Vampyrellida

All known vampyrellids are heterotrophic amoebae with a free-living (non-parasitic) life cycle that lacks flagellate stages, except for Lateromyxa gallica, and is characterized by an alternation between mobile and immobile cellular stages:[3]

• The mobile, amoeboid cells, called 'trophozoites' or 'swarmers'[lower-alpha 1] in old literature. Their main activity is to disperse, search and gather food through phagocytosis.[3]

• The immobile but highly metabollically active 'digestive cyst' stage, that appears after the feeding. In some species it is called a 'resting phase', but it is different from a true resting cyst (or spore) that is metabollically inactive to survive adverse conditions. To reach this stage, the trophozoite retracts its filopodia, secretes a layered cell wall, and strongly attaches itself to the substrate or floats freely. Either a central main vacuole or multiple separate vacuoles appear to digest the food. The cytoplasm color may change to a bright red, orange or yellow color, or remain colorless. When the digestive phase is finished, one or multiple trophozoites hatch from the cyst through holes in the cell wall.[3]

In some species, near the end of the digestive cyst stage, asexual reproduction takes place inside the cyst through a cell division (called 'internal plasmotomy'), resulting in 2–4 daughter cells. These cells are released as young trophozoites through the holes. Other species do not divide inside the closed cyst, and instead divide during or after the hatching process ('external plasmotomy'). Lateromyxa gallica shows an unusual mode of reproduction: while feeding on the inside of algal cells, the plasmodia shed and develop into digestive cysts.[3]

There is a lack of evidence for sexual reproduction in vampyrellids, except for some meiotic stages in resting cysts revealed in Lateromyxa gallica through ultrastructural studies.[5]

Many vampyrellid species have more than one nucleus and behave like plasmodia. They can fuse their cells upon contact, and split apart when moving in opposite directions. Some species readily grow plasmodia as large as a Petri dish under laboratory conditions, while others only fuse when the cell density is high and the food availability is low. It is uncertain to what extend this can happen in the natural environment. In contrast, Placopus species are rarely ever seen with more than two nuclei.[3]

Under adverse environmental conditions, vampyrellids can transform into several types of resting stages:[3]

• Hypnocysts, thin-walled and devoid of food content, formed when the trophozoite is disturbed by external stress.[3]

• Secondary cysts, thin-walled and devoid of food content, formed as a result of starvation.[3]

• True resting cysts, also called 'sporocysts' or 'spores' in old literature. They form in natural samples and old cultures, when there is no food or the conditions are unfavorable. They build several cyst walls and condense their cellular contents. They can survive events of desiccation or freezing, up to at least three years.[3]

Vampyrellids have a cosmopolitan distribution: they appear in all continents except Antarctica and all marine ecosystems. They inhabit a wide range of marine, brackish and freshwater habitats, and are frequently isolated from soil samples.[3] Marine ecosystems hold a surprisingly high diversity,[6] and they are found mostly in benthic habitats (e.g. tidal pools, diatom lawns, associated with red algae...). There is a significant positive correlation between the diversity of Vampyrellida and the nutrient availability in the sediment.[7] According to environmental sequencing vampyrellids colonize neotropical soil,[8] glacial cryoconite systems,[9] Brassicaceae leaves,[10] Sphagnum-inhabited peat bogs,[11] hydrothermal sediments[6] and the deep sea.[12]

Trophozoite (left) and digestive cyst (right) of Vampyrella pendula on a Oedogonium filament

Vampyrellids display a great trophic diversity. They are predators of a long list of organisms of diverse evolutionary affinities, structures and sizes, including chlorophyte and streptophyte green algae, diatoms, chrysophytes, cryptophytes, euglenids, heterotrophic flagellates, ciliate cysts, fungal hyphae and spores, yeasts, and even micrometazoa such as nematodes and rotifer eggs. Bacterivory is rare and mostly involves filamentous cyanobacteria. Though there are generalist omnivorous predators such as Leptophrys, some vampyrellid species are specialized predators; for example, the algivorous Vampyrella and Placopus are restricted to few species of hard-walled green algae, while Arachnomyxa and Planctomyxa prefer Volvocales and euglenids.[3]

Vampyrella lateritia extracting algal cell content with a pseudopodium (arrow)

Vampyrellids have evolved strategies to deal with relatively large bulky prey that are difficult to consume. They display at least four different feeding strategies to engulf entire prey or to devour the contents of other eukaryotic cells. These feeding strategies are not mutually exclusive, and the same species can display each with a different type of prey.[3]

• Free capture. Similarly to amoebae of other supergroups, they catch and enclose their prey within a food vacuole by usual phagocytosis. Some can paralyse their prey before the enclosement. The size of the enveloping is widely varied, from numerous small cells at the same time to entire nematodes or colonial green algae.[3]

• Colony invasion. They attach to the colonies of volvocalean algae, dissolve and penetrate the extracellular gelatinous mucilage matrix, and phagocytose individual cells inside the colony. Possibly for protection against predators, they transform into digestive cysts inside of the colony.[3]

• Protoplast extraction, the most famous strategy. They specifically remove, ingest and digest the cellular contents of their prey, always by dissolving the prey's organic cell wall or simply displacing the prey's siliceous wall, and invading through pseudopodia (called 'calyculopodia') to remove the cell contents . Some species eject the prey cytoplasm by applying pressure, a process known as 'plasmoptysis', which is followed by a rapid formation of a large vacuole. This process resembles a sucking motion, and is likely the reason for their comparison to vampires. In marine species no plasmoptysis is observed, which suggests that the osmotic pressure given by salinity is important for plasmoptysis.[3]

• Prey infiltration. Similarly to protoplast extractors, they perforate the cell wall of an algal prey, but invade the cell itself and completes the cycle within it. Some are able to move laterally from one cell to the next in filamentous prey. They divide into smaller portions that turn into digestive cysts.[3]

Vampyrellida represents one of the major groups of free-living amoebae, phylogenetically separate from other groups of amoebae such as Amoebozoa, Heterolobosea and Nucleariidae. Instead, Vampyrellida is an isolated clade within the Rhizaria supergroup.[26] They are the closest relatives of the Phytomyxea, parasites of plants and algae that, unlike vampyrellids, disperse through flagellated stages during their life cycle and spend most of their active life within host cells.[3] Current classifications place both Vampyrellida and Phytomyxea, along with other small groups of Rhizaria, within the phylum Endomyxa.[4] Several phylogenetic analyses have recovered a sister group relationship between Vampyrellida and Phytomyxea and have named their clade Proteomyxia[1] or Phytorhiza.[27]

There are currently at least 50 credible vampyrellid species distributed in 10 genera, scattered across five well-established clades found through genetic data, four of which are families. Despite the advances, most of the vampyrellid diversity is still unknown or undescribed.[3]

• Family Vampyrellidae Zopf 1885 emend. Hess, Sausen et Melkonian 2012[2]
  • Vampyrella Cienkowski 1865 (20 species)
• Family Leptophryidae Hess, Sausen & Melkonian 2012[2]
  • Arachnomyxa Hess 2017 (1 species)
  • Leptophrys Hertwig & Lesser 1874 (3 species)
  • Planctomyxa Hess 2017 (1 species)
  • Platyreta Cavalier-Smith & Bass 2008 (1 species)
  • Theratromyxa Zwillenberg 1952 (1 species)
  • Vernalophrys Gong et al. 2015 (1 species)
• Family Placopodidae Jahn 1928 = Hyalodiscidae Poche 1913 = lineage B3
  • Placopus Schulze 1875 = Hyalodiscus[lower-alpha 2] Hertwig & Lesser 1874 (6 species)
• Family Sericomyxidae More, Simpson & Hess 2021
  • Sericomyxa More, Simpson & Hess 2021 (1 species)
• 'Thalassomyxa clade' = lineage B5
  • Thalassomyxa Grell 1985 (3 species)
• Genera that likely belong to Vampyrellida but for which there is no genetic data, and are thus considered incertae sedis:
  • Arachnula Cienkowski 1856 (2 species)
  • Asterocaelum Canter 1973 (1 species)
  • Gobiella Cienkowski 1881 (2 species)
  • Lateromyxa Hülsmann 1993 (1 species)
  • Monadopsis Klein 1993 (1 species)
  • Penardia Cash 1904 (2 species)

The following taxa have been associated with Vampyrellida, but their placement is uncertain or might not belong to the group.[3]

• Hyalodiscus angelovica Sawyer 1975
• Hyalodiscus caeruleus Schaeffer 1926
• Hyalodiscus foliaceus Lepsi 1931
• Hyalodiscus korotnewi Mereschovsky 1879
• Hyalodiscus macronucleus Lepsi 1931
• Hyalodiscus minimus Lepsi 1960
• Hyalodiscus placopus Hülssmann 1974 [not Paragocevia placopus (Page & Willumsen 1980) Page 1987]
• Hyalodiscus simplex Wohlfarth-Bottermann 1977
• Vampyrella chaetoceratis (Paulsen 1910) Ostenfeld 1913 [Apodinium chaetoceratis Paulsen 1910; Paulsenella chaetoceratis (Paulsen 1910) Chatton 1920]
• Vampyrella labyrinthuloides (Archer 1875) Valkanov 1940 [Chlamydomyxa labyrinthuloides Archer 1875]
• Vampyrella montana (Lankester 1896) Valkanov 1940 [Chlamydomyxa montana Lankester 1896]
• Vampyrellidium perforans Surek & Melkonian 1980 (nucleariid amoeba)
• Vampyrellidium vagans Zopf 1885 (nucleariid amoeba)
• Vampyrellidium roseus (Trichense 1885) Schepotieff 1912 [Protogenes roseus Trichense 1885]
• Vampyrina buetschlii Frenzel 1897