DESCRIPTION OF THE PHYLUM APICOMPLEXA

EUKARYA> CHROMALVEOLATA> ALVEOLATAE> APICOMPLEXA

Apicomplexata (a-pi-com-plex-A-ta) is derived from two Latin roots that mean the top (apex) infolds (complexus). The reference is to a set of organelles at the tip of the spindle-shaped sporozoite (Figure 1), a mobile stage in the life cycles of these organisms.

INTRODUCTION TO THE APICOMPLEXA

Apicomplexans are parasites that inhabit a variety of animals, and, economically, they are among the most important organisms on earth. They cause diseases that can devastate populations of humans and their livestock. Malaria alone is responsible for 2-3% of annual human death, most in sub-Saharan Africa (World Health Organization, 2010 Malaria Report); however, the infection rates can range as high as 35%.

Most of the apicomplexans have a life history which can be quite elaborate and require more than one host (see Figure 1A. for a general life cycle of Apicomplexa). The fusion of gamonts precedes the formation of a cyst within which oogamous reproduction occurs. Motile sperm have one or two posteriorly-directed flagella (Figure 1.B.), though some taxa have lost the flagella altogether and a few have three flagella. Following fusion, the zygote undergoes meiosis in the formation of sporozoites, making the life history haplontic. Much of the reproduction when in the infective stages is through asexual means. The fundamental apicomplexan cell is represented by the sporozoite (Figure 1.C.). The cell covering is alveolar with perforations called micropores. The anterior end of the cell has a set of organelles, which together make up the apical complex. The apex of the cell has a small opening called a polar ring, which is supported in many taxa by series of supporting microtubules called a conoid . Characteristic rows of vesicles, micronemes , appear to be secretion bodies derived from the goli apparatus. Associated with the micronemes are rhopteries , which likely facilitate the secretion of materials necessary for the entry of the cell into the host cell.

Apicomplexans fall into two large clades: Gregarines + Cryptosporidians and Piroplasmids-Haemosporidians + Coccidians (see Figure 2). The topology of Figure 2 is based on Perkins and Keller (2001), Kuvardina et al. (2002), Leander et al. (2003a and 2003b), Kuo et al. (2008), Morrison (2009), and Rueckert and Leander (2009). Aside from Rueckert and Leander (2009) few phylogenetic studies have been made with a broad range of taxa. We have included the chromerids and colpodellids in the phylum because they consistently emerge as basal groups in the Apicomplexa clade.

FIGURE 1. Sprorzoite Structure and General Life Cycle of Apicomplexa
A	B
C	A. GENERAL LIFE CYCLE. 1-zygote, 2-sporozoite generation, 3-merozoites, 4-gametes. B. A scanning electron micrograph of an Eimeria sperm. F= flagella; N= nucleus. C. SPOROZOITE STRUCTURE. Structure of an apicomplexan sporozoite. 1-polar ring, 2-conoid, 3-micronemes, 4-rhoptries, 5-nucleous, 6-nucleolus, 7-mitochondria, 8-posterior ring, 9-suppedicular microtubules, 10-golgi apparatus, 11-micropore.
Images A and C by Franciscosp2 and placed in the Public Domain; C is from a figure in Ferguson et al. (2008).

FIGURE 2. A simplified phylogeny of major groups in the Apicomplexa (taxa in shaded box) within the Alveolata (clade A and all taxa in bold). The cladogram is a consensus drawn from Perkins and Keller (2001), Kuvardina et al. (2002), Leander et al. (2003a and 2003b), Kuo et al. (2008), Morrison (2009), and Rueckert and Leander (2009).

CHROMERIDA

Basal groups of apicomplexans have both photosynthetic (chromerids) and free-living taxa (colpodellids). Chromerida, considered to be a new phylum by Moore et al. (2008), has only a few described species, but they may harbor a large hidden diversity. So far, taxa of the chimerids are all photosynthetic symbionts of corals of the Great Barrier Reef (Obornik et al 2011. They are photosynthetic, but lack chlorophyll c, a characteristic of photosynthetic chromalveolates. Janouškovec et al. (2010) suggest that members of this group represent the ancestral condition from which the dinoflagellates, apicomplexans, and heterokonts evolved by the secondary acquisition of a red algal symbiont, which occurs in many taxa that are no longer photosynthetic (e.g. malaria) but carries out other metabolic functions (Gleeson 2000; Lim and McFadden 2010).

Chromerids (e.g. Chromera and Vitrella) are photosynthetic cells that have a life history which is reminiscent of the Heterokontae. Obornik et al. (2012) report a fairly simple life history for Vitrella in which vegetative cells may produce autospores within the vegetative cell wall or they may also form a zoosporangium and release biflagellated zoospores (see Figure 3). The motile cells of both Chromera and Vitrella are biflagellated (anteriorly-directed and posteriorly-directed flagella) and share features with the colpodellids and perkinsids.

FIGURE 3. Vitrella cells from culture. OP= circular operculum on the cell, ASP= autosporangium, ZSP= zoosporangium, VC= vegetative cell.
Image from Obornik et al. (2012), Figure 2

COLPODELLIDS

Colpodellids are biflagellated free-living cells that feed on small eukaryotes and bacteria. The cells have the typical alveolate pellicle with micropores and an arrangement of trichocysts (Myl’nikova and Myl’nikov 2009) and alveolar sacs that appear similar to that of gymnodinoid dinoflagellates (Leander et al. 2003b). Furthermore, they have ultrastructural characters that place them in the apicomplexa: a polar ring, conoid, rhopteries, and micronemes. These taxa seem to be able to feed by drawing out cellular contents of the prey items through myzocytosis (sucking out cellular contents by means of a feeding tube) the arrow in Figure 4 points to the feeding tube).

Though they are typically reported as free-living, Yuan et al. (2012) report a Colpodella species as the causative agent of relapsing infection in China. Similar strains were found in the stools of calves with diarrhea. Thus, it appears that some colpodellids might be obligate parasites of vertebrates.

FIGURE 4. Colpodella, a free-living predatory biflagellate cell.
Size bar = 1.5µm
Image from Leander et al. (2003).

CRYPTOSPORIDIA

Cryptosporidium is best known for being an opportunistic parasite for those whose immune system is compromised by HIV AIDS. They infect cells of the intestinal mucosa of many vertebrates, including livestock and fish (Alvarez-Pellitero and Sitja-Bobadilla 2002; Fayer 2010). They tend to be spread by the ingestion of infective spores (Figure 5) from contaminated water.

Once considered to be coccidians, molecular phylogenetics has placed them as an early-diverging group (Zhu et al. 2000; Leander et al. 2003) or associated with the gregarines (Rueckert and Leander 2009). Like many gregarines, cryptosporidians use a single host in which to complete their life cycle; however, unlike the gregarines, cryptosporidians utilize vertebrate hosts. Cryptosporidians are unusual in that some species have mitochondria that have no DNA and they have no apicoplasts (reduced chloroplasts that are typical of apicomplexans). [See Life History of Cryptosporidium by CDC]

FIGURE 5. Cryptosporidium oospores.
Size bar = 10µm
Image from Ren et al. (2011).

GREGARINES

The gregarines, typically parasites of arthropods, mollusks, and annelids, have relatively simple life cycles (e.g. Monocystis, see Figure 6). The trophozoite develops within a cell into a plasmodium and divides into merozoites by schizogony. Merozoites are released by lysing the host cells and then invade other cells. Typically, these cycles occur in cells that line the lumen of the gut or other ducts. Eventually, gamonts (Figure 7 in gut of meal worm) are formed and emerge from the host cells to group together in the lumen by a process called syzygy . Together, each gamont forms multiple gametes which fuse and form zygocysts (also called oocysts), which are expelled to be taken up by another host.

Mattesia has a life history similar to that of Monocystis, but Mattesia remains in the haemocoel of its insect host. The zygocysts are released when the dead host decays or is eaten by another insect. Figure 8 shows a Fire Ant (Solenopsis invicta) whose head has turned yellow with the concentration of zygocysts inside. When ingested by a potential host, sporozoites emerge from the zygocyst and invade the cells of the lumen wall. [See also the life history of Stylocephalus.]

FIGURE 6. The lifecycle of Monocystis. The earthworm, the single host for this organism, swallows the spore. In the gizzard, the spore releases sporozoites which burrow through the intestinal wall and get into the circulatory system. They travel to the testes where they infect sperm mother cells and then release more sporozoites. Some become gametocytes producing spores that leave the sperm duct and remain infective in the soil.
Image from Olsen (1967)


FIGURE 7. Gregarina gamonts joining in the gut of infected mealworms. Image from Systematics Biodiversity Image Archive	FIGURE 8. (left) Zygocysts of Mattesia from the haemolymph of a Fire Ant. (right) Fire Ant filled with the yellow zygocysts of Mattesia. Image from Pereira et al. 2002.

COCCIDIANS

Coccidians have life histories that are similar to those of the gregarines; however, they tend to infect vertebrate hosts. Like the gregarines, coccidians invade epithelial cells of the gut or other things like the gall bladder duct (see Figure 9). The animal ingests a zygocyst from which sporozoites emerge and invade appropriate cells. The epithelial cycle continues as in the gregarines (see developing schizonts of Eimeria in Figure 10), but is different in the formation of the zygote. The trophozoite enlarges in some of the epithelial cells to form a functional egg, called a macrogamete. Other gametocytes release multiple sperm (also called microgametes), which fertilize the macrogametes. The resulting zygocyst emerges from the cell by lysing it and passes outside the body, usually with the feces. Coccidial diseases are very important disease agents for the domestic animals, particularly dogs, cats, cattle, rabbits, and poultry. Coccidiosis most often manifests itself by diarrhea and can lead to death of the host. [For more detail, see the life history of Eimeria.]

FIGURE 9. The life cycle of Eimeria in a bird host. The bird swallows a spore that germinates in the gut to release sporozites which invade the epithelial cells lining the caecum, a pocket at the junction of the large and small intestine. There, they go through the extended epithelial phase, invading more and more epithelial cells. Then, some of the plasmodia become gamonts which produce microgametes (sperm) and macrogametes (eggs). The zygote develops into the spore which leaves with the feces.

From Olsen (1974)

FIGURE 10. Eimeria early schizont in the bile duct of a rabbit.
Image from http://ww2.sjc.edu/faculty_pages/cmorgan/Parasitology/

Toxoplasma is a coccidial organism that alternates between cats and mice. The typical epithelial cycle occurs in the cat, but zygocysts which have passed out in the feces of the cat “germinate” when consumed by a mouse. The sporozoites go into a blood infective stage and feed on rbc’s (red blood cells; see Figures 11 and 12). When the mouse is eaten by a cat, the merozoites in the bloodstream of the mouse invade the intestinal epithelial cells and the cycle continues. The danger to humans is that Toxoplasma zygocysts can germinate in the gut of anyone who handles cat feces (cat boxes, or even cats that have recently defecated). The sporozoites in the human system behave as though we are mice and begin an erythrocytic cycle. In most cases a healthy human can fight off a Toxoplasma infection. However, Toxoplasma can cross the placental barrier in a pregnant woman and cause death of the fetus. [For more detail, see life history of Toxoplasma.]

FIGURE 11. A thick blood smear of Toxoplasma. The rbc’s have been removed by acetic acid.
Image from http://ww2.sjc.edu/faculty_pages/cmorgan/Parasitology/

FIGURE 12. The typical life cycle of Toxoplasma. In short, the primary host is the cat or other carnivores in whom a typical epithelial infection occurs in the intestine. Spores are expelled and become infective oocysts in the feces. The oocyst can be eaten by any number of small mammals or birds and go through a stage that infects red blood cells. Infected prey are then eaten by the cat and sporozoites invade the intestinal epithelium. Oocysts can be taken up by the cat and develop directly into an intestinal infection.

Image from Grell 1973.

HAEMOSPORIDIANS AND PIROPLASMIANS

Haemosporidians typically have complex life cycles that alternate between an arthropod and a vertebrate host. Malaria (Plasmodium spp.; Figure 13), one of the most important diseases of humankind, is a haemosporidian. The trophozoite (Figure 14), or feeding stage occurs in the red blood cell (rbc). Tertian malaria, caused primarily by Plasmodium vivax, typically invades a rbc as a spindle-shaped cell called a merozoite, which enlarges and forms a plasmodium. After three days, the plasmodium breaks apart in a process called schizogony and then lyses the rbc to release more merozoites. Plasmodium vivax is synchronous in its infective cycle. During day 1 of this cycle, the infected person has chills and fevers as the waste products of the lysed cells flood into the circulatory system. On day 2, the person feels weak, but improves as the toxins are removed and lost rbc’s are replaced. Day 3 begins with the person feeling almost normal until another round of cell lysis begins. Some of the developing plasmodia form gametocytes, which concentrate in the peripheral blood. There, they are taken by a mosquito during its blood meal. The macrogametocyte forms eggs and the microgametocyte forms sperm in the gut of the mosquito. Syngamy forms a zygote called an ookinete that breaches the gut wall and forms an oocyst which develops into many sporozoites in the haemolymph. The sporozoites concentrate in the salivary glands from which they are injected into the blood of another person. Initially, the sporozoites invade liver cells where they go through a cycle of plasmodium and merozoites as in the erythrocytic stage, but this stage produces almost no symptoms. They can stay in the liver cycle for up to 20 years before they again break out into the circulatory system and the cycle of chills and fevers begins. [For more detail, see life history of Plasmodium.]

FIGURE 13. The life cycle of tertian malaria. A-H illustrates the erythrocytic stages from the early ring stage, the plasmodium and then the formation of merozoites. I and J are the macrogametocyte and microgametocytes, respectively. When taken up by an Anopheles mosquito, go through sexual fusion and the formation of sporozoites that infect the salivary glands. Again, while feeding, the adult Anopheles injects sporozoites into the circulatory system. These invande the liver and go therough a protracted liver stage from which the erythrocytic develops.

FIGURE 14. Plasmodium in a human blood smear. The ring stages are trophozoites. The large staining objects are gametocytes.
Image from http://www.zoology.ubc.ca/courses/bio332/Labs/Apicomplexa/plasmodium/

Malaria is limited on earth mainly by the range of the particular mosquitoes that can serve as hosts. For Plasmodium, that is the Aedes mosquito, which occurs mainly in tropical and subtropical climates. The great European powers of the 18th and 19th centuries found that in their acquisition of lands in the building of empires, they had to contend not only with the people who occupied those lands, but with the diseases that they encountered. In the tropics, one of the most important diseases was malaria. This was much more than a nuisance. Britain found that when it tried to occupy areas where tertian malaria was common, as in India, they had to field three times more troops than they would otherwise because many were down for two of the three days. A “cure” was found in the extract of the bark of the cinchona tree of South America. The substance was quinine, which the British called tonic [This was the source of gin and tonic]. However, quinine does not really cure the person infected, but it prevents the liver stage from breaking out into the symptomatic erythrocytic stage. Even today, malaria remains a scourge on humankind. According to the CDC, 350-500 million cases of malaria occur worldwide, and over one million people die, most of them young children in sub-Saharan Africa.

Babesia follows a life cycle similar to that of Plasmodium and is the causative agent of Texas Fever in cattle. The vector or intermediate host is the cattle tick. The erythrocytic cycle occurs in cattle (Figure 15). [See the life history of Babesia.]

FIGURE 15. blood smear of a bovid showing the trophozoite rings of Babesia.
Image from http://www.ulb.ac.be/sciences/biodic/images/protozoaires/babesia.jpg

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By Jack R. Holt. Last revised: 03/01/2016

Diversity of Life

DESCRIPTION OF THE PHYLUM APICOMPLEXA

DESCRIPTION OF THE PHYLUM APICOMPLEXA (LEVINE 1970)

DESCRIPTION OF THE PHYLUM APICOMPLEXA (LEVINE 1970)

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