the same as Schizosphaerella, but diagenetically altered (diagenesis is the process by which the nature of a fossil can be altered by geological processes after it gets deposited). The inner layer represented the two plates of the original fossil fused together while the outer layer resulted from crystal formation around the fossil.


Mean Schizosphaerella size over time compared to levels of carbonate production, from Mattioli et al. (2009).

Schizosphaerella seems to have preferred oligotrophic conditions with a deep nutricline (i.e. nutrients in the sea were spread out rather than being concentrated near the surface). An inverse relationship existed between Schizosphaerella and coccolith abundance (Cobianchi & Picotti, 2001) that was also related to the concentration of organic carbon in the water - high organic carbon (i.e. eutrophic conditions) meant more coccoliths and fewer schizospheres, low organic carbon the reverse. Periods of schizosphere abundance also relate to higher sea levels as reduced land level meant reduced organic run-off into the oceans. Both calcareous groups, however, showed reductions during periods of elevated CO₂ levels that punctuated the Mesozoic. The Toarcian anoxic event in the early Jurassic seems to have resulted from extensive vulcanism in southern Africa; the mean size of schizospheres becomes much smaller during this period as calcification became reduced by higher ocean acidity (Mattioli et al., 2009). This reduction in calcification is correlated with the extinction of a number of other organisms. Study of such past events is the best means available to us of understanding the effects that elevated carbon dioxide levels could potentially have in our own time (see, palaeontology can be practical too!).

REFERENCES

Aubry, M.-P., F. Depêche & T. Dufour. 1988. Stomiosphaera minutissima (Colom, 1935) from the Lias of Mallorca (Balearic Islands) and Umbria (Italy), and Schizosphaerella punctulata Deflandre & Dangeard, 1938: taxonomic revision. Geobios 21 (6): 709-727.

Cobianchi, M., & V. Picotti. 2001. Sedimentary and biological response to sea-level and palaeoceanographic changes of a Lower–Middle Jurassic Tethyan platform margin (Southern Alps, Italy). Palaeogeography, Palaeoclimatology, Palaeoecology 169 (3-4): 219-244.

Erba, E. 2004. Calcareous nannofossils and Mesozoic oceanic anoxic events. Marine Micropaleontology 52: 85-106.

Mailliot, S., S. Elmi, E. Mattioli & B. Pittet. 2007. Calcareous nannofossil assemblages across the Pliensbachian/Toarcian boundary at the Peniche section (Ponta do Trovão, Lusitanian Basin). Ciencias da Terra (UNL) 16: 1-13.

Mattioli, E., B. Pittet, L. Petitpierre & S. Mailliot. 2009. Dramatic decrease of pelagic carbonate production by nannoplankton across the Early Toarcian anoxic event (T-OAE). Global and Planetary Change 65 (3-4): 134-145.

Perch-Nielsen, K. 1989. Mesozoic calcareous nannofossils. In Plankton Stratigraphy vol. 1. Planktic foraminifera, calcareous nannofossils and calpionellids (H. M. Bolli, J. B. Saunders & K. Perch-Nielsen, eds) pp. 329-426. Cambridge University Press.

Streng, M., T. Hildebrand-Habel & H. Willems. 2004. A proposed classification of archeopyle types in calcareous dinoflagellate cysts. Journal of Paleontology 78 (3): 456-483.

Like, Wow. Just... Wow.

This is something I saw this morning at Small Things Considered, that I thought was just so spectacularly brilliant that I just had to copy it:



One hundred and sixty-seven species of ciliate, artfully arranged and all drawn to scale, from the gigantic Stentor to the sinuous Homalozoon to the infinitesimal Cinetochilum. The image comes from here, where not only can you see it in its full glory, but you'll find the key to the numbering that tells you what each one of these marvels is. The species are partially arranged in line with their chosen habitats - those towards the top left are found in the open water column in lakes, those around the centre of the bottom are anaerobes, while the others make their homes among sediment. And there's even little extra bits of detail hidden within - see if you can find the Chilodonella crawling along the Epistylis stalk, for instance. Enjoy!

Then if you're in the mood for more details on ciliates, including comments on their mind-blowingly complicated genetic system, take a look at my earlier posts here and here. And if anyone is feeling really generous and wants to get this printed out as a wall poster for me...

Of Gregarines

An assortment of lecudinid eugregarines. The front end of the cell is towards the lower left in each individual. Image from Leander (2007) via Brian S. Leander.

The Sporozoa are perhaps the most famous group of protozoan parasites. As well as being one of the few protozoan groups distinctive enough to be well-characterised prior to the advent of electron microscopy and molecular analysis (albeit with a few hangers-on such as microsporidians and myxozoans that have since been cast aside from the sporozoan community), distinguished by their lack of motile organelles and intracellular invasion of their hosts, sporozoans include the causative agents of such maladies as malaria and toxoplasmosis. In many references, you may find the Sporozoa referred to as Apicomplexa, a name that refers to the apical complex, an organelle at the front end of the cell that is used to invade the cells of the sporozoan's host. However, as the apical complex is also found in some flagellates that are closely related to sporozoans (such as Colpodella), the name Apicomplexa is better used for the larger clade including these taxa while the name Sporozoa is restricted to the nested aflagellate clade (Cavalier-Smith & Chao, 2004).

Sporozoans have been divided into three classes, the invertebrate parasites Gregarinae (or Gregarinea), Coccidia (intestinal parasites of vertebrates) and Hematozoa (parasites of vertebrate blood cells). Phylogenetic analyses have indicated that the basal division in Sporozoa is between the vertebrate-parasitic Coccidia and Hematozoa on one branch (the Coccidiomorpha), and the Gregarinae on the other, though the Gregarinae is less well supported as monophyletic than the Coccidiomorpha and may yet be paraphyletic (Leander & Ramey, 2006; Leander et al., 2006). One notable exception is that the vertebrate parasite Cryptosporidium, previously regarded as a coccidian, may in fact be related to the gregarines or even derived from within them. Not surprisingly, their choice of hosts means that the Coccidiomorpha are by far the better studied of the two clades, while the Gregarinae have kind of been the poor relation. Nevertheless, it is the gregarines that are my focus today.

Gregarines have been divided into three groups, the archigregarines, eugregarines and neogregarines (Leander, 2007), but it seems more than likely that these represent a series of grades, with eugregarines paraphyletic to neogregarines and archigregarines paraphyletic to the eugregarine + neogregarine clade. In contrast to the complex life-cycles of some coccidiomorphs, gregarines have fairly simple life histories with only a single host. Transmission from one host to another is usually via oocysts released with the host faecal matter, but some gregarine oocysts hitch a ride with their host's gametes during copulation as protozoan STDs. Once inside the host, the oocysts hatch out into infective sporozoites that attach to or invade host cells and develop into feeding trophozoites. Some gregarines can reproduce asexually; the majority cannot. Sexual reproduction occurs by two trophozoites joining together as reproductive gamonts and becoming enclosed within a gametocyst; within the gametocyst they will each divide into hundreds of gametes that will fuse to form oocysts, ready for release.


Selenidium sp., showing the wriggling movement. From Leander (2007).

As I said before, the "archigregarines" probably represent the basal grade of gregarines. They are all intestinal parasites of marine invertebrates, and as such have been unfairly condemned as of little interest to anyone. Archigregarines have very similar sporozoites and trophozoites that are vermiform (worm-shaped) and generally move by wriggling (go here for videos of gregarine movement). Some archigregarines have cells with numerous longitudinal folds, others are smooth. Archigregarines also retain the ancestral characteristic of feeding on their host by using their apical complex to pierce the host cell and sucking out its contents.

The 'eugregarines' include the majority of gregarines (at least, the majority of described gregarines), and include parasites of freshwater and terrestrial as well as marine invertebrates. Again, their study has been biased towards those species that are parasites of insects, with the remainder being generally snubbed. Most marine eugregarines have been lumped together as the genus 'Lecudina', with little to unite them other than that they are marine eugregarines (Leander, 2007). Eugregarines differ from archigregarines in having morphologically quite distinct sporozoites and trophozoites. Their cell walls also became very rigid, and they lost the wriggling ability of archigregarines. Instead, eugregarines developed a system of gliding motility, with an actinomyosin skeleton running along the edge of the numerous surface folds. Ancestrally, eugregarines are intestinal parasites like archigregarines, but instead of the active feeding process of eugregarines, eugregarines absorb nutrients from the host through micropores on the cell surface (Leander et al., 2006).


Two conjoined gamonts of the polychaete coelom parasite Pterospora floridiensis. From Leander (2007).

Neogregarines are a derived subgroup of eugregarines with reduced trophozoites that specialise on terrestrial hosts (mostly insects) and mostly live in non-intestinal tissues. Another group of eugregarines, the urosporidians, became parasites of their host's coelom. Urosporidians lost their direct attachment to host cells, and became free-floating within the tissue as united gamont pairs. The gliding motility and longitudinal folds of other eugregarines were lost, and instead urosporidians move by pulsations of the cell walls. Cells became branched - many are V-shaped with two primary branches that each divide distally into a number of smaller "fingers".

Archigregarines in particular retain a number of features that are believed to be ancestral for sporozoans as a whole (such as sucking feeding), and Leander et al. (2006) suggest that they may constitute the ancestral group not just for eugregarines, but also for coccidiomorphs and hence sporozoans as a whole. Interestingly, gregarines (including archigregarines), so far as is known, lack the residual plastid found in coccidiomorphs. It is currently a subject of some debate as to whether the sporozoan (really coccidiomorph) plastid is homologous with that found in the related dinoflagellates or not (see here for an earlier take of mine on the issue), and the position of the plastid-less 'archigregarines' could have significant implications for this debate.

REFERENCES

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.

Leander, B. S. 2007. Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends in Parasitology 24 (2): 60-67.

Leander, B. S., S. A. J. Lloyd, W. Marshall & S. C. Landers. 2006. Phylogeny of marine gregarines (Apicomplexa) — Pterospora, Lithocystis and Lankesteria — and the origin(s) of coelomic parasitism. Protist 157: 45-60.

Leander, B. S., & P. A. Ramey. 2006. Cellular identity of a novel small subunit rDNA sequence clade of apicomplexans: description of the marine parasite Rhytidocystis polygordiae n. sp. (host: Polygordius sp., Polychaeta). Journal of Eukaryotic Microbiology 53 (4): 280-291.

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.

Another Non-missing Not-quite-link

Today's Nature has a significant article that I'd like to draw your attention to, but before I do I've got a complaint to make. One of the letters in today's Nature (Seeber, 2008) addresses the question of citations in online Supplementary Information. I've moaned before about the problems with online Supplementary Information for papers - most notably the issue of it becoming unavailable over time - and Seeber's letter gives me one more reason to dislike SI. Apparently, the various sources of citation rankings such as impact factors don't include citations that only appear in Supplementary Info. What really gets my goat, though, is that the editor of Nature states in a replying note that, "Supplementary information for Nature... does not usually contain references". This is simply not true.

The Supplementary Information for the paper I'm about to write on has a bibliography of 53 references. Saarela et al. (2007) included 13 supplementary references, as did Xu et al. (2007). Brandt et al. (2007) had 62. The SI for Bininda-Emonds et al. (2007) has 75 references. In fact, I haven't often seen a Supplementary Information file that hasn't included extra references, so if Nature has a policy of discouraging supplementary references, they're not doing a very good job of enforcing it.

Now that that little gripe is over and done with, on to the good stuff:



Moore, R.B., M. Oborník, J. Janouškovec, T. Chrudimský, M. Vancová, D. H. Green, S. W. Wright, N. W. Davies, C. J. Bolch, K. Heimann, J. Šlapeta, O. Hoegh-Guldberg, J. M. Logsdon & D. A. Carter. 2008. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451 (7181): 959-963. DOI: 10.1038/nature06635

After years of ignorance, we are slowly piecing together an understanding of the inter-relationships between the various groups of eukaryotes. In the process of doing so, researchers have confirmed some traditionally recognised groups, dismantled others, and recognised new groupings that were previously unsuspected. One well-supported group of protists that has emerged into the light is the Alveolata. Alveolates combine three superficially dissimilar groups - the ciliates, dinoflagellates and sporozoans - united by the possession of alveoli, flattened membrane-bound vesicles directly under the cell surface, supported by microtubules. Within the alveolates, it is also generally agreed that the dinoflagellates and sporozoans are more closely related to each other than to the ciliates.

The sporozoans are parasitic forms that include a number of significant pathogens such as Plasmodium, the cause of malaria, and Cryptosporidium. One of the interesting, relatively recent discoveries about this group of organisms was that some of them possess a remnant, colourless plastid (referred to as the apicoplast), which together with the presence of chloroplasts in the related dinoflagellates suggested a photosynthetic ancestor. Understanding the origin of apicoplasts has become particularly significant as it has been touted as a potential target in developing treatments for sporozoan infections that target the parasite without damaging the host.

Unfortunately, a direct connection between the apicoplast and the dinoflagellate chloroplast has remained largely theoretical. Not all sporozoans possess apicoplasts - only a particular clade (including coccidians and Plasmodium) does so, while other sporozoans such as gregarines and Cryptosporidium show no sign of them. Chloroplasts or chloroplast remnants are also absent in an assortment of alveolate flagellate taxa (such as Colpodella) that are regarded as falling within the dinoflagellate-sporozoan clade. Direct comparison of apicoplasts and dinoflagellate chloroplasts is pretty much impossible - apicoplasts have (unsurprisingly) lost all photosynthetic genes, while dinoflagellate chloroplasts have developed severe wierdnesses of their own where they have pretty much lost all genes except the photosynthetic ones*. As a result, researchers have been unable to entirely rule out the possible that sporozoans gained their plastids independently from dinoflagellates. This is where today's announced discovery comes in.

*And severely altered what little they have left. In fact, dinoflagellate genomes as a whole are wierd beyond all belief - they're the only eukaryotes to have lost histones, for instance. I have no idea why they're so strange.

Chromera velia is a small photosynthetic eukaryote, shown above in a photo from the News and Views section of Nature. It is generally immotile, though an internal(!) cilium is present at one end of the cell, and motile stages were seen briefly in old cultures. Reproduction was mainly by binary division - frustratingly, Moore et al. add "not restricted to binary division", but completely fail to explain what this means and how sexual reproduction occurred (if it occurred). In fact, the paper as a whole is frustratingly uninformative about the ultrastructure of Chromera*, being mostly dedicated to the molecular phylogeny of the new taxon relative to other alveolates.

*I mean, seriously, how can you refer to an internal cilium and not go further?

The molecular phylogeny quite strongly supports Chromera as more closely related to sporozoans than dinoflagellates, though less closely related to sporozoans than are colpodellids. The discovery of this photosynthetic member of the sporozoan line adds additional support to the idea that sporozoans are ancestrally photosynthetic.

However, this does not automatically mean that dinoflagellate and sporozoan plastids share a single origin, despite the authors' conclusions. Analysis of plastid genes gave conflicting results - psbA supported a dinoflagellate-Chromera grouping, but SSU rDNA did not. Alveolates have also been suggested to be closely related to the chromists, another group of mostly photosynthetic eukaryotes (including brown and golden algae and diatoms), in a larger grouping called 'chromalveolates'. The existence of the chromalveolate clade was first suggested by their mutual possession of chlorophyll c, a form of chlorophyll not found in any other organisms*. However, Chromera lacks chlorophyll c, and possesses chlorophyll a only, like the red algae from which chromalveolate plastids are derived.

*For those unfamiliar with the various chlorophylls, chlorophyll a is the ancestral form found in pretty much all chlorophyll-containing organisms. Chlorophyll b is found in green algae, land plants and organisms with green alga-derived plasmids, as well as a few Cyanobacteria. Chlorophyll c, as I've said, is found in chromists and dinoflagellates.

The authors of Chromera assume that this indicates a loss of chlorophyll c in the ancestor of Chromera, but I would say that this is too strong a conclusion. The possibility that the sporozoan + Chromera ancestor gained its chloroplast independently from the dinoflagellate ancestor remains alive and well, and, as always, we need to look further into this question.

REFERENCES

Bininda-Emonds, O. R. P., M. Cardillo, K. E. Jones, R. D. E. MacPhee, R. M. D. Beck, R. Grenyer, S. A. Price, R. A. Vos, J. L. Gittleman & A. Purvis. 2007. The delayed rise of present-day mammals. Nature 446: 507-512 (SI here).

Brandt, A., A. J. Gooday, S. N. Brandão, S. Brix, W. Brökeland, T. Cedhagen, M. Choudhury, N. Cornelius, B. Danis, I. De Mesel, R. J. Diaz, D. C. Gillan, B. Ebbe, J. A. Howe, D. Janussen, S. Kaiser, K. Linse, M. Malyutina, J. Pawlowski, M. Raupach & A. Vanreusel. 2007. First insights into the biodiversity and biogeography of the Southern Ocean deep sea. Nature 447: 307-311 (SI here).

Saarela, J. M., H. S. Rai, J. A. Doyle, P. K. Endress, S. Mathews, A. D. Marchant, B. G. Briggs & S. W. Graham. 2007. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446: 312-315 (SI here).

Seeber, F. 2008. Correspondence: Citations in supplementary information are invisible. Nature 451 (7181): 887.

Xu, X., Q. Tan, J. Wang, X. Zhao & L. Tan. 2007. A gigantic bird-like dinosaur from the Late Cretaceous of China. Nature 447: 844-847 (SI here).

Taxon of the Week: A Selection of Ciliates

Of all the groups of unicellular or paucicellular (excuse the neologism) eukaryotes generally lumped under the heading of 'protozoa' or 'protists', ciliates are one of the most noteworthy. Together with sporozoans, they were one of the very few groups to be recognised as distinctive* before the microbial classificatory revolution that was permitted by the appearance of SEM and molecular phylogeny. Through the example of Paramecium, they are also one of the few protist groups whose existence is widely known by the general public. While other prostists such as many flagellate** groups tend to be morphologically fairly plain, ciliates attain a diversity of form and complexity that seems incredible for unicellular organisms.

*Except for an unfortunate tendency for the non-ciliate Stephanopogon to keep trying to mooch its way into the ciliate party. Researchers still have pretty much no idea what to do with Stephanopogon, but the ciliates are adamant that they want nothing to do with it.

**Pre-revolution classifications generally divided protozoans on the basis of locomotory structures between flagellates (with flagella), amoebae (pseudopods), ciliates (cilia) and sporozoans (parasitic taxa without locomotory structures). While it is well-recognised by now that these divisions are largely artificial*** (as is the term 'protozoa' itself), they retain a certain degree of utility as descriptive conveniences (as does 'protozoa'), though 'amoeba' should probably be passed over for 'amoeboid' so as not to cause confusion with the actual genus Amoeba. Also, while light microscopists distinguished flagella (relatively long and few) and cilia (relatively short and usually arranged in tracts), there is no real difference between the two. Some researchers would prefer to refer to all such structures in eukaryotes as 'cilia', reserving the term 'flagella' for bacterial locomotory structures, which are very different.

***Especially as many protists have both amoeboid and flagellate stages in their life cycles.

While the new technologies allowed ciliates as a whole to retain their integrity, they did incite a bit of reshuffling within the clade. Earlier classifications emphasised features of the oral apparatus, but from the 1980s the importance of ultrastructural characters such as arrangement of cilia was recognised (Lynn, 2003). With the addition of molecular data, the ciliates settled (a little uneasily) down into eleven or so classes, some of them well-supported by both molecular and morphological data, some by only one or the other. It is with one of these classes, the Spirotricha, that we concern ourselves today.

The Spirotricha are a diverse bunch, and support for them as a total group is, admittedly, fairly low (though support increases if the divergent Protocruzia is left out of the mix). The classic feature of the spirotrichs are the cirri - bunches of cilia fused into tendril-like structures, which can be seen fairly well in the photo at the top of the post of Euplotes (from A Micronaturalist's Notebook. Not all taxa united molecularly with spirotrichs possess cirri, but features of macronuclear* division also support the grouping.

*An individual ciliate possesses multiple nuclei - one small micronucleus and one or more larger macronuclei. The macronuclei are involved in the day-to-day production of enzymes and such, while the micronucleus is involved in reproduction. When conjugation (sexual reproduction) occurs, the macronuclei break down and only the micronucleus is propagated. The macronuclei are then regenerated from the daughter micronuclei (see here for a more detailed and accurate description - like many so-called 'simple' organisms, ciliates make up for simplicity of structure by indulging in obscenely complicated life cycles).

Euplotes is one of the best-known of the spirotrichs. The photo above well illustrates how Euplotes uses its cirri to walk along the substrate, though they can also be used for swimming. Euplotes is a predator of other ciliates, and as such has a rather large oral cavity. Its voracity in feeding can be remarkable - Kloetzel noted in 1974 that "In extreme cases (with small Tetrahymena, which are eaten much more rapidly than large ones) a Euplotes cell can ingest 17 Tetrahymena within 5 min, representing an area of food vacuole membrane approximately twice that of the entire Euplotes surface". Trust me, I'm fighting the urge to add exclamation marks after that one.



Spirotrichs also include the only ciliate group to have a significant fossil records, the tintinnids. Unlike other ciliates, tintinnids form a lorica (a vase-shaped shell) that may be preserved after the death of the organism (shown above in an SEM by Fiona Scott from Australian Antarctic Division). A detailed taxonomy exists of tintinnids based mainly on lorica structure and composition, and it has been suggested that tintinnids with agglutinated loricas are basal to those with hyaline loricas. However, studies based on living tintinnids show that different lorica types may be possessed by species with the same or similar ciliary arrangements, and there does not appear to be a close correlation between lorica structure and ultrastructure of the living organism (Agatha & Strüder-Kypke, 2007).

REFERENCES

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

Kloetzel, J. A. 1974. Feeding in ciliated protozoa. I. Pharyngeal disks in Euplotes: a source of membrane for food vacuole formation? Journal of Cell Science 15: 379-401.

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.

Pseudo-worms and such

Yesterday I started with dinoflagellates, and showed a fairly typical example. While the typical dinoflagellates are fairly neat in their own right, this post will deal with some far less typical dinoflagellates - the parasitic members of the orders Blastodiniales and Syndiniales.

In the Fensome, Taylor et al. (1993) classification of dinoflagellates, Blastodiniales were a group of extracellular parasites with a dinokaryon (the distinctive dinoflagellate nucleus - see the previous post) for only part of their complicated life cycles. Blastodiniales were a diverse group, and Fensome et al. made no secret of its probable polyphyly. Most families of Blastodiniales start out as a trophont (feeding stage) attached to the host by rhizoids, a peduncle or a stylet (the exception is Blastodinium, in which the trophont is not actually attached but resides within the gut of copepods). The trophont may produce spores while attached and feeding (palisporogenesis), or may detach first before producing spores (palintomy). The spores are eventually released as motile dinospores, that have been recorded fusing to form gametes in at least some taxa, or give rise directly to the new generation of trophonts. Plastids are present in Blastodininium and Protoodinium, while other Blastodiniales are non-photosynthetic.

In Cachonella (Cachonellaceae), the trophont is attached to its siphonophore host by rhizoids. When it is finished feeding, it detaches and develops long tubular processes within the host's gut (the illustration in Fensome et al. has definite B-grade sci-fi appeal). After being passed from the host, the ex-trophont produces coccoid aplanospores (non-motile spores) that in turn remain attached to each other while shedding a series of cyst membranes, to form a branching structure with a spore at the end of each branch. Eventually the non-motile aplanospores give rise to motile dinospores.

Haplozoon is a very distinctive form that Fensome et al. assigned to Blastodiniales (though Leander et al. (2002) disputed this position, as Haplozoon appears to possess a dinokaryon throughout its life-cycle). Haplozoon initially attaches to its host (a larvacean or annelid) as a unicellular trophont by a stylet. It then undergoes multiple cell divisions to give rise to a flat worm- or ribbon-like (apparently) multicellular form with a single trophocyte (feeding cell), multiple rows of gonocytes (dividing cells) and a distal row of sporocytes (spore-producing cells). The single nuclei of the sporocytes become four, and individual sporocytes are released as cysts (probably eventually releasing four dinospores, but this doesn't appear to have actually been observed). While the mature stage of Haplozoon has generally been interpreted as multicellular (or colonial), Leander et al. found that SEM images of H. axiothellae appeared to show a single continuous membrane covering all "cells", and so interpreted Haplozoon as forming a unique compartmentalised syncytium (multinucleate single cell).

The non-photosynthetic Syndiniales possess dinoflagellate-like flagella, but do not possess a dinokaryon. In the Syndiniaceae, the trophont is a multinucleate plasmodium. In the Sphaeriparaceae, the trophont produces a long chain of aplanospores that are eventually released as dinospores.

Amoebophrya is a member of Syndiniales whose trophont develops a large conical cavity, the mastigocoel, in which multiple flagella are formed before the entire structure flips inside-out to give rise to a long worm-like, multinucleate, multiflagellate, mobile stage, the vermiform. The vermiform then undergoes multiple cleavages to form hundreds of individual dinospores.

REFERENCES

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

Leander, B. S., J. R. Saldarriaga & P. J. Keeling. 2002. Surface morphology of the marine parasite Haplozoon axiothellae Siebert (Dinoflagellata). European Journal of Protistology 38: 287-297.

Little whirling photosynthetic (and not so photosynthetic) thingies

I spent long and hard thinking of what I should make the subject of my first post (honestly, it took minutes!) but I eventually decided to write something on a subject I've spent a little time on recently but know precious little about - dinoflagellates (Dinoflagellata).

Dinoflagellates are unicellular protists, generally accepted to form a clade called Alveolata with ciliates and sporozoans (the image at left is a generalised dinoflagellate from Andrew MacRae's Dinoflagellates [http://www.geo.ucalgary.ca/~macrae/palynology/dinoflagellates/anatomy.html]). They are most familiar to the general public as the main culprit behind toxic algal blooms. The main distinguishing feature of dinoflagellates is that they possess two distinct flagella - a fairly straight one that sticks out from the cell, and a wavy one that wraps around the cell, usually in a groove. Most dinoflagellates also have a distinctive nucleus that lacks histones, the proteins that DNA wraps around in other eukaryotes, and with chromosomes that don't decondense between divisions. According to Fensome, Taylor et al. (1993), about half of dinoflagellates are photosynthetic, while the other half are mostly parasitic (some are both).

I got onto the subject of dinoflagellates because I was organising my records on dinoflagellate taxonomy (I try and cover the taxonomy of all organisms, and I am completely happy in the knowledge that this is probably an impossible task for one person - you can see a number of my efforts, varying from some I'm quite proud of to the truly tragic, at http://www.palaeos.org/). Dinoflagellates have perhaps the worst taxonomy of any group of organisms - worse than fossil plants, worse than South American harvestmen, worse than hominins. You may be aware that there are separate taxonomic codes for plants and animals. There are organisms that are neither plants nor animals, but because the codes were developed before this was understood, protists are assigned to either the botanical or zoological codes depending on which they were traditionally regarded as. Photosynthetic protists are covered by the botanical code, mobile protists are zoological. Problem is, some protists are both photosynthetic and mobile. Dinoflagellates are probably the largest group of organisms that have been regarded by different workers as under different taxonomic codes. As a result, the literature is full of names for dinoflagellates that are valid under one code but not under the other, and cases different codes require different names for the same thing. Palaeontologists working on dinoflagellates agreed to use the botanical code after 1961, and Fensome, Taylor et al. (1993) suggested the same thing for neontological taxa.

The other major issue with dinoflagellates is reconciling the fossil and living taxa. Many dinoflagellates form resistant vegetative cysts at some stage in the life-cycle, and these are the only stage that can be fossilised. Fossil taxonomy, therefore, is based on these. Neontological taxonomy, however, is generally based on the motile stage of the cycle. As a result, two separate taxonomies have developed in parallel, and there are relatively few cases where a cyst can be connected with a motile form. The worst case of this problem involves the fossil genus Spiniferites Mantell 1850, which has long been known to represent the cyst of the living genus Gonyaulax Diesing 1866. Unfortunately, because both of these genera are quite large and involve a lot of species, most workers have turned something of a blind eye to this point, and no real solution has been developed.

Coming up later, a few examples of the odder dinoflagellates, and the boundary between unicellularity and multicellularity. Unless, of course, I get distracted and cover something else.