Polychromophilus

The genus Polychromophilus consists of obligate intracellular eukaryotic parasites that infect bats from every continent except Antarctica. They are transmitted by bat flies, which act as an insect vector as well as the parasite’s site of sporogeny. Polychromophilus follows a fairly typical Haemospororidian lifecycle, with gametocytes and gametes restricted to the bloodstream of the host and meronts infecting organs – most notably the lungs and the liver. The type species is Polychromophilus melanipherus, and was described by Dionisi in 1898.

Polychromophilus
Scientific classification
(unranked): Diaphoretickes
Clade: TSAR
Clade: SAR
Infrakingdom: Alveolata
Phylum: Apicomplexa
Class: Aconoidasida
Order: Haemospororida
Family: Plasmodiidae
Genus: Polychromophilus
Species

Polychromophilus adami
Polychromophilus corradetti
Polychromophilus deanei
Polychromophilus fulvida
Polychromophilus melanipherus
Polychromophilus murinus

Taxonomy

Polychromophilus was first described by Dionisi in 1898, who also differentiated between the first two species, Polychromophilus murinus and Polychromophilus melanipherus. Both of these original species were named after their primary hosts – Vespertilio murinus and Miniopterus schreibersi respectively.

In 1906, Schingareff managed to observe and describe merozoites within macrophages of Myotis daubentoni and Miniopterus schreibersi and suspected that nycteribiid flies acted as insect vectors. This was not evidenced until Corradetti discovered sporozoites within such flies in 1936, and was further supported by later research.[1]

The genus was divided into two subgenera — Polychromophilus and Bioccala but the subgenus Bioccala was raised to genus status in 1984.[2]

This genus along with Haemoproteus and Hepatocystis appears to be a sister clade to Plasmodium. It appears to have evolved from the avian/saurian clade of Plasmodium.[3]

Life cycle

Polychromophilus sporozoites remain within the salivary glands of their insect vectors until a blood meal is taken. The sporozoites enter the primary host’s bloodstream and infect erythrocytes, inside of which the parasite develops into gametocytes. The gametocytes then proceed to sexually reproduce via gametogony, involving the exflagellation of the parasite forming numerous microgametes and macrogametes.[4]

The microgametes and macrogametes remain within the blood until they are taken in by an insect vector during another blood meal. The gametes then fuse in pairs within the gut of the insect, and the fertilised macrogamete develops into an ookinete. This then enters the body of the insect vector and further develops into an oocyst between the epithelial cells and basement membrane of the midgut.[4][5]

The oocyst then begins to divide into numerous sporozoites which remain within the thick oocyst capsule. Upon maturation, the oocyst bursts releasing the sporozoites into the insect vector, where they migrate toward the salivary gland ready to continue their cycle. The bursting of the oocysts leaves behind large residual bodies within the insect vector, which do not continue sporozoite development.[4]

Merogony of the parasite, although less well understood, has been observed to occur in a variety of organs and cell types of the primary bat host. Large bodies have been discovered in organs including the spleen and lungs, while small meronts have been found to develop within the Kupffer cells of the liver. The meronts are often transported around the body by macrophages in the blood.[4]

Hosts and habitat

The genus Polychromophilus infects a diverse range of bats, and is present on every continent inhabited by their hosts. The type species, Polychromophilus melanipherus, was first observed in the Roman Campagna within the type host Miniopterus schreibersi. The presence of the parasite has since been discovered in numerous locations worldwide, including Israel, Australia, the Congo, Ethiopia, Brazil, and North America.[1]

The insect vectors of Polychromophilus comprise entirely of bat flies of three different genera – Basilia, Nycteribia, and Penicillidia. No other insects are known to carry the parasite.

Host records

Description

Sporozoites are elongated and straight or slightly curved in shape, and not particularly motile. When prepared with a Giemsa-stain, their oval and slightly unconventional nucleus becomes visible. Their pellicle comprises a thin outer membrane separated from a double inner membrane, underneath which lies 21 subpellicular microtubules evenly spaced around the periphery. Many micronemes are present in the anterior tip of the sporozoite, and a single mitochondrion containing tubular cristae lies behind the nucleus.[4]

Gametocytes tend to take up almost the entirety of their host erythrocyte, and hence are covered by a thin layer of erythrocyte. They are contained within a trilaminar pellicle, consisting of a parasitophorous vacuole membrane, the gametocyte plasmalemma, and an inner double membrane. Multiple intracellular organelles are visible within the gametocytes, including mitochondria with tubular cristae, a Golgi apparatus, micronemes, primary lysosomes, and a microtubule organising centre comprising two centrioles. No visible cytosome is present. Microgametocytes stain pink with Giemsa, and contain a large diffuse nucleus lacking a visible nucleolus. Macrogametocytes, on the other hand, stain blue-purple due to a higher number of ribosomes within the cytoplasm and contain a small distinct nucleus with a clearly visible nucleolus.[8] The gametocytes are known to doubly infect the same erythrocyte, a feature considered characteristic of some species.[4]

Oocysts are covered by an amorphous capsule comprising an inner granular layer and an outer lighter layer. The capsule is often observed to form invaginations into the oocyst cytoplasm. The oocyst generally contains multiple cristate mitochondria, and mature oocysts are packed with sporozoites.[4]

References
  1. Garnham, P. C. C. (1973). "The zoogeography of Polychromophilus and description of a new species of a Gregarine (Lankesteria galliardi)". Annales de Parasitologie Humaine et Comparée. 48 (2): 231–242. doi:10.1051/parasite/1973482231. ISSN 0003-4150. PMID 4206622.
  2. Landau, I.; Baccam, D.; Ratanaworabhan, N.; Yenbutra, S.; Boulard, Y.; Chabaud, A. G. (1984). "Nouveaux haemoproteidae parasites de chiroptères en Thailande". Annales de Parasitologie Humaine et Comparée. 59 (5): 437–447. doi:10.1051/parasite/1984595437.
  3. Witsenburg F, Salamin N, Christe P (2012). "The evolutionary host switches of Polychromophilus: a multi-gene phylogeny of the bat malaria genus suggests a second invasion of mammals by a haemosporidian parasite". Malar. J. 11: 53. doi:10.1186/1475-2875-11-53. PMC 3342143. PMID 22356874.
  4. Gardner, R. A.; Molyneux, D. H. (June 1988). "Polychromophilus murinus: a malarial parasite of bats: life-history and ultrastructural studies". Parasitology. 96 (3): 591–605. doi:10.1017/s0031182000080215. ISSN 0031-1820. PMID 3136420.
  5. Fayer, R. (1986-01-01). "Illustrated Guide to the Protozoa". The American Journal of Tropical Medicine and Hygiene. 35 (1): 215–216. doi:10.4269/ajtmh.1986.35.215. ISSN 0002-9637.
  6. Landau, I.; Rosin, G.; Miltgen, F.; Hugot, J.-P.; Leger, N.; Beveridge, I.; Baccam, D. (1980). "Sur le genre Polychromophilus (Haemoproteidae, parasite de Microchiroptères)". Annales de Parasitologie Humaine et Comparée. 55 (1): 13–32. doi:10.1051/parasite/1980551013.
  7. Megali A, Yannic G, Christe P (2011). "Disease in the dark: molecular characterization of Polychromophilus murinus in temperate zone bats revealed a worldwide distribution of this malaria-like disease". Mol. Ecol. 20 (5): 1039–48. doi:10.1111/j.1365-294X.2010.04905.x. PMID 21073585.
  8. Garnham, P. C. C.; Lainson, R.; Shaw, J. J. (1971). "[NO TITLE AVAILABLE]". Memórias do Instituto Oswaldo Cruz. 69 (1): 119–125. doi:10.1590/s0074-02761971000100009. ISSN 0074-0276. PMID 4997955.
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