A hotspot of Toxoplasma gondii Africa 1 lineage in Benin: How new genotypes from West Africa contribute to understand the parasite genetic diversity worldwide

Abstract

Through international trades, Europe, Africa and South America share a long history of exchanges, potentially of pathogens. We used the worldwide parasite Toxoplasma gondii to test the hypothesis of a historical influence on pathogen genetic diversity in Benin, a West African country with a longstanding sea trade history. In Africa, T. gondii spatial structure is still non-uniformly studied and very few articles have reported strain genetic diversity in fauna and clinical forms of human toxoplasmosis so far, even in African diaspora. Sera from 758 domestic animals (mainly poultry) in two coastal areas (Cotonou and Ouidah) and two inland areas (Parakou and Natitingou) were tested for T. gondii antibodies using a Modified Agglutination Test (MAT). The hearts and brains of 69 seropositive animals were collected for parasite isolation in a mouse bioassay. Forty-five strains were obtained and 39 genotypes could be described via 15-microsatellite genotyping, with a predominance of the autochthonous African lineage Africa 1 (36/39). The remaining genotypes were Africa 4 variant TUB2 (1/39) and two identical isolates (clone) of Type III (2/39). No difference in terms of genotype distribution between inland and coastal sampling sites was found. In particular, contrarily to what has been described in Senegal, no type II (mostly present in Europe) was isolated in poultry from coastal cities. This result seems to refute a possible role of European maritime trade in Benin despite it was one of the most important hubs during the slave trade period. However, the presence of the Africa 1 genotype in Brazil, predominant in Benin, and genetic analyses suggest that the triangular trade was a route for the intercontinental dissemination of genetic strains from Africa to South America. This supports the possibility of contamination in humans and animals with potentially imported virulent strains.

Toxoplasma gondii Genotypes Circulating in Serbia—Insight into the Population Structure and Diversity of the Species in Southeastern Europe, a Region of Intercontinental Strain Exchange

“…Patterns 11 and 12 (strain IDs: 057-16, 061-16, 062-16, 075-16) which originated from golden jackals may represent the same genotype, which could not be matched in the ToxoDB. Patterns shaded blue (6,7,26) indicate genotypes which have been detected in hosts residing in both the domestic and sylvatic environment, while the rose-shaded patterns (3,18) indicate genotypes which were detected in two host species from the domestic environment. A NJ tree which included the Serbian isolates typed on nine markers was constructed (Figure 2).…”

“…Along with the reports of Africa 1 genotypes in Turkey in humans as well as in animals [36,37], these findings indicate the presence of African lineages in SEE. Global distribution of Africa 1 has been suggested, which gains importance in view of the fact that Africa 1 has been shown to be virulent in mice; Africa 4, on the other hand, may have more limited distribution, and has been shown to be avirulent to mice [18]. No lineage I genotype was detected in Serbia.…”

“…In addition, it has been experimentally demonstrated that infection with a number of isolates from South America results in mortality of laboratory mice, which indicates virulence [14]. Lineages I, II, III and likely Africa 1 circulate globally, while lineages of apparent limited geographical distribution have been detected in North America [15], South America [16], and Africa [17,18]. Differences in the diversity of the genotype population not only appear to be geographical, but also related to the eco-system, that is, the anthropogenic versus the wild environment.…”

A uniqueToxoplasma gondiihaplotype under strong selection has accompanied domestic cats in their global expansion

“…In addition, conflicting scenarios have been proposed to explain the global spread of these clonal lineages (Minot et al, 2012;Bertranpetit et al, 2017;Shwab et al, 2018). Given the crucial importance of domestic cats and rodents in the transmission of T. gondii, a presumed role of these host species in the global spread of the major clonal lineages has been repeatedly evoked in the literature (Lehmann et al, 2006;Shwab et al, 2018;Hamidović et al, 2021). However, this hypothesis could not be formally tested previously (Shwab et al, 2018;Hamidović et al, 2021) owing to the paucity of T. gondii samples in many regions (Su et al, 2003;Lehmann et al, 2006;Khan et al, 2007;Minot et al, 2012;Lorenzi et al, 2016).…”

“…Given the crucial importance of domestic cats and rodents in the transmission of T. gondii, a presumed role of these host species in the global spread of the major clonal lineages has been repeatedly evoked in the literature (Lehmann et al, 2006;Shwab et al, 2018;Hamidović et al, 2021). However, this hypothesis could not be formally tested previously (Shwab et al, 2018;Hamidović et al, 2021) owing to the paucity of T. gondii samples in many regions (Su et al, 2003;Lehmann et al, 2006;Khan et al, 2007;Minot et al, 2012;Lorenzi et al, 2016). Moreover, lack of good estimates of parasite mutation rate and generation time hampered attempts to date dispersal time in relation to expansion history of principal hosts.…”