Chrysista

Nannochloropsis sp., from Inks002.

Belongs within: Sar.
Contains: Xanthophyceae, Phaeophyceae, Chrysophyceae.

The Chrysista are a clade of mostly photosynthetic eukaryotes ancestrally with ciliary supra-tz helix (Cavalier-Smith 2018).

Filling in the gaps
Published 11 June 2007

It is universally accepted these days that the algae are a polyphyletic grouping, at least from the viewpoint of nuclear and cytoplasmic ancestry. Chlorophyll originally developed within the blue-green algae, actually a clade of bacteria (Cyanobacteria). Chloroplasts in eukaryotes then arose through endosymbiosis between a non-photosynthetic protist and a cyanobacterium. However, many authors now agree that there was probably only one such primary endosymbiosis event that led to the majority of modern chloroplasts (there is a lonely cercozoan*, Paulinella, that appears to have derived its chloroplast independently). The direct descendants of this lucky protist today are the green plants and algae (Viridiplantae), the red algae (Rhodophyta) and a small group of unicells called the blue-green algae (Glaucophyta). Red and blue-green algae both have only a single chlorophyll type, chlorophyll a, while green algae possess a second form as well, chlorophyll b (interestingly, a small handful of cyanobacteria also possess chlorophyll b, and molecular phylogenies show that these oddjobs are not closely related within the cyanobacteria). The remaining algae are derived from secondary symbioses, where a eukaryotic alga has become an endosymbiont of another eukaryote followed by loss of the endosymbiont’s independence and genetic material. This is rather spectacularly demonstrated by two secondary algal groups, the chlorarachneans and cryptophytes, whose chloroplasts retain a highly-reduced eukaryotic nucleus between the membranes surrounding the chloroplast. Two groups, the amoeboid chlorarachneans and flagellate euglenoids, have chloroplasts derived from green algae as shown by their possession of chlorophyll b. Four groups, the dinoflagellates, cryptophytes, haptophytes and ochrophytes, have chloroplasts seemingly derived from red algae. These four groups also share a third chlorophyll type, chlorophyll c, as well as the ancestral chlorophyll a, and on this basis it has been suggested that they all derive from a single endosymbiotic ancestor (though this seems likely, the case is not airtight as there are a number of non-photosynthetic protists without chloroplasts that seem to be closely related to one or another of the chlorophyll c groups). Some dinoflagellates have replaced their ancestral chloroplasts with chloroplasts derived from haptophytes in a tertiary endosymbiosis.

*Originally I had identified Paulinella in this post as an amoebozoan, but it belongs to a different amoeboid group, the Cercozoa.

Multicellularity has evolved a number of times within algae. Viridiplantae became multicellular multiple times whereas red algae probably evolved multicellularity once at the base of the Bangiophyceae+Florideophyceae clade. Ochrophytes include two groups of multicellular algae, the brown algae (Phaeophyceae) and some members of the yellow-brown algae (Xanthophyceae).

Ochrophytes are the clade of photosynthetic heterokonts. Heterokonts are a well-supported clade of protists distinguished in most members by, among other features, a shorter posterior flagellum and a longer anterior flagellum with numerous side bristles (mastigonemes). At cell division, the anterior flagellum moves backwards and loses the mastigonemes to become the posterior flagellum, while a new anterior flagellum is generated (Andersen 2004). As well as the two above-mentioned classes, ochrophytes include diatoms and a whole bunch of unicellular algae previously united as the golden algae (chrysophytes). The chrysophytes have proven to be paraphyletic with regard to the other ochrophytes, and have been divided into a whole host of smaller classes.

Schizocladia ischiensis, from Rizouli et al. (2020).

Now we’ve gotten through all that, I’ll finally introduce today’s star: Schizocladia ischiensis Henry, Okuda & Kawai in Kawai, Maeba et al. 2003. The position of the brown algae in relation to other ochrophytes has been obscured by the absence of clear connecting features between the multicellular brown algae and the various unicellular golden algae. The significance of Schizocladia is that it goes some way towards filling that gap. Schizocladia is a small marine ochrophyte that grows as filaments of cells in single file. Like phaeophytes, Schizocladia has cell walls impregnated with alginates. Unlike brown algae, Schizocladia lacks cellulose or plasmodesmata (cytoplasmic connections between cells). Propagation in Schizocladia was via zooids produced in individual compartments in swollen cells at the end of the filaments.

The molecular phylogenies presented in the original description of Schizocladia agreed in positioning it as the sister group of Phaeophyceae. They also agreed with the result found by other studies that there is a clade composed of Phaeophyceae (+Schizocladia), Xanthophyceae and the unicellular Phaeothamniophyceae (the unicellular Chrysomeridales may also belong to this clade but do not appear to have been investigated molecularly). While the Xanthophyceae do include some multicellular members, it also includes unicellular forms, and multicellularity was probably evolved independently of Phaeophyceae. Xanthophyceae do possess cellulose in the cell walls, and the presence of alginates has also been demonstrated in some species.

Due to the absence of some supposed key phaeophyte characters, Schizocladia was not included in Phaeophyceae but placed in its own independent class Schizocladiophyceae. Nevertheless, its simple morphology provides a nice connection between the unicellular ochrophytes and multicellular phaeophytes.

Parcelling plastids
Published 5 July 2007

The Table of Contents alert for a bright, shiny new issue of Protist arrived in my e-mail box today. This is a journal I can usually rely on to supply something worthy of note (often some things), and today’s was no exception. Right near the beginning of the issue, we receive a new class of heterokont (Horn et al., 2007).

So many new chromist classes have appeared in recent years that they’re almost becoming routine. Horn et al. (2007) dubbed their contribution Synchromophyceae, containing a single species Synchroma grande scraped off marine rocks on the coast of the Canary Islands (perhaps not the most unpleasant place to do field work). Synchroma is a photosynthetic amoeboid that forms a meroplasmodium (a network of individual cells connected by branching and anastomosing [fusing together where they meet] reticulopodia). Meroplasmodial forms are extremely rare in chromists. The only other chromist that exhibits this body form is the haptophyte Reticulosphaera japonensis (Cavalier-Smith et al. 1996). The main cell body is contained in a flattened lorica, which is adpressed to the substrate and is more or less circular on a flat surface. In reproduction, one daughter cell remains sessile in the lorica, while the other is released as a migratory cell. Migratory and floating cells are fusiform with axopodia extending from the anterior and posterior ends. Sessile cells could also spontaneously convert to migratory cells by hatching out of their lorica. At no stage in the life-cycle were flagella present.

Time lapse of vegetative reproduction in Synchroma grande, from Horn et al. (2007).

Phylogenetic analysis of Synchroma demonstrated that it is part of the Ochrophyta, the photosynthetic heterokont clade. Both rbcL and 18S rDNA maximum likelihood trees placed Synchroma as sister to the Chrysophyceae+Synurophyceae clade, but support in both cases was relatively low. The absence of a girdle lamella in Synchroma’s chloroplasts supports its exclusion from either of those two classes.

The most interesting feature of Synchroma, however, lies in the arrangement of chloroplasts in the cell. As I mentioned above, the chromist chloroplast is believed to be derived from an endosymbiotic red alga in a secondary endosymbiosis. As a result, the chromist chloroplast is surrounded by four membranes that represent (from the inside out) the original cyanobacterium’s external cell membrane, the vacuolating membrane of the primary host, the primary host’s external cell membrane, and the vacuolating membrane of the secondary host. There is some debate about whether the chloroplasts of all chromist groups (and those of their putative sister group, the alveolates) derive from a single endosymbiotic event, or have been independently derived from multiple events. The majority of authors currently favour the former option, or at least that the number of events was quite few. However, Synchroma has a unique arrangement of chloroplasts in regard to surrounding membranes. Each individual chloroplast is surrounded by two membranes, and then multiple chloroplasts are clustered in packages contained by the remaining two membranes. Horn et al. suggest in passing that Synchroma may preserve an ancestral stage in the endosymbiotic process, after the loss of the eukaryotic endosymbiont’s nucleus but before the separation of the endosymbiont’s chloroplasts (after all, there is no reason why the eukaryotic endosymbiont would have necessarily had only one chloroplast per cell). In light of the derived position of Synchroma within the chromists, if this is indeed an ancestral state it makes the idea of a single endosymbiosis event rather unlikely, because this would require that the ancestral state was lost repeatedly in all other chromist groups. However, I feel that it is much more likely that the other explanation suggested by Horn et al. for Synchroma‘s unusual chloroplasts is correct: that it is a derived state resulting from an abnormal division pattern. The possibility that within chromists cryptophytes, haptophytes and heterokonts have gained their chloroplasts independently is not completely unbelievable, but the idea that multiple hterokont groups have done the same seems to be pushing it a little. Especially as all members of this undoubtedly monophyletic clade possess red algal-derived chloroplasts—if they derived them independently, why shouldn’t at least some have green algal chloroplasts?

Systematics of Chrysista
<==Chrysista [Phaeista]C-S18
    |  i. s.: ChrysowaernellaAB19
    |--+--Raphidomonadea [Raphidoistia]C-S18
    |  |    |--RaphopodaC-S18
    |  |    |    |  i. s.: HelioraphaC-S18
    |  |    |    |--Commation Thomsen & Larsen 1993C-S18, C-S97 [Commatiida]
    |  |    |    `--Actinophryidae [Actinophryales, Actinophryida, Nucleohelea]AS12
    |  |    |         |--ActinophrysC-S18
    |  |    |         |    |--A. marina (Mikryukov 1995)TS02
    |  |    |         |    |--A. sol Muller 1773W86
    |  |    |         |    `--A. vesiculataV63
    |  |    |         `--ActinosphaeriumC-SC06 [incl. CamptonemaP99, EchinosphaeriumP99]
    |  |    |              |--A. eichhornii Ehrenberg 1840W86
    |  |    |              |--A. nucleofilumC-SC06
    |  |    |              `--A. solMH96
    |  |    `--RaphidophyceaeDL-G16
    |  |         |--SulcophycidaeC-S18
    |  |         |    |--Olisthodiscus luteusAB19, R87
    |  |         |    `--SulcochrysisC-SC06
    |  |         `--Raphidophycidae [Chloromonadida, Raphidomonadales, Raphidophyceae]C-S18
    |  |              |  i. s.: GoniostomumAS12
    |  |              |         HaramonasAS12
    |  |              |         MerotrichaAB19
    |  |              |--Fibrocapsa japonica Toriumi & Takano 1973DL-G16
    |  |              `--+--Heterosigma Hada 1968S73
    |  |                 |    |--*H. inlandicum Hada 1968S73
    |  |                 |    |--H. akashiwo (Hada) Hada 1968 [=Entomosigma akashiwo Hada 1967]S73
    |  |                 |    `--H. carteraeC-SC06
    |  |                 `--+--Vacuolaria virescensC-SC06
    |  |                    `--ChattonellaC-SC06
    |  |                         |--C. antiquiaKI02
    |  |                         |--C. marinaOSS10
    |  |                         `--C. subsalsaC-SC06
    |  `--FucistiaC-S18
    |       |--ChrysomerophyceaeC-SC06
    |       |    |  i. s.: Antarctosaccion applanatumC-SC06
    |       |    `--ChrysomeridalesC-SC06
    |       |         |--Giraudyopsis stelliferaC-SC06
    |       |         |--ChrysomerisC-SC06
    |       |         `--PhaeosaccionKM03
    |       `--+--XanthophyceaeDL-G16
    |          `--+--+--PhaeophyceaeC-SC06
    |             |  `--Schizocladia Henry, Okuda & Kawai in Kawai, Maeba et al. 2003KM03 (see below for synonymy)
    |             |       `--*S. ischiensis Henry, Okuda & Kawai in Kawai, Maeba et al. 2003KM03
    |             `--AurophyceaeC-S18
    |                  |--Aurearena [Auarearenophycidae]C-S18
    |                  `--Phaeothamniophycidae [Phaeothamniophyceae]C-SC06
    |                       |  i. s.: Tetrasporopsis fuscescensKM03
    |                       |--Pleurochloridella [Pleurochloridellales]AB19
    |                       |    `--P. botrydiopsisKI02
    |                       `--PhaeothamnialesC-SC06
    |                            |--Phaeoschizochlamys mucosaKM03
    |                            `--+--Phaeothamnion confervicolaKM03, C-SC06
    |                               `--StichogloeaKM03
    |                                    |--S. doederlieniiKM03
    |                                    `--S. globosaDG01
    `--Limnistia [Limnista]C-S18
         |--+--ChrysophyceaeDL-G16
         |  `--Picophagea [Synchromophyceae]C-SC06
         |       |--ChrysopodocystisC-S18
         |       |--GuanochromaC-S18
         |       |--LeukarachnionC-S18
         |       |--Synchroma pusillum Schmidt et al. 2012C-S18, DL-G16
         |       |--Picophagus Guillou & Chrétiennot-Dinet 1999 [Picophagaceae, Picophagales]C-SC06
         |       |    `--P. flagellatusC-SC06
         |       `--Chlamydomyxa Archer 1875C-SC06, KC01 [Chlamydomyxales]
         |            |--C. labyrinthuloidesC-SC06
         |            `--C. montanaC-SC06
         `--Eustigmatales [Eustigmatida, Eustigmatophyceae, Eustigmatophyta]C-SC06
              |  i. s.: Vischeria helveticaC-SC06, KI02
              |         Monodus subterraneaKI02
              |         BotryochloropsisAS12
              |--+--Eustigmatos magnaC-SC06
              |  `--Pseudocharaciopsis minutaC-SC06, KI02
              `--+--Monodopsis subterraneaC-SC06
                 `--NannochloropsisC-SC06
                      |--N. gaditanaC-S18
                      |--N. granulataKI02
                      |--N. oceanicaC-SC06
                      |--N. oculataKI02
                      `--N. salinaKM03

Schizocladia Henry, Okuda & Kawai in Kawai, Maeba et al. 2003KM03 [Schizocladiaceae, Schizocladiales, SchizocladiophyceaeSRR14, Schizocladiophycidae]

*Type species of generic name indicated

References

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

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

Andersen, R. A. 2004. Biology and systematics of heterokont and haptophyte algae. American Journal of Botany 91 (10): 1508–1522.

[C-S97] Cavalier-Smith, T. 1997. Amoeboflagellates and mitochondrial cristae in eukaryote evolution: megasystematics of the new protozoan subkingdoms Eozoa and Neozoa. Archiv für Protistenkunde 147: 237–258.

[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.

Cavalier-Smith, T., M. T. E. P. Allsopp, M. M. Häuber, G. Gothe, E. E. Chao, J. A. Couch & U.-G. Maier. 1996. Chromobiote phylogeny: the enigmatic alga Reticulosphaera japonensis is an aberrant haptophyte, not a heterokont. European Journal of Phycology 31 (3): 255–263.

[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.

[CS02] Cetlin, A. B., & M. V. Safonov. 2002. Intersticial’nye polihety (Annelida) Kandalakšskogo zaliva Belogo Morâ. Zoologicheskii Zhurnal 81 (8): 899–908.

[DG01] Daugbjerg, N., & L. Guillou. 2001. Phylogenetic analyses of Bolidophyceae (Heterokontophyta) using rbcL gene sequences support their sister group relationship to diatoms. Phycologia 40 (2): 153–161.

[DL-G16] Derelle, R., P. López-García, H. Timpano & D. Moreira. 2016. A phylogenomic framework to study the diversity and evolution of stramenopiles (=heterokonts). Molecular Biology and Evolution 33 (11): 2890–2898.

Horn, S., K. Ehlers, G. Fritzsch, M. C. Gil-Rodríguez, C. Wilhelm & R. Schnetter. 2007. Synchroma grande spec. nov. (Synchromophyceae class. nov., Heterokontophyta): an amoeboid marine alga with unique plastid complexes. Protist 158 (3): 277–293.

[KI02] Kawachi, M., I. Inouye, D. Honda, C. J. O’Kelly, J. C. Bailey, R. R. Bidigare & R. A. Andersen. 2002. The Pinguiophyceae classis nova, a new class of photosynthetic stramenopiles whose members produce large amounts of omega-3 fatty acids. Phycological Research 50: 31–47.

[KM03] Kawai, H., S. Maeba, H. Sasaki, K. Okuda & E. C. Henry. 2003. Schizocladia ischiensis: a new filamentous marine chromophyte belonging to a new class, Schizocladiophyceae. Protist 154: 211–228.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[MH96] Miller, S. A., & J. P. Harley. 1996. Zoology 3rd ed. Wm. C. Brown Publishers: Dubuque (Iowa).

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

[R87] Rizzo, P. J. 1987. Biochemistry of the dinoflagellate nucleus. In: Taylor, F. J. R. (ed.) The Biology of Dinoflagellates pp. 143–173. Blackwell Scientific.

[SRR14] Silberfeld, T., F. Rousseau & B. de Reviers. 2014. An updated classification of brown algae (Ochrophyta, Phaeophyceae). Cryptogamie, Algologie 35 (2): 117–156.

[S73] Sournia, A. 1973. Catalogue des espèces et taxons infraspécifiques de Dinoflagellés marins actuels publiés depuis la révision de J. Schiller. I. Dinoflagellés libres. Beihefte zur Nova Hedwigia 48: 1–92.

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

[W86] Whitelegge, T. 1886. List of the freshwater Rhizopoda of N. S. Wales. Part I. Proceedings of the Linnean Society of New South Wales, series 2, 1 (2): 497–504.

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