Cryptophyceae

Cryptomonas, copyright Wolfgang Bettighofer.

Belongs within: Cryptista.

The Cryptophyceae are a group of flagellate protists including both photosynthetic and phagotrophic taxa.

Cryptophytes: four genomes for the price of one
Published 5 August 2017

Sometimes, the little things really do make a difference. Cryptophytes (or cryptomonads) are one of the many groups of minute flagellate protists to be found around the world whose role in our lives tends to get dismissed because of their microscopic size. Nevertheless, cryptophytes make up a large part of the photosynthetic phytoplankton in both freshwater and marine habitats and so ultimately are a starting point for many of the food chains that we depend on. They also had an important role to play in our developing understanding of how modern eukaryote cells have evolved.

Structure of a typical cryptophyte, from here.

As well as occurring in the phytoplankton, cryptophytes have also been found in damp soil and snow. They have a distinctive, slightly lop-sided cell morphology with two haired flagella of unequal length inserted in an invaginated gullet towards the right side of the front of the cell. This invagination is also lined on the ventral side by organelles called ejectosomes (sometimes spelled ‘ejectisome’). When the organism is threatened, these ejectosomes shoot out a proteinaceous ribbon that propels the cell rapidly away from the source of irritation. Some of the references to ejectosome function that I’ve found seem to imply that the expelled ribbon is itself toxic, but I’m not sure if I’ve understood correctly. Smaller ejectosomes may also play a role in capturing bacteria and the like for the cryptophyte to feed on. Cryptophytes have a distinctive way of moving through the water column, resulting from the uneven lengths of their two propellent flagella, that has been reffered to as ‘recoiling’. Essentially, they move in a series of circular tumbles while the cell itself corkscrews around its axis. This movement is distinctive enough that cryptophytes have been dubbed with the Dutch vernacular name of ‘rekylalger’, ‘recoiling algae’ (Novarino 2003).

Diagram of typical cryptophyte movement, from Novarino (2003).

The majority of cryptophytes are heterotrophic: one or more large chloroplasts provide much of the cell’s energy, but they are also capable of ingesting particulate matter through the gullet. As alluded above, the cryptophyte chloroplast has been significant in the study of how chloroplasts evolved. The 1960s and 1970s saw an increasing acceptance of the concept that some organelles, most notably mitochondria and chloroplasts, had originally appeared through a process of endosymbiosis: bacteria had become intimately associated with eukaryote cells, becoming embedded in the host cell and eventually ceding enough of their vital functions to the host to be unable to function as independent organisms. The chloroplasts of the ancestors of land plants arose in this manner from cyanobacteria, as indicated by the presence of a remnant but reduced bacterial genome within the chloroplast itself, and the presence of a double membrane around each chloroplast (corresponding the cyanobacterium’s original cell membrane, plus the vacuoule membrane in which it had been enclosed by the host eukaryote). In the early 1970s, however, it was found that cryptophyte chloroplasts have not two but four surrounding membranes. What is more, wedged between two of those membranes was a tiny remnant cell nucleus, dubbed the nucleomorph. The nucleomorph was a crucial piece of evidence in demonstrating that cryptophyte chloroplasts had arisen by a process of secondary endosymbiosis. A eukaryote cell containing a chloroplast that had arisen in the manner described above was itself engulfed and converted to a chloroplast by another eukaryote. The four membranes around the cryptophyte membrane were therefore, from the inside out, the original cyanobacterium cell membrane, the vacuole membrane containing the cyanobacterium, the cell membrane of the primary host cell (with the nucleomorph between this and the last), and the vacuole membrane in which that had been contained in turn. Other groups of eukaryotes also have chloroplasts that arose in this way, such as brown algae and dinoflagellates, but in these the nucleus of the captured eukaryote cell has entirely disappeared.

Another cryptophyte structural diagram of the species Guillardia theta, showing the arrangement of the chloroplast, from here. This also shows the sites of the four genomes contained in the typical cryptophyte cell.

Exactly when the cryptophyte chloroplast arose remains a contentious subject. Various lines of evidence point to the captured chloroplast donor being a red alga, as is also the case with the aforementioned brown algae and dinoflagellates. As such, some have argued for the chloroplasts of all such algae being descended from a single capture event. However, there are also a number of protists related to such taxa that lack chloroplasts. In the case of cryptophytes, there is strong evidence that the sister clade to the the photosynthetic cryptophytes is the chloroplast-less genus Goniomonas. The subsequent sister to these two clades together is less certain but a number of recent studies have pulled forward another chloroplast-less group, the katablepharids. If the cryptophyte chloroplast shares an origin with that of brown algae, then it must have somehow been lost in the ancestors of both Goniomonas and katablepharids. So far, an author’s preference for a single or multiple origins of red alga-derived chloroplasts tends to come down to whether they think it is easier for chloroplasts to be lost or gained, a question whose answer is still unclear.

The diversity within cryptophytes is still not that well understood, largely due to difficulties in observing significant characters. Prior to the advent of scanning electron microscopy, some authors had gone so far as to dismiss cryptophytes as essentially unclassifiable. Nevertheless, not everything was as bleak as the pessimists would have it. Cryptophyte taxa may differ from each other in overall size and shape. They may also differ in cell colour, due to the presence of various accessory pigments in addition to chlorophyll. The primary accessory pigments found in cryptophytes are known as phycocyanin and phycoerythrin; species containing the former are a blue-green colour whereas those containing the latter are reddish, golden or a greenish yellow. The use of scanning electron microscopy has led to the discovery of other useful features such as those relating to the periplast, a protein envelope that covers the inside and outside of the cryptophyte cell membrane. Electron microscopy has shown that the outer periplast layer is often ornamented, such as by being divided into scales. And even more recently, of course, researchers have recognised the value that molecular tools may have to offer cryptophyte taxonomy, though said tools have also complicated matters by, for instance, giving hints that previously recognised ‘taxa’ may represent different life cycle stages of a single organism. Whatever the eventual result, there is no question that we still have a lot to learn about cryptophytes.

Systematics of Cryptophyceae

Characters (from Adl et al. 2012): Autotrophic, mixotrophic or heterotrophic with ejectisomes (trichocysts); mitochondrial cristae flat tubules; two cilia emerging subapically or dorsally from right side of an anterior depression (vestibulum); longitudinal grooves (furrows) and/or tubular channels (gullets) or a combination of both, extending posteriorly from vestibublum on ventral side; gullet/furrow complexes lined with large ejectisomes; with or without plastid-nucleomorph complex; chloroplasts when present contain chlorophylls a and c2 and phycobiliproteins, located in thylakoid lumen; chloroplast covering comprised of inner and superficial periplast components.

Cryptophyceae [Cryptomonadales, Cryptomonadida, Cryptophyta]AS12
| i. s.: Chilodinium Massart 1920FT93
| Chrysidella Pascher 1911FT93
| PyrenomonasMO08
| |--P. helgolandiiMO08
| |--P. ovalisC-S18
| `--P. salinaMP95
| Teleaulax amphioxeiaEDF04
| Plagioselmis nannoplancticaBI09
| StoreatulaAB19
|--Cryptomonas Ehrenberg 1831C-SC06, FT93
| |--C. abbreviataC-S18
| |--C. caudataOC09
| |--C. erosaKN03
| | |--C. e. var. erosaKN03
| | `--C. e. var. reflexaKN03
| |--C. obovoideaC-SA96
| |--C. ovataC-SC06
| |--C. paramecium [=Chilomonas paramecium]C-S18
| |--C. phiS03
| |--C. rostratisformisKN03
| |--C. schaudinniLT64
| `--C. rostrellaC-SC03
`--+--Guillardia thetaC-SC06
`--+--+--Proteomonas sulcataC-SC06
| `--RhodomonasC-SC06
| |--R. abbreviataMO08
| |--R. lensC-S18
| |--R. marinaOI05
| `--R. salinaGLB04
`--+--+--Hanusia phiOI05
| `--Geminigera cryophilaC-SC06
`--+--Falcomonas daucoidesC-SC06
`--+--+--Komma caudataC-SC06
| `--HemiselmisC-SC06
| |--H. anderseniiOC09
| |--H. brunnescensOI05
| `--H. virescensC-SC06
`--ChroomonasC-SC06
|--C. acutaC-S18
|--C. caudataSX97
|--C. coeruleaOC09
|--C. mesostigmaticaC-SC06
|--C. nordtstedtiiMM05
|--C. ovalisSX97
|--C. pochmanniiOC09
`--C. salinaC-S18

*Type species of generic name indicated

References

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[BI09] Burki, F., Y. Inagaki, J. Bråte, J. M. Archibald, P. J. Keeling, T. Cavalier-Smith, M. Sakaguchi, T. Hashimoto, A. Horak, S. Kumar, D. Klaveness, K. S. Jakobsen, J. Pawlowski & K. Shalchian-Tabrizi. 2009. Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, Telonemia and Centroheliozoa, are related to photosynthetic chromalveolates. Genome. Biol. Evol. 2009: 231–238.

[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.

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[C-SC03] Cavalier-Smith, T., & E. E.-Y. Chao. 2003. Phylogeny of Choanozoa, Apusozoa, and other Protozoa and early eukaryote megaevolution. Journal of Molecular Evolution 56: 540–563.

[C-SC06] Cavalier-Smith, T., & E. E.-Y. Chao. 2006. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). Journal of Molecular Evolution 62: 388–420.

[EDF04] Ekelund, F., N. Daugbjerg & L. Fredslund. 2004. Phylogeny of Heteromita, Cercomonas and Thaumatomonas based on SSU rDNA sequences, including the description of Neocercomonas jutlandica sp. nov., gen. nov. European Journal of Protistology 40: 119–135.

[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.

[GLB04] Gray, M. W., B. F. Lang & G. Burger. 2004. Mitochondria of protists. Annual Review of Genetics 38: 477–524.

[KN03] Knapp, C. W., F. deNoyelles Jr., D. W. Graham & S. Bergin. 2003. Physical and chemical conditions surrounding the diurnal vertical migration of Cryptomonas spp. (Cryptophyceae) in a seasonally stratified Midwestern reservoir (USA). Journal of Phycology 39: 855–861.

[LT64] Loeblich, A. R., Jr & H. Tappan. 1964. Sarcodina: chiefly “thecamoebians” and Foraminiferida. In: Moore, R. C. (ed.) Treatise on Invertebrate Paleontology pt C. Protista 2 vol. 1. The Geological Society of America and The University of Kansas Press.

[MP95] Maher, M., R. Palmer, F. Gannon & T. Smith. 1995. Relationship of a novel bacterial fish pathogen to Streptobacillus moniliformis and the fusobacteria group, based on 16S ribosomal RNA analysis. Systematic and Applied Microbiology 18: 79–84.

[MM05] Melkonian, M., & D. Mollenhauer. 2005. Robert Lauterborn (1869–1952) and his Paulinella chromatophora. Protist 156: 253–262.

[MO08] Moore, R. B., M. Oborník, J. Janouškovec, T. Chrudimský, M. Vancová, D. H. Green, S. W. Wright, N. W. Davies, C. J. S. Bolch, K. Heimann, J. Šlapeta, O. Hoegh-Guldberg, J. M. Logsdon, Jr. & D. A. Carter. 2008. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451: 959–963.

Novarino, G. 2003. A companion to the identification of cryptomonad flagellates (Cryptophyceae = Cryptomonadea). Hydrobiologia 502: 225–270.

[OC09] Okamoto, N., C. Chantangsi, A. Horák, B. S. Leander & P. J. Keeling. 2009. Molecular phylogeny and description of the novel katablepharid Roombia truncata gen. et sp. nov., and establishment of the Hacrobia taxon nov. PLoS One 4 (9): e7080.

[OI05] 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.

[S03] Simpson, A. G. B. 2003. Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). International Journal of Systematic and Evolutionary Microbiology 53: 1759–1777.

[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.

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