Centrohelid
The centrohelids or centroheliozoa are a group of heliozoan protists, single-celled eukaryotes with stiff radiating arms supported by microtubules and bearing extrusomes. Their cells are spherical, ranging from 3 to 150 μm. Unlike other heliozoa, centrohelids lack flagella, have flat ribbon-shaped mitochondrial cristae, and arrange their microtubules in hexagons or triangles. Their microtubule-generating organelle, the centroplast, has a unique shape with a central trilamellar disc surrounded by two hemispherical caps. Some are naked or covered in a mucous coat, but most centrohelids produce cell coverings, namely organic spicules and siliceous scales of various species-specific shapes. Several species form colonies.
Centrohelids are passive predators with a cosmopolitan distribution. They feed on bacteria, other protists, and invertebrate larvae by phagocytosis; they can merge several cells around a larger prey to ingest it. Although they have been studied in aquatic environments, they are more diverse in soil habitats. They include both free-floating and benthic forms, some of which attach to the substrate by a stalk.
Centrohelids are the closest relatives of the haptophyte algae, together forming the clade Haptista. Both groups have mineralized scales and at least one thin microtubule-based appendage. The common ancestor of centrohelids lost flagella and probably produced the two known types of cell coverings, organic spicules and complex siliceous scales. Some species can still produce both, while others secondarily lost or simplified them.
In biological classification, centrohelids compose the taxon Centroplasthelida, in reference to their centroplast. Around 130 species have been described, but they only represent about 10% of the total estimated diversity, according to environmental DNA surveys. They are classified in 11 families grouped into two major clades, Pterocystida and Panacanthocystida.
Characteristics
Centrohelids are heliozoans or "sun animalcules", a type of single-celled organisms that have axopodia, narrow stiff projections radiating from the cell and granting a sun ray appearance. These axopodia are internally supported by bundles of microtubules and bear visible extrusomes, organelles involved in the capture of prey, known as kinetocysts in centrohelids. Their cells are spherical, ranging in size from 3 μm to 150 μm.Centrohelid heliozoa are distinguished from other heliozoa by the absence of flagella and by several cellular features. One is their flat, ribbon-shaped mitochondrial cristae. Another is a uniquely shaped microtubule-organizing center, the organelle responsible for generating the axopodia. The MTOC of centrohelids, known as the centroplast, is located at the center of the cell and has a unique inner differentiation of a central trilamellar disc sandwiched between two dense hemispherical structures, each around 0.1–1.5 μm in diameter. Centrohelids are also distinct in the arrangement of their axoneme-forming microtubules into hexagons and triangles.
A few centrohelids are naked or with a mucous coat. The majority are able to produce two kinds of cell coverings: organic spicules and siliceous scales, which are generated in diverse shapes. The specific shape of the siliceous scales of many centrohelids helps identify the species. Some centrohelids bear both scales and spicules, either simultaneously or throughout their life cycles.
Some centrohelids have a mucous stalk to attach to the substrate. Some form colonies, with individual cells connected by cytoplasmic bridges, each cell with their own layer of spicules or scales. An exception is Yogsothoth: its colonies lack any bridges, and instead contain a roundish mass of densley packed cells surrounded by a thick outer layer of scales that differ from the inner plate scales covering each cell.
Although centrohelids have only one cell nucleus in normal conditions, multiple centrohelid cells have been observed fusing their cytoplasms to engulf a larger prey, resulting in a multinucleated cell.
Nutrition
Centrohelids feed on bacteria, other protists, and even larvae of invertebrates, through phagocytosis. They are considered passive feeders, capturing prey as they pass by. Experiments studying the feeding behavior of centrohelids are rare, but they have been observed consuming environmentally impactful strains of cyanobacteria, such as Microcystis aeruginosa and Aphanizomenon. This predation is interesting due to its potential to regulate harmful algal blooms caused by such cyanobacteria. In mixed cultures of centrohelids and actinophryids, another group of heliozoan passive feeders with the same ecological niche, the centrohelids outcompete actinophryids, causing a sharp decline in their population. Centrohelids can also fuse with more centrohelid cells to ingest actinophryid cells. Actinophryids actively avoid centrohelids, suggesting that they perceive centrohelids as threats.One marine centrohelid genus, Meringosphaera, practices kleptoplastidy, i.e., temporarily seizes chloroplasts from its prey cells to use them for photosynthesis. In particular, it retains plastids from different green-colored algae of the class Dictyochophyceae. Despite the retainment being temporary, some of the genes associated with the retained plastids have been transferred to the centrohelid host's nucleus ; this feature is a major step in the transition towards acquiring permanent plastids.
Ecology
Centrohelids are free-living predatory protists with a ubiquitous distribution. They are found abundantly in global freshwater environments, and also occur widely in marine and soil habitats, where they are comparatively understudied. Despite their ubiquity, little is known about their biogeography. Most reports of centrohelids are done in temperate zones due to insufficient studies in tropical regions. Within temperate regions, the species diversity of freshwater centrohelids appears to be influenced by the type of body of water: highest diversity occurs in terrace forest lakes, while Sphagnum peat bogs have the lowest diversty. According to environmental DNA analyses, soil-dwelling centrohelids are twice as diverse as their freshwater counterparts, and ten times more than marine ones.Like other heliozoans, most known species are found in aquatic benthic environments, where they prey on a variety of other microbes. Some float in the water column, while others attach to substrates by a stalk. Free-floating forms are well known, but the ecological niche of centrohelids is considered to be the benthos, inhabiting the superficial layer of detritus and interstitial spaces.
Evolution
Before molecular phylogenetics, centrohelids were grouped with other axopodial protists in the polyphyletic taxon Heliozoa. Over the 1990s and 2000s decades, smaller heliozoan groups were removed from this artificial taxon and into their true evolutionary lineages, particularly Stramenopiles and Rhizaria. The centrohelids, the largest heliozoan group, remained difficult to resolve, and could not be placed within any other phyla.With the first 18S rRNA gene sequences of centrohelids, weakly supported analyses indicated some affinities to bikonts, and they were suggested to have evolved from bikont flagellates such as ancyromonads. Based on further low-support 18S rRNA analyses and some cellular similarities, a relationship with haptophytes was later suggested, but phylogenetic trees were generally inconsistent. They also branched with telonemids and cryptomonads in a clade known as CCTH, later renamed Hacrobia.
In the 2010s, the monophyly of Haptista was further confirmed with maximal support in larger-scale phylogenomic analyses, and Hacrobia was found to be paraphyletic. Haptista branches closer to the SAR supergroup, while the clade containing cryptomonads and their relatives, Cryptista, is closer to plants. An elusive microheliozoan, Microheliella maris, previously suggested to be a possible centrohelid relative, branches next to Cryptista instead. All these groups belong to the large eukaryotic clade Diaphoretickes, from which all heliozoa are presumed to have evolved.
Traits present in haptophytes are inferred as the ancestral state of centrohelids. Both have an outer coat of complex mineralized scales: calcareous in haptophytes, siliceous in centrohelids. Another common feature is the presence of a thin microtubule-based appendage used for feeding: the axopodia in centrohelids, and the haptonema in haptophytes. Centrohelids evolved from a common flagellate ancestor that secondarily lost its flagella, and was probably capable of producing both siliceous scales and organic spicules.
Taxonomy
Nomenclature
The centrohelids compose the taxon Centroplasthelida, described by protistologists Colette Febvre-Chevalier and Jean Febvre in 1984, in reference to the centroplast that characterizes them among other heliozoa. A similar earlier name Centrohelida, established by Kühn in 1926, is not preferred because it includes both centrohelids and gymnosphaerids. A modified version of this name, Centrohelea, was used by some authors, especially Thomas Cavalier-Smith. The synonym Centroheliozoa was coined by Monika Dürrschmidt and David J. Patterson in 1987, and is used as an alternative common name for the group.History
Traditionally, the classification and species identification of centrohelids has been based upon the morphology of their cell coverings. According to the main cell covering types, three families were distinguished before molecular phylogenetics: "Heterophryidae", either naked or covered in organic spicules, proposed as the most primitive family; "Raphidiophryidae", interpreted as more derived, with tangential siliceous plate-scales; and "Acanthocystidae", interpreted as the most derived, with the most complex coverings, including a double layer of siliceous scales.With the first molecular analyses using the 18S rRNA gene, and the first sequence of a naked centrohelid, centrohelids were divided into two orders based on the presence of insertions in this gene: Acanthocystida and Pterocystida, both containing species with and without silica scales. The hypothesis for the ancestral centrohelid changed from a naked or spicule-bearing form to a form capable of producing complex coverings, secondarily lost or simplified. As such, "Acanthocystidae" represented the paraphyletic ancestral state, and "Heterophryidae" the polyphyletic derived state. Only Raphidiophryidae remained monophyletic, while the remaining centrohelids were grouped in new monophyletic families, including a modified Heterophryidae and Acanthocystidae.
The discovery and sequencing of new centrohelids led to updates in their higher classification. The circumscription of several families was modified to match molecular data. New relatives of Acanthocystida were grouped in a larger clade Panacanthocystida. In the clade Pterocystida, families were briefly grouped into two orders: Raphidista, later abandoned due to the lack of phylogenetic support, and Pterista, still accepted. The two major clades, Pterocystida and Panacanthocystida, are often considered superorders.