Babesiosoma, Jakowska and Nigrelli, 1956

Netherlands, Edward C., Cook, Courtney A., Du Preez, Louis H., Vanhove, Maarten P. M., Brendonck, Luc & Smit, Nico J., 2020, An overview of the Dactylosomatidae (Apicomplexa: Adeleorina: Dactylosomatidae), with the description of Dactylosoma kermiti n. sp. parasitising Ptychadena anchietae and Sclerophrys gutturalis from South Africa, International Journal for Parasitology: Parasites and Wildlife 11, pp. 246-260 : 249

1.4. The genus Babesiosoma

More than 60 years after the naming of the genus Dacytylosoma , the genus Babesiosoma was erected to incorporate the species that: (1) contain less granular but more vacuolated cytoplasm; (2) have a nucleus similar to species of Babesia , without a definite karyosome; (3) reproduce by schizogony or binary fission; and (4) do not produce more than four merozoites. Barta (1991) pointed out that certain of these characters, that, together, define Babesiosoma , are in general hard to unambiguously recognise. For example, (1) the less granular, more vacuolated cytoplasm indicates more amylopectin inclusions; (2) ultrastructurally a definite karyosome is present in the nuclei; and (3) the multiplication through binary fusion is dubious as this was probably confused with mature paired merozoites after merogonic duplication. However, the separation of the two genera is still considered justified as species of Babesiosoma produce only four merozoites during each merogonic cycle and double that number of sporozoites (eight) within oocysts in the definitive host ( Barta, 1991) compared to species of Dactylosoma that produce up to 16 merozoites and double the number of sporozoites within their oocyst ( Barta and Desser, 1986; Barta, 1991).

There are currently five recognised species of Babesiosoma (see Table 2 ), three described from fish hosts ( Smit et al., 2003), namely Babesiosoma bettencourti ( França, 1908), Babesiosoma mariae (syn. Dactylosoma mariae ; B. hannesi Paperna, 1981 ) and Babesiosoma tetragonis Becker and Katz, 1965 . The remaining two species are described from North American amphibian hosts. Babesiosoma jahni (syn. Dactylosoma jahni ) is the type species of the genus, described from the Eastern newt Notophthalmus viridescens (Rafinesque, 1820) . Babesiosoma stableri was described from the northern leopard frog Rana pipiens Schreber 1782 and was experimentally transmitted to Anaxyrus americanus Holbrook, 1836 , A. woodhousii (Girard, 1854) , A. terrestris (Bonnaterre, 1789) , and Rana catesbeianae (Shaw, 1802) . The latter ranid frog, R. septentrionalis (Baird, 1854) , and R. clamitans (Latreille, 1801) have all been found infected naturally in Ontario, Canada ( Barta and Desser, 1984); see Table 2 .

Species previously regarded as belonging to Babesiosoma , but formally transferred to other genera are Haemohormidium aulopi ( Mackerras and Mackerras, 1925) , Haemohormidium ophicephali ( Misra et al., 1969) (syn. Babesiosoma hareni , Babesiosoma batrachi , Dactylosoma striata , Dactylosoma notopterae ), and Haemohormidium rubrimarensis ( Saunders, 1960) (see Siddall et al., 1994; Cook et al., 2015). Enigmatic taxa, removed from the genus Babesiosoma are incertae sedis ( Babesiosoma ) anseris Haiba and El-Shabrawy, 1967, incertae sedis ( Babesiosoma ) gallinanun Fahmy, Arafa, Mandour, Kalifa and Abdel-Salem, 1979, and incertae sedis ( Babesiosoma ) ptyodactyli El-Naffer, Abdel-Rahman, and Khalifa 1979 (see Barta, 1991). Furthermore Babesiosoma aegypta Mohamed, 1978 , Babesiosoma tilapiae Imam, Marzouk, Hassan, Derhall and Itman, 1985 , and Babesiosoma aegyptiacus Eid, Negm-Eldin and Imam, 1991 were considered by Negm-Eldin (1998) to be supported by insufficient proof to document the validity of these species ( Smit et al., 2003).

Babesiosoma species are characterised by merogonic replication within the vertebrate host leading to the formation of gamonts followed by sporogonic and merogonic replication in the invertebrate host and vector (see Jakowska and Nigrelli, 1956; Barta and Desser, 1986; Barta, 1991). In the vertebrate host, asexual development consists of primary and secondary merogony, except for B. mariae . The latter species was shown by Negm-Eldin (1998) to contain a third merogonic cycle (tertiary merogony). Babesiosoma stableri undergoes primary merogony when a merozoite enters a vertebrate (frog) host's erythrocyte. Within the erythrocytes, the merozoites undergo nuclear division, transforming into a binucleate meront. These binucleate meronts then undergo a second nuclear division, ultimately forming the characteristic and tetranucleate cruciform meront (four merozoites arranged in a cross shape) typical of members of Babesiosoma (see Barta and Desser, 1986; Barta, 1991). The cruciform meront's merozoites then separate and penetrate other erythrocytes, either repeating the cycle of primary merogony or initiating secondary merogony. The secondary merogonic cycle is completed in the same manner as primary merogony ultimately producing secondary merozoites that either repeat secondary merogony or mature into gamonts ( Barta and Desser, 1986; Barta, 1991). For B. mariae in its fish host, the primary and secondary merogonic cycles are shorter compared to B. stableri and mature gamonts are produced from tertiary merozoites in the third merogonic cycle ( Negm-Eldin, 1998). Mature gamonts are then ingested in the blood meal of the natural leech vector, Desserobdella picta and undergo syzygy, ultimately maturing into gametes that fuse to form an ookinete. The ookinete then penetrates intestinal epithelial cells to initiate sporogony. Mature sporozoites then make their way to the salivary glands, where they undergo similar merogonic replication as in the vertebrate host, producing merozoites that will repeat the merogonic cycle or enter the ductules of the salivary glands. When the leech takes its next blood meal, the merozoites are injected into its new vertebrate host ( Jakowska and Nigrelli, 1956; Barta and Desser, 1986; Barta, 1991).