Labyrinthulomycetes

Vegetative cells of Thraustochytrium, copyright Celeste Leander.

Belongs within: Bigyra.

The Labyrinthulomycetes, slime nets, are a group of mostly aquatic protists producing a network of anastomosing filaments.

Slime nets: another group of not-fungi
Published 10 March 2008
Colony (left) and individual cells of Labyrinthula, from here.

Labyrinthuleans, commonly referred to as ‘slime nets’ are one of those organisms that, being neither animals nor plants, have been shuffled back and forth between and within the nomenclatural codes over the years, resulting in the same taxon being referred to by multiple different names. Labyrinthulea, Labyrinthista and Labyrinthulomycota are just three options that might be encountered. They are one of the protist groups that have been described as ‘slime moulds’, though they lack the dramatic life cycles of the Mycetozoa, the slime moulds proper. Most labyrinthuleans are found in aquatic habitats, but some species are terrestrial.

Labyrinthuleans may be divided into three groups, the Thraustochytriales, Labyrinthulales and the Diplophrys group. Note that these may not be phylogenetically separate groups—the molecular analysis of Cavalier-Smith & Chao (2006), for instance, doesn’t separate the three—but they are still useful form groups. The Labyrinthulales and Thraustochytriales are united by the possession of an organelle called a bothrosome or sagenogen(etosome) that produces large amounts of filamentous net-like ectoplasmic membrane that the individual cells move along and absorb nutrients through, hence the name of ‘slime nets’. Many labyrinthuleans are parasitic and invade and break down cells of host organisms, absorbing nutrients released by the decomposing cells. The individual cells form aggregative masses during reproduction, within which enlarged cells undergo meiosis and release flagellated zoospores (Barnes 1998). The most obvious difference between the two groups seems to be the mode of colony formation—whereas Labyrinthulales form dispersed colonies of loosely connected cells surrounded by ectoplasmic matrix as seen above, Thraustochytriales (as exemplified below) form more compact colonies with the ectoplasmic net growing as “roots” from the base of the colony. The small inset photo shows the zoospore of Schizochytrium.

Colony of Schizochytrium limacinum, with inset zoospore, from here.

The genera Diplophrys and Sorodiplophrys are associated with the labyrinthuleans by molecular (Cavalier-Smith & Chao 2006) and ultrastructural (Dykstra & Porter 1984) data. However, while they do produce and move on ectoplasmic outgrowths, they lack a bothrosome for the production of said ectoplasm. Zoospore production has also never been recorded for these genera. The terrestrial Sorodiplophrys has an aggregative stage in its life cycle, but the aquatic Diplophrys marina does not (the actual type species of Diplophrys, D. archeri, has not been observed since 1902, and D. marina is only tentatively included in the same genus). Interestingly, the analysis of Cavalier-Smith & Chao (2006) places Diplophrys marina within the Labyrinthulales, which if correct implies that it lost the labyrinthulean characteristics during its evolutionary history.

As ‘slime moulds’, the labyrinthuleans were originally regarded as fungi (hence some publications refer to them as labyrinthulomycetes). However, it is now universally agreed that they are in fact members of the heterokonts (Chromista) based on the ultrastructure of the zoospores, as well as molecular data. Within the heterokonts, Cavalier-Smith & Chao (2006) place labyrinthuleans in a basal heterotrophic clade that also includes bicoecids and opalozoans and is sister to the remaining heterokonts. Labyrinthuleans are therefore not even close relatives of the other “ex-fungal” chromists in the Pseudofungi.

Labyrinthuleans have relatively little economic significance to humans. Some labyrinthuleans attack hosts of economic significance to humans, such as bivalves or golf course turf. Oils from the thraustochytrialean Schizochytrium contain one of the current dietary buzzwords, omega-3 fatty acids, so commercial growth of Schizochytrium is used to produce dietary supplements and alternatives to fish oils. Interestingly, webpages, patents, articles, etc. referring to such uses of Schizochytrium seem to invariably refer to it, somewhat misleadingly, as an ‘alga’, and the product as ‘algal oil’. This strikes me as only a marginal improvement over ‘fungus’.

Return of the slime-nets
Published 19 May 2008
Vegetative cells of Labyrinthula terrestris within epidermis of Poa trivialis. Scale bar = 10 µm. Photo from Bigelow et al. (2005).

As alluded to above, the vast majority of known labyrinthuleans are marine, a habitat in which they appear to be pretty much ubiquitous (Raghukumar 2002). It is thought that within the marine habitat labyrinthuleans mostly act as decomposers, living by breaking down and extracting nutrients from dead plant, algal and animal matter. They are very effective in this role—for instance, thraustochytrids are capable of breaking down sporopollenin, the extraordinarily resistant polymer that coats pollen grains. However, because labyrinthuleans in such a role have little direct effect on humans (though their significance to nutrient cycles vital to other organisms that are significant to humans is probably considerable), this is not how they have been most studied. Instead, much more attention has been given to their interactions with living organisms as commensals or pathogens.

Despite numerous records of labyrinthuleans as pathogens, it seems likely that in the majority of cases they are not primarily so, but merely facultative. Despite their rapid growth on necrotic algal tissue, growth of thraustochytrids on live algae is minimal or non-existent, even when said algae have been deliberately innoculated with thraustochytrid spores. Raghukumar (2002) postulated that antimicrobial substances produced by healthy plants might effectively keep thraustochytrid growth down. Labyrinthulids are somewhat more aggressive in their relationships with marine plants and algae, but are not necessarily harmful—the species Aplanochytrium minutum, for instance, has been recorded living within the tissues of brown algae without any noticeable adverse effects on the host. Thraustochytrids are also known as pathogens of animals—in many cases, the effects of thraustochytrid infection are not severe except in young animals, but the QPX organism that has caused mass mortality in the clam Mercenaria mercenaria has been shown using molecular means to belong to the thraustochytrids.

Lottia alveus, the seagrass-inhabiting limpet driven to extinction by the seagrass wasting disease epidemic of the 1930s. Reconstruction from here.

A dramatic exception to the generally low-key nature of labyrinthulean pathogenicity reared its ectoplasm in the 1930s. In the early part of that decade, a wasting disease of then-unknown cause devastated populations of the seagrass Zostera marina in the North Atlantic. More than 90% of the seagrass beds on both sides of the Atlantic were wiped out. In some places, the effect was so severe that the ecology of the area affected was completely altered and the seagrass never returned (Short et al. 1987). The indirect effects of this devastation on other organisms, needless to say, were also severe. Migratory waterfowl populations declined, while several commercial fisheries were hard hit—in particular, the scallop fishery on the American eastern seaboard collapsed entirely. At least one species dependent on the seagrass, the limpet Lottia alveus, became extinct as a result of the epidemic. By the 1940s, the epidemic had run its course, and seagrass populations began to recover by the 1950s. The reasons for the wasting disease remained unknown, though it was suggested that abnormally high sea temperatures may have been a factor. It wasn’t until a smaller scale outbreak of seagrass wasting disease in 1986 that Short et al. (1987) were able to show that it was caused by a Labyrinthula species. While the cataclysmic levels of the 1930s have never, thankfully, returned, wasting disease remains a concern for the maintenance of seagrass populations.

Grass infected with rapid blight. Photo by D. Bigelow.

It is a pathogenic species that also provides the sole exception yet known to the otherwise entirely aquatic lifestyle of Labyrinthulea. Rapid blight of cool season lawn turf was first described in California as recently as 1995, and has since been recorded from multiple locations across the southern United States. Once again, the identity of the causative organism was difficult to resolve, but it was eventually described as a new species of Labyrinthula in 2005. How a representative of an otherwise exclusively marine genus came to be parasitising grass in a terrestrial environment remains a complete unknown, though Bigelow et al. (2005) suggested that Labyrinthula may be more common in soil than previously thought, but overlooked due to the difficulty in culturing it.

Systematics of Labyrinthulomycetes

Characters (from Adl et al. 2012): Producing an ectoplasmic network of branched, anastomosing, wall-less filaments via a specialized organelle known as the bothrosome; Golgi-derived scales; biciliate zoospores with lateral insertion in many species.

Labyrinthulomycetes (see below for synonymy)
    |  i. s.: AmphifilidaAB19
    |           |--AmphifilaAB19
    |           |--FibrophrysAB19
    |           `--Sorodiplophrys Olive & Dykstra 1975AB19, KC01
    |         ElniaAS12
    |         Oblongichytrium [Oblongichytrida]AB19
    |         Labyrinthomyxa Duboscq 1921KC01
    |         Pyrrhosorus Juel 1901KC01
    |--ThraustochytridaAB19
    |    |  i. s.: Althornia Jones & Alderman 1972AB19, KC01
    |    |         BotryochytriumAB19
    |    |         MonorhizochytriumAB19
    |    |         ParietichytriumAB19
    |    |         SicyoidochytriumAB19
    |    |--Aurantiochytrium limacinumDL-G16
    |    `--+--+--‘Thraustochytrium’ multirudimentaleC-SC06
    |       |  `--Schizochytrium Goldst. & Belsky 1964C-SC06, KC01
    |       |       |--S. aggregatumLE18
    |       |       `--S. minutumC-SC06
    |       `--Thraustochytrium Sparrow 1936C-SC06, KC01
    |            |  i. s.: T. kinneiMNI02
    |            |--T. pachydermumC-SC06
    |            `--+--T. aggregatumC-SC06
    |               `--+--T. striatumC-SC06
    |                  `--Ulkenia Gaertn. 1977C-SC06, KC01
    |                       |  i. s.: U. profundaMNI02
    |                       |--+--U. visurgensisC-SC06
    |                       |  `--Japonochytrium Kobayasi & Ôkubo 1953C-SC06, KC01
    |                       `--+--‘Labyrinthuloides’ haliotidisC-SC06
    |                          `--+--U. radiataC-SC06
    |                             `--‘Thraustochytrium’ aureumC-SC06
    `--+--Labyrinthuloides Perkins 1973C-SC06, KC01
       |    |--L. minuta [=Labyrinthula minuta]AC97
       |    |--L. saliensAC97
       |    |--L. schizochytropsAC97
       |    `--L. yorkensisAC97
       |--LabyrinthulidaAB19
       |    |  i. s.: Aplanochytrium Bahnweg & Sparrow 1972AB19, KC01
       |    |           |--A. kerguelenseC-SC06
       |    |           `--A. stocchinoiDL-G16
       |    |         StellarchytriumAB19
       |    `--Labyrinthula Cienkowski 1867C-SC06, AS12 (see below for synonymy)
       |         |--L. algeriensisMS98
       |         |--L. macrocystisSMP87
       |         |--L. marinaMS98
       |         `--L. vitollinaMS98
       `--AmphitremidaAB19
            |--Diplophrys Barker 1868C-SC06, LT64 [Diplophryidae]
            |    |--*D. archeri Barker 1868LT64
            |    `--D. marinaC-SC06
            `--Amphitremidae [Amphitrematidae, Amphitreminae]AS12
                 |--Paramphitrema Valkanov 1970G86
                 |    `--P. pontica Valkanov 1970G86
                 |--Amphitrema Archer 1867LT64
                 |    `--*A. wrightianum Archer 1869LT64
                 `--Archerella Loeblich & Tappan 1961 [=Ditrema Archer 1877 non Temminck & Schlegel in von Siebold 1844]LT64
                      `--*A. flavum (Archer 1877) [=*Ditrema flavum]LT64

Labyrinthula Cienkowski 1867C-SC06, AS12 [incl. Labyrinthodictyon Valkanov 1969KC01, Pseudoplasmodium Molisch 1925KC01]

Labyrinthulomycetes [Labyrinthista, Labyrinthulaceae, Labyrinthulales, Labyrinthulata, Labyrinthulea, Labyrinthulia, Labyrinthulidae, Labyrinthulomorpha, Labyrinthulomycota, Thraustochytriaceae, Thraustochytriales, Thraustochytridae]

*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.

[AC97] Azevedo, C., & L. Corral. 1997. Some ultrastructural observations of a thraustochytrid (Protoctista, Labyrinthulomycota) from the clam Ruditapes decussatus (Mollusca, Bivalvia). Diseases of Aquatic Organisms 31: 73–78.

Barnes, R. S. K. 1998. The Diversity of Living Organisms. Blackwell Publishing.

Bigelow, D. M., M. W. Olsen & R. L. Gilbertson. 2005. Labyrinthula terrestris sp. nov., a new pathogen of turf grass. Mycologia 97 (1): 185–190.

[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.

[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.

Dykstra, M. J., & D. Porter. 1984. Diplophrys marina, a new scale-forming marine protist with labyrinthulid affinities. Mycologia 76 (4): 626–632.

[G86] Golemansky, V. G. 1986. Rhizopoda: Testacea. In: Botosaneanu, L. (ed.) Stygofauna Mundi: A Faunistic, Distributional, and Ecological Synthesis of the World Fauna inhabiting Subterranean Waters (including the Marine Interstitial) pp. 5–16. E. J. Brill/Dr. W. Backhuys: Leiden.

[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).

[LE18] Lax, G., Y. Eglit, L. Eme, E. M. Bertrand, A. J. Roger & A. G. B. Simpson. 2018. Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes. Nature 564: 410–414.

[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.

[MS98] Margulis, L., & K. V. Schwartz. 1998. Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth 3rd ed. W. H. Freeman and Company: New York.

[MNI02] Moriya, M., T. Nakayama & I. Inouye. 2002. A new class of the stramenopiles, Placididea classis nova: description of Placidia cafeteriopsis gen. et sp. nov. Protist 153: 143–156.

Raghukumar, S. 2002. Ecology of the marine protists, the Labyrinthulomycetes (thraustochytrids and labyrinthulids). European Journal of Protistology 38 (2): 127–145.

[SMP87] Short, F. T., L. K. Muehlstein & D. Porter. 1987. Eelgrass wasting disease: cause and recurrence of a marine epidemic. Biological Bulletin 173 (3): 557–562.

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