| List of Plasmodium species | |
|---|---|
| Scientific classification | |
| Domain: | Eukaryota |
| Kingdom: | Chromalveolata |
| Superphylum: | Alveolata |
| Phylum: | Apicomplexa |
| Class: | Aconoidasida |
| Subclass: | Haemosporidiasina |
| Order: | Haemosporida |
| Suborder: | Laveraniina |
| Family: | Plasmodiidae |
| Genus: | Plasmodium |
| Species | |
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see text |
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The genus Plasmodium is a member of the order Haemosporidia. It is the largest genus within this order and currently consists of over 250 species.
The species in this genus are entirely parasitic with part of their life cycle spent in a vertebrate host and another in an invertebrate host - usually a mosquito. Vertebrates infected by members of this genus include mammals, birds and reptiles.
Host range among the mammalian orders is non uniform. At least 29 species infect non human primates; rodents outside the tropical parts of Africa are rarely affected; a few species are known to infect bats, porcupines and squirrels; carnivores, insectivores and marsupials are not known to act as hosts.
The listing of host species among the reptiles has rarely been attempted. Ayala in 1978 listed 156 published accounts on 54 valid species and subspecies between 1909 and 1975.[1] The regional breakdown was Africa: 30 reports on 9 species; Australia, Asia & Oceania: 12 reports on 6 species and 2 subspecies; Americas: 116 reports on 37 species.
The diagnostic criteria of this family are:
Mammalian erythrocytes do not possess a nucleus. Although it has been suggested that the nucleus was lost in the erythrocytes better to enable them to traverse capilaries evidence for this is lacking. It appears that this loss along with the mitochondria that the erythrocytes also lose may protect the erythrocytes against oxidative stress.[2]
The full taxonomic name of a species includes the subgenus but this is often omitted in practice. The full name indicates some features of the morphology and type of host species. Sixteen subgenera are currently recognised.
The avian species were discovered soon after the description of P. falciparum and a variety of generic names were created. These were subsequently placed into the genus Plasmodium although some workers continued to use the genera Laverinia and Proteosoma for P. falciparum and the avian species respectively.
The 5th and 6th Congresses of Malaria held at Istanbul (1953) and Lisbon (1958) respectively recommended the creation and use of subgenera in this genus. Laverinia was applied to the species infecting humans and Haemamoeba to those infecting lizards and birds. This proposal was not universally accepted. Bray in 1955 proposed a definition for the subgenus Plasmodium and a second for the subgenus Laverinia in 1958. Garnham described a third subgenus - Vinckeia - in 1964. Several additional subgenera have been created since. The current subgenera are listed below.
Asiamoeba Telford 1988
Bennettinia Valkiūnas 1997[3]
Carinamoeba Garnham 1966
Giovannolaia Corradetti, Garnham & Laird 1963[4]
Haemamoeba Grassi & Feletti 1890
Huffia Garnham & Laird 1963
Lacertaemoba Telford 1988
Laverania Bray 1958[5]
Novyella Corradetti, Garnham & Laird 1963
Nyssorhynchus Poinar 2005
Ophidiella Garnham 1966
Plasmodium Bray 1963 emend. Garnham 1964
Paraplasmodium Telford 1988
Sauramoeba Garnham 1966
Vinckeia Garnham 1964
The current classification scheme was developed prior to the widespread use of DNA sequence based taxonomy and is based on host and morphological criteria. Plasmodium has since been shown to be paraphytic with the genera Haemoproteus and Hepatocystis (vide infra).[6] Revision of this genus will be undertaken once sufficient DNA sequence material is available.
This forthcoming reclassification project is not unique to this genus as DNA based taxonomy is revising many traditional groupings of protozoa.
Species in this subgenus infect higher primates (including man) and have characteristic sickle shaped female gametocytes.
The type species is Plasmodium falciparum.
Species infecting higher primates other than those in the subgenus Laverania are placed in the subgenus Plasmodium.
The type species is Plasmodium malariae.
Parasites infecting other mammals including lower primates (lemurs and others) are classified in the subgenus Vinckeia.
The type species is Plasmodium bubalis.
Schizonts contain scant cytoplasm, are often round, do not exceed the size of the host nucleus and stick to it. Gametocytes, while varying in shape tend to be round or oval, do not exceed the size of the nucleus and stick to it.
The type species is Plasmodium juxtanucleare.
Schizonts contain plentiful cytoplasm, are larger than the host cell nucleus and frequently displace it. They are found only in mature erythrocytes. Gametocytes are elongated. Exoerythrocytic schizogony occurs in the mononuclear phagocyte system.
The type species is Plasmodium circumflexum.
Mature schizonts are larger than the host cell nucleus and commonly displace it. Gametocytes are large, round, oval or irregular in shape and are substantially larger than the host nucleus.
The type species is Plasmodium relictum.
Mature schizonts, while varying in shape and size, contain plentiful cytoplasm and are commonly found in immature erythryocytes. Gametocytes are elongated.
The type species is Plasmodium elongatum.
Mature schizonts are either smaller than or only slightly larger than the host nucleus. They contain scanty cytoplasm. Gametocytes are elongated. Sexual stages in this subgenus resemble those of Haemoproteus. Exoerythrocytic schizogony occurs in the mononuclear phagocyte system
The type species is Plasmodium vaughani.
Although over 3200 species of lizard have been identified as hosts to Plasmodium species, only 29 species of snakes have been. All snake infecting species are placed into the sungenus Ophidiella.
The schizonts and gametocytes are greatly disparate in size (4 to 15 times).
The schizonts are small and give rise to 8 or fewer merozoites. The gametocytes like the schizonts are small.
The type species is Plasmodium minasense.
The schizonts are medium-sized and undergo 3 to 5 nuclear divisions. The gametocytes are medium-sized
The schizonts are of medium size. Exoerythrocytic schizonts may be produced in both fixed and wandering host cells. The gametocytes are large. One species in this subgenus is capabale of merogony in a vector of the Lutzomyia genus.
Large schizonts giving rise to 12 or more merozoites. The gametocytes like the schizonts are large. The asexual stages tend to disappear from the lymphocytes once the gametocytes appear in the lymphocytes.
The type species is Plasmodium agamae.
The species in this subgenus infect only snakes.
The type species is Plasmodium weyoni.
One species has been identified from Dominican amber - Plasmodium dominicum. The vertebrate host of this species is unknown but it seems likely that it may have been a bird.
The type species is Plasmodium dominicum.
Although the evolution of this genus has been studied by a number of authors, details are still being elucidated.
A number of useful phylogentic trees of this genus have been published
Tree of Life website
American Museum of Natural History
PLOS site
Paper on Plasmodium
Paper on Plasmodium
Paper on Plasmodium
From these trees it is clear that:
A paper by Blanquart and Gascuel[9] examined Plasmodium 84 mitochondial sequences and included Hepatocystis, Haemoproteus and Leukocytozoon sequences.
The results agree with the previous analyses showing that Hepatocystis, Haemoproteus and Plasmodium appear to be derived from a Leukocytozoon ancestor. Hepatocystis appears to be a sister group to the great ape-rodent clade with the lower primate clade being ancestral to all three. In terms of Plasmodium subgenera they suggest that the subgenus Plasmodium is ancestral to both Laverania and Vinckeia.
The bird and lizard species are intermixed as previously found.
Examination of the protease gene (SERA) in 18 species[10] has shown that the ancestral state had only a single gene and that gene duplications have occurred in the extant species. This paper confirms the groupings found elsewhere with an Asian clade. The rodent species seem to be more closely related to the Laverania subgenus than does the subgenus Plasmodium.
This branching order is also found in an analysis of the mitochondial genes[11] This latter paper puts the divergence between the reptile-bird and mammal clades at 38.4 ± 3.2 million years ago (Mya). Other divergence times reported include
P. falciparum – P. reichenowi - 4 million years ago (±0.9 million years)
P. ovale - P. cynomolgi/P. gonderi/P. simiovale/P. fieldi/P. inui/P. fragile/P. coatneyi/P. knowlesi - 19 million years ago
P. malariae and P. inui/P. hylobati - 19 million years ago
P. malariae/P. inui/P. hylobati - P. chabaudi/P. yoelii - 25.7 million years ago (±2.6 million years)
P. knowlesi - P. cynomolgi/P. simiovale/P. fieldi/P. inui/P. fragile/P. coatneyi - 6.3 million years ago (±1.4 million years)
A deletion mutation of ~100 base pairs including part of the LS1 rRNA gene is found in the sequences of two African species - P. gonderi and an undescribed parasite taken from a mandrill - and 2 Asian species - P. cynomolgi and P. simiovale.[12] This mutation was not found in the other species examined (Leucocytozoon caulleryi, Leucocytozoon sabrazesi, P. bergei, P. chabaudi, P. falciparum, P. floridense, P. gallacium, P. fragile, P. juxtanucleare, P. knowelsi, P. mexicanum, P. reichenowi, P. relictum, P. simiae, P. vivax, P. yoelii and two unnamed Haemoproteus species.) These mutations are rare events and strongly suggests these species are related.
An estimate of the dates of evolution of several species[13] using the date of separation of the African species P. gonderi and the Asian clade at 10 million years ago gives estimates as follows:
While most phylogenetic trees have tended to agree that Plasmodium has descended from Leukocystis or Haemoproteus like species a Bayesian phylogenetic reconstruction suggests that Plasmodium may be the ancestral genus that has given rise to Haemoproteus and other genera.[14] Further study in this area is required.
Four species (P. billbrayi, P. billcollinsi, P. falciparum and P. reichenowi) form a clade within the subgenus Lavernia. This subgenus is more closely related to the other primate species than to the bird species or the included Leuocytozoon species. Both P. billbrayi and P. billcollinsi infect both the chimpanzee subspecies included in this study (Pan troglodytes troglodytes and Pan troglodytes schweinfurthii). P. falciparum infects the bonbo (Pan paniscus) and P. reichenowi infects only one subspecies (Pan troglodytes troglodytes).
A report of a new species that clusters with P. falciparum and P. reichenowi in chimpanzees has been published, although to date the species has been identified only from the sequence of its mitochondrion.[15] Further work will be needed to describe this new species, however, it appears to have diverged from the P. falciparum- P. reichenowi clade about 21 million years ago. A second report has confirmed the existence of this species in chimpanzees.[16] This report has also shown that P. falciparum is not a uniquely human parasite as had been previously believed. A third report on the epidemiology of P. falciparum has been published.[17] This study investigated two mitochondrial genes (cytB and cox1), one plastid gene (tufA), and one nuclear gene (ldh) in 12 chimpanzees and two gorillas from Cameroon and one lemur from Madagascar. Plasmodium falciparum was found in one gorilla and two chimpanzee samples. Two chimpanzee samples tested positive for Plasmodium ovale and one for Plasmodium malariae. Additionally one chimpanzee sample showed the presence of P. reichenowi and another P. gaboni. A new species - Plasmodium malagasi - was provisionally identified in the lemur. This species seems likely to belong to the Vinckeia subgenus but further work is required.
A study of ~3000 wild ape specimens collected from Central Africa has shown that Plasmodium infection is common and is usually with multiple species.[18] The ape species included in the study were western gorillas (Gorilla gorilla), eastern gorillas (Gorilla beringei), bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). 99% of the strains fell into six species within the subgenus Laverina. P. falciparum formed a monophyletic lineage within the gorilla parasite radiation suggesting an origin in gorrilas rather than chimpanzees.
It has been shown that P. falciparum forms a clade with the species P. reichenowi.[19] This clade may have originated between 3 million and 10000 years ago. It is proposed that the origin of P. falciparum may have occurred when its precursors developed the ability to bind to sialic acid Neu5Ac possibly via erythrocyte binding protein 175. Humans lost the ability to make the sialic acid Neu5Gc from its precursor Neu5Ac several million years ago and this may have protected them against infection with P. reichenowi.
Another paper has suggested that the P. falciparum isolates found in apes are derived from humans and that P. falciparum and P. reichenowi diverged when humans and chimpanzees/gorillas did (between 5 million years ago and 7 million years ago million years ago).[20]
A review of this subgenus has been published[21] Based on the analysis of the cytochrome b gene the relationships in this subgenus appear to as follows: P. falciparum and P. reichenowi are sister species. Their closest relation is P. billcollinsi. P. gaboni and P. billbrayi are sister species whose closest relation is P. gora. P. gorb is more closely related to the P. falciparum/reichenowi/billcollinsi clade than the P. gaboni/billbrayi/gora clade. This putative taxonomy will need confirmation from other DNA studies.
The dates of the evolution of the species within the subgenus Laverania have been estimated as follows:[22]
Laverania: 12 million years ago (Mya) (95% estimated range: 6 million years ago - 19 million years ago)
P. falciparum in humans: 0.2 million years ago (range: 0.078 million years ago - 0.33 million years ago)
P. falciparum in Pan paniscus: 0.77 million years ago (range: 0.43 million years ago - 1.6 million years ago)
P. falciparum in humans and Pan paniscus: 0.85 million years ago (0.46 million years ago - 1.3 million years ago)
P. reichenowi - P. falciparum in Pan paniscus: 2.2 million years ago (range: 0.41 million years ago - 3.1 million years ago)
P. reichenowi - 1.8 million years ago (range: 0.6 million years ago - 3.2 million years ago)
P. billbrayi - P. falciparum 1.1 million years ago (range: 0.52 million years ago - 1.7 million years ago)
P. billcollinsi - 0.97 million years ago Mya (range: 0.38 million years ago - 1.7 million years ago)
Another estimate using the mutation rate (1.2 x 10-8 subsititutions/site/year) of the cytochrome b gene placed the spread of P. falciparum to humans at 365,000 years ago (95% credible interval: 112,000 to 1,036,000 years).[23]
Revised names have been proposed for the P. gora and P. gorb species - Plasmodium blacklocki and Plasmodium adleri resectively. [24] These names were chosen to honour the malariologists Saul Adler (1895–1966) and Donald Blacklock (1879–1953). It has also been proposed that the P. falciparum strains infecting gorrilas should be renamed Plasmodium praefalciparum. The species P. billbrayi seems to be synonymous with earlier named P. gaboni.
Host-parasite relations:
P. falciparum has been isolated from chimpanzees, gorillas and humans. The non human strains may be reclassified as P. praefalciparum.
P. reichenowi has been isolated from chimpanzees.
P. billcollinsi has been isolated from chimpanzees.
P. billbrayi has been isolated from chimpanzees.
P. gaboni has been isolated from chimpanzees.
P. adleri has been isolated from gorillas.
P. blacklocki has been isolated from gorillas.
It appears that P. falciparum has been introduced into South America on several occasions.[25] The extant strains fall into two clades - one northern and one southern. The most probable origin of these strains is Africa and it seems that they were introduced with the slave trade.
Colobine and macaque monkeys migrated from Africa into the Eurasian continent 10 and 6 millions of years ago respectively and became the ancestors of the extant Asian old world monkey species.[26] Asian old world monkey malaria parasite species infect both colobine and macaque monkeys. The existing divergence between the Asian and African clade of this subgenus seems likely to have been caused by intercontinental allopatric speciation along with that of their hosts.
Malaria parasites of the lemurs are not traditionally grouped with the subgenus Plasmodium being placed rather within subgenus Vinckeia. This classification may not be correct.[27] Based on an analysis of the mitocondria, these parasites seem to group with the others infecting primates. The origin of the primate infecting species (excluding those in the Laverina subgenus) may date back to the Eocene - a time when the primate radiation began. This analysis also suggests that the species infecting gorillas and humans may have originated in chimps.
At least 9 species belong to the 'Asian' clade of Plasmodium. These species include Plasmodium coatneyi, Plasmodium cynomolgi, Plasmodium fieldi, Plasmodium fragile, Plasmodium inui, Plasmodium hylobati, Plasmodium simiovale, Plasmodium simium and Plasmodium vivax.
Several of the 'Asian' clade - Plasmodium coatneyi, Plasmodium cynomolgi, Plasmodium fragile, Plasmodium inui, Plasmodium fieldi, Plasmodium hylobati, Plasmodium inui, Plasmodium knowlesi and Plasmodium simiovale and an African species Plasmodium gonderi - have a single single S-type-like gene and several A-type-like genes. It seems likely that these species form a clade within the subgenus Plasmodium.
Plasmodium vivax may have originated in Asia and the related species Plasmodium simium appears to be derived through a transfer from the human P. vivax to New World monkey species in South America. This was proposed in a study of howler monkeys near São Paulo, Brasil.[28]
The 'Asian' species form a clade with P. simium and P. vivax being clearly closely related as are P. knowseli and P. coatneyi; similarly P. brazillium and P. malariae are related. P. hylobati and P. inui are closely related. P. fragile and P. gonderi appear to be more closely related to P. vivax than to P. malariae.
An analysis of four apicoplast genome-encoded genes (small subunit rRNA, large subunit rRNA and caseinolytic protease C) of nine 'Asian' species (P. coatneyi, P. cynomolgi, P. fieldi, P. fragile, P. hylobati, P. inui, P. knowlesi, P. simiovale and P. vivax) and the African species P. gonderi suggests that P. coatneyi and P. knowlesi are closely related and that P. fragile is the species most closely related to these two.[29] Also P. vivax and P. cynomolgi appear to be related.
P. coatneyi and P. inui appear to be closely related to P. vivax.[7]
Within the 'Asian' clade are three unnamed potential species. One infects each of the two chimpanzee subspecies included in the study (Pan troglodytes troglodytes and Pan troglodytes schweinfurthii).[17] These appear to be related to the P. vivax/P. simium clade.
Analysis of the merozoite surface protein in ten species of the Asian clade suggest that this group diversified between 3 and 6.3 million years ago - a period that coincided with the radiation of the macques within South East Asia.[30] The inferred branching order differs from that found from the analysis of other genes suggesting that this phylogenetic tree may be difficult to resolve. Positive selection on this gene was also found.
P. vivax appears to have evolved between 45,000 and 82,000 years ago from a species that infects south east Asian macques.[31] This is consistent with the other evidence of a south eastern origin of this species. An second estimate put the earliest date of the evolution of P. vivax at at 265,000 years.[32]
P. vivax and P. knowesli appear to have diverged 25-30 million years ago.[20]
The pattern emerging from this data suggests that the ancestor of P. gonderi and the 'Asian' clade (P. coatneyi, P. cynomolgi, P. fieldi, P. fragile, P. hylobati, P. inui, P. knowlesi, P. simiovale and P. vivax) infected a primate host - perhaps the ancestor of the extant Rhesus monkey - and migrated with its vertebrate host from Africa to Asia via the Middle East. The Asian branch then gave rise to several clades - P. fragile-P. coatneyi/P. knowlesi, P. hylobati/P. inui and P. cynomolgi - P. simium/P. vivax. P. fieldi and P. simiovale appear to be relatively early diverging species within this clade. The timing of these events is still rather uncertain.
As a rule (with the noticable exception of P. knowesli) the Asian species have a 72 hour intra erythroctytic life cycle.
The species infecting Old World monkeys (subgenus Plasmodium) seem to form a clade.
P. ovale is more closely related to P. malariae than to P. vivax.
Two unnamed potential species infect the bonbo (Pan paniscus) and these are related to the P. malariae/P. brazillium clade.
Plasmodium ovale has recently been shown to consist of two cocirculating species - Plasmodium ovale curtisi and Plasmodium ovale wallikeri.[33] These two species can only be distinguished by genetic means and they separated between 1.0 and 3.5 million years ago.
The species P. gonderi appears to be the closest relation to the Asian clade.
One paper has reported a strain of malaria in a chimpazee with a mitochondrial sequence identical to that of P. ovale and a second closely related to it.[34] It seems likely as has been proposed earlier that P. ovale may have an animal reservoir.
A recently (2009) described species (Plasmodium hydrochaeri) that infects capybaras (Hydrochaeris hydrochaeris) may complicate the phylogentics of this genus.[35] This species appears to be most similar to Plasmodium mexicanum a lizard parasite. Further work in this area seems indicated.
Unlike other eukaryotes studied to date Plasmodium species have two or three distinct SSU rRNA (18S rRNA) molecules encoded within the genome.[36] These have been divided into types A, S and O. Type A is expressed in the asexual stages; type S in the sexual and type O only in the oocyte. Type O is only known to occur in Plasmodium vivax at present. The reason for this gene duplication is not known but presumably reflects an adaption to the different environments the parasite lives within.
It has been reported that the C terminal domain of the RNA polymerase 2 in the primate infecting species (other than P. falciparum and probably P. reichenowei) appears to be unusual[37] suggesting that the classification of species into the subgenus Plasmodium may have an evolutionary and biological basis.
An estimation of the date of evolution of this genus based upon the mutation rate in the cytochrome b gene places the evolution of P. falciparum at 2.5 Mya.[38] The authors also estimated that the mammalian species of this genus evolved 12.8 Mya and that the order Haemosporida evolved 16.2 Mya. While the date of evolution of P. falciparum is consistent with alternative methods, the other two dates are considerably more recent than other published estimates and probably should be treated with caution.
Another paper[11] examining the dates of evolution using the concatenated sequences of the cytochrome c oxidase III, cytochrome c oxidase I and cytochrome b genes - all from the mitochondrion - suggested the following dates for the evolution of the species examined (P. coatneyi, P. cynomolgi, P. falciparum, P. fieldi, P. fragile, P. gonderi, P. hylobati, P. inui, P. knowlesi, P. malariae, P. ovale, P. reichenowi, P. simiovale, P. vivax) was as follows:
Asian-African clade divergence: 12-19 million years ago
Primate-rodent clade divergence: 15-30 million years ago
Reptile/bird-mammal clade divergence: 20-30 million years ago
These estimates differ significantly from other studies. All dates estimated so far should probably be regared with some suspicion given the existing disagreements between the various authors.
It is known from many written historical sources that P. vivax malaria was endemic in the wetlands of England from the 1500s until the 20th century.[39] It is suspected that this disease was introduced by the Romans sometime before 400 AD. It seems likely that it remained endemic in these areas at least up to 1000 AD.
Because of the number of species parasited by Plasmodium further discussion has been broken down into following pages:
The vertebrate host is the first criterion used for speciation and may be sufficent alone to determine the subgenus as in Ophidiella and Vinckeia. The morphological features of the parasite itself most commonly used to describe a species include the number of pigment granules, the degree of encirclement of the host nucleus, the size of the parasite, the degree of host nucleus displacement and the degree of host cell enlargement.
At least one species has been isolated from the mandrill (Mandrillus leucophaeus) that awaits full publication. It is currently known as Plasmodium sp. DAJ-2004.
At least one species related to P. ovale appears to be present in chimpanzees. It is known only from a DNA sequence and awaits description.
P. vivax strains can be separated into two distinct types depending on the organisation of the A and S rRNA genes.[40] A gene conversion occurred in an Old World strain and this mutated strain give rise to a new calde of parasites in the New World. The Old World strains were subsequently re introduced - possibly via the slave trade - and these are related to the monkey parasite P. simium. The specific name Plasmodium collinsi has been proposed for the New World strains but this has not yet been accepted.
A second mutation is present in the ORF 470 gene of the plasmid in the New World P. vivax strains. This protein is highly conserved. In the Old World strains of P. vivax and its relations a valine is present. In the New World strains this residue has been replaced by an isoleucine (G -> A in the first codon position).
Two separate strains of P. vivax can be identified on the basis of the circumsporozoite protein (CSP) gene.[41] Both of these alleles can be found in P. simium and they occur both in the New and Old Worlds. This suggests a complex history of transmission across the world and between species.
Another as yet unnamed species was isolated from humans in Madang, Papua New Guinea in 1993.[42] This species differed immunologically and genetically from then then generally recognised species infecting humans. Additional isolates of this putative species were also found in Sepik also in Papua New Guinea, Brazil, Indonesia and Madagascar.[43] The circumsporozoite protein of this species appears to be identical to that of Plasmodium semiovale. At least two species of mosquito Anopheles deaneorum and Anopheles oswaldoi appear to be capable of transmitting this parasite. [44] These reports have not gone unchallenged and the status of this putative species is unclear at present.[45]
This listing while currently incomplete will be updated when the relevant information becomes available.
The literature is replete with species initially classified as Plasmodium that have been subsequently reclassified. With the increasing use of DNA taxonomy some of these may be once again be classified as Plasmodium.
The following species have been classified into the genus Hepatocystis:
The following species have been classified into the genus Haemoemba:
The following species has been classified into the genus Garnia:
The following species has been classified into the genus Fallisia:
The following species that have been described in the literature are currently regarded as being of questionable validity (nomen dubium).
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Review: [1]