Acantharia

Abstract

Acantharia are marine planktonic unicellular eukaryotes within the Radiolaria and currently encompass nearly 50 genera and 150 species. They are distributed worldwide from subsurface to deep waters and appear to be most numerous in oligotrophic surface waters. Their main distinctive features are an internal star‐shaped skeleton made of strontium sulfate mineral and an amoeboid cell that possesses multiple nuclei, extensive axopods and contractile myonemes. Acantharia feed on a large variety of prey, but some species are mixotrophs through symbiosis with intracellular eukaryotic microalgae, typically the haptophyte Phaeocystis. As part of their life cycle, some taxonomic groups form heavy cysts that rapidly sink to deep waters creating a biogeochemically relevant vertical flux of carbon, strontium and barium. Overall, Acantharia remain poorly studied, and our knowledge of their biology and ecology is still in its infancy.

Key Concepts

  • Acantharia are marine skeleton‐bearing planktonic protists that form a monophyletic taxon among radiolarians within the super‐group Rhizaria.
  • Acantharia have a complex cellular organisation (e.g. presence of myonemes and axopods) and exhibit an internal skeleton made of strontium sulfate (celestite), enriched in barium and composed of spicules that follow a specific geometric pattern (i.e. Müller's law).
  • There are nearly 50 genera and 150 species, distributed in several suborders, and most taxonomic criteria are based on skeleton morphology (e.g. central junction, form and shape of spicules).
  • Acantharia are ubiquitous in the world's oceans, and particularly abundant in surface oligotrophic waters at tropical and subtropical latitudes, but remain largely overlooked due to rapid skeleton dissolution upon cell death and inappropriate sampling methods.
  • Acantharia are primarily grazers with the use of their axopods, but several species are actually mixotrophs as they host intracellular symbiotic microalgae, making them significant primary consumers and producers in pelagic ecosystems.
  • Some acantharian species undergo encystment that is part of the reproduction process in deep waters, creating a biogeochemically significant vertical flux of carbon, nitrogen and strontium in the mesopelagic and bathypelagic zones.

Keywords: protist; strontium; Radiolaria; celestite skeleton; symbiosis; Acantharia; plankton; ocean

Figure 1. Schematic phylogenetic tree of Acantharia based on ribosomal genes (18S and 28S rRNA) from Decelle et al. (, ), showing the match between molecular clades, morphological features of the skeleton (i.e. central junction, presence of symbionts) and the four taxonomic suborders (Holacanthida, Chaunacanthida, Symphiacanthida and Arthracanthida). Note that the central junction of clade IV is not reported here as it is not visible due to dense endoplasm. Morphology of acantharians from clades I and III is unknown as all ribosomal sequences come from environmental plankton community samples. Nonsupported nodes are reported by a surrounded question mark.
Figure 2. General organisation of the acantharian cell and its endoskeleton. (a) Geometric arrangement of the spicules following Müller's law: two quartets of polar spicules (P) alternate with two quartets of tropical spicules (T) and one quartet of equatorial spicules (E). (b) Light microscopy photograph of an acantharian cell (Arthracanthida) hosting endosymbiotic microalgae (small round brown/yellow cells) within the endoplasm. (c) Zoom of a cell portion showing the general ultrastructure: the endoplasm (End) is limited by the capsular wall (Ca), and the ectoplasm (Ect) is covered by the periplasmic cortex (Co). Several nuclei (N) and endosymbiotic microalgae (Mi), which are only present in clades E and F, and in a single species of clade B, are located in the endoplasm. Myonemes (My) are linked to the periplasmic cortex and to the apex of the spicules (S). Thin radiating axopods (Ax) can extend several microns into the surrounding water for prey capture.
Figure 3. A panel of acantharian cells and their various cytoplasmic and skeletal features imaged by light (LM), confocal and scanning electron microscopy (SEM). (a) External view of a living acantharian cell with its periplasmic cortex attached to each spicule of the skeleton; scale bar = 50 µm (Image courtesy of Sébastien Colin; confocal microscopy). (b, c) SEM images of myonemes (indicated by arrows) located at the extremity of a spicule; scale bars = 1 µm. (d–f) LM images of symbiotic acantharians from clade F (Arthracanthida) with intracellular microalgae (yellow cells) belonging to the Haptophyceae genus Phaeocystis; scale bars = 20 µm. (g–l) SEM pictures of different acantharian celestite skeletons from the Chaunacanthida of clade C (g), and the Arthracanthida of clades F (h, i) and E (j–l); scale bars = 30 µm.
Figure 4. Scanning electron microscopy (SEM) images of acantharian skeletons showing the evolution of the central junction (the way the spicules cross the cell) across molecular clades: (a, b) central junction can be loose in clade C, (c) tight with fused spicules in clade D or (d–f) tight and well developed, forming a large central body in most species of clades E and F. Note that acantharians from clades A and B have no central junction (their 10 spicules simply cross the cell), and specimens are therefore very fragile and difficult to observe in SEM.
Figure 5. Reproduction in Acantharia occurs either directly from the adult stage (a–f), or after encystment of the cell (g, h). (a–f) Light microscopy images showing a time lapse of an acantharian cell at the end of a gametogenesis when thousands of swarmers produced within the endoplasm are released in the environment within few minutes; scale bar = 20 µm. (g) Round and (f) elongated acantharian cysts photographed by scanning electron microscopy; scale bars = 20 and 100 µm, respectively. (i) Scanning electron microscopy photograph of an acantharian swarmer with its two flagella; scale bar = 1 µm.
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Further Reading

Boltovskoy D and Correa NM. 2010. Acantharia. Version 28 September 2010. The Tree of Life Web Project. http://tolweb.org/Acantharia/2385/2010.09.28

Decelle J, Colin S and Foster RA (2015) Photosymbiosis in marine planktonic protists (Chapter 19). In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N and Not F (eds) Marine Protists: Diversity and Dynamics. Tokyo: Springer.

Stoecker DK, Johnson MD, de Vargas C and Not F (2009) Acquired phototrophy in aquatic protists. Aquatic Microbial Ecology 57: 279–310.

Suzuki N and Not F (2015) Biology and ecology of Radiolaria (Chapter 8). In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N and Not F (eds) Marine Protists: Diversity and Dynamics. Tokyo: Springer.

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Decelle, Johan, and Not, Fabrice(Nov 2015) Acantharia. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0002102.pub2]