A partition of Toxoplasma gondii genotypes across spatial gradients and among host species, and decreased parasite diversity towards areas of human settlement in North America

Jiang, Tiantian; Shwab, E. Keats; Martin, Robbie M.; Gerhold, Richard W.; Rosenthal, Benjamin M.; Dubey, J. P.; Su, Chunlei

doi:10.1016/j.ijpara.2018.01.008

Cited by 43 publications

(38 citation statements)

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“…Phylogenetic analyses of strongly variable loci coding for virulence factors such as surface and secretory antigens, often under significant selective pressure, have been widely used to infer possible genetic population structure models, evolutionary relationships between T. gondii populations, reservoirs, and transmission patterns, among other factors [20,55,56]. Our results suggest that Spanish and French T. gondii populations could be genetically related based on limited SAG3 sequences of sheep origin deposited in the GenBank database.…”

Section: Discussionmentioning

confidence: 77%

“…Vast research on T. gondii population structure, diversity, and geographical distribution is being conducted worldwide [19,20]. Despite the importance of the ovine industry in Europe, information about T. gondii strains circulating in European ovine livestock is scarce (Table 1); while most ovine isolates and genotyping descriptions in Europe are clonal [21], some specific findings of novel genotypes [22] and non-clonal isolates [23], along with mixed infections [24], deserve attention.…”

Section: Introductionmentioning

confidence: 99%

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Isolation and genetic characterization of Toxoplasma gondii in Spanish sheep flocks

et al. 2020

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Background Toxoplasma gondii is a major cause of abortion in small ruminants and presents a zoonotic risk when undercooked meat containing cysts is consumed. The aim of the present study was to investigate the genetic diversity among the T. gondii strains circulating in ovine livestock in Spain. Methods Selected samples collected from abortion outbreaks due to toxoplasmosis (n = 31) and from chronically infected adult sheep at slaughterhouses (n = 50) in different Spanish regions were bioassayed in mice, aiming at parasite isolation. In addition, all original clinical samples and the resulting isolates were genotyped by multi-nested PCR-RFLP analysis of 11 molecular markers and by PCR-DNA sequencing of portions of the SAG3, GRA6 and GRA7 genes. Results As a result, 30 isolates were obtained from 9 Spanish regions: 10 isolates from abortion-derived samples and 20 isolates from adult myocardial tissues. Overall, 3 genotypes were found: ToxoDB#3 (type II PRU variant) in 90% (27/30) of isolates, ToxoDB#2 (clonal type III) in 6.7% (2/30), and ToxoDB#1 (clonal type II) in 3.3% (1/30). When T. gondii-positive tissue samples (n = 151) were directly subjected to RFLP genotyping, complete restriction profiles were obtained for 33% of samples, and up to 98% of the specimens belonged to the type II PRU variant. A foetal brain showed a clonal type II pattern, and four specimens showed unexpected type I alleles at the SAG3 marker, including two foetal brains that showed I + II alleles as co-infection events. Amplicons of SAG3, GRA6 and GRA7 obtained from isolates and clinical samples were subjected to sequencing, allowing us to confirm RFLP results and to detect different single-nucleotide polymorphisms. Conclusions The present study informed the existence of a predominant type II PRU variant genotype (ToxoDB#3) infecting domestic sheep in Spain, in both abortion cases and chronic infections in adults, coexisting with other clonal (ToxoDB#1 and ToxoDB#2), much less frequent genotypes, as well as polymorphic strains as revealed by clinical sample genotyping. The use of multilocus sequence typing aided in accurately estimating T. gondii intragenotype diversity.

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Section: Discussionmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Isolation and genetic characterization of Toxoplasma gondii in Spanish sheep flocks

et al. 2020

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“…This method improved resolution in distinguishing different T. gondii strains, and as it is a nested PCR, it is more sensitive. This effort generated an integrated database to reveal global T. gondii diversity (Su et al, 2012), distribution of genotypes world-wide (Shwab et al, 2014), and partition of genotypes into a spatial gradient and animal species in North America (Jiang et al, 2018). Surprisingly, the phylogenetic network generated from the PCR-RFLP data is similar to that obtained from whole genome sequence data (Lorenzi et al, 2016).…”

Section: Which Enteric Protozoan Pathogens Are Zoonotic and What Are mentioning

confidence: 99%

Are molecular tools clarifying or confusing our understanding of the public health threat from zoonotic enteric protozoa in wildlife?

Robertson

Clark

Debenham

et al. 2019

International Journal for Parasitology: Parasites and Wildlife

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Emerging infectious diseases are frequently zoonotic, often originating in wildlife, but enteric protozoa are considered relatively minor contributors. Opinions regarding whether pathogenic enteric protozoa may be transmitted between wildlife and humans have been shaped by our investigation tools, and have led to oscillations regarding whether particular species are zoonotic or have host-adapted life cycles. When the only approach for identifying enteric protozoa was morphology, it was assumed that many enteric protozoa colonized multiple hosts and were probably zoonotic. When molecular tools revealed genetic differences in morphologically identical species colonizing humans and other animals, host specificity seemed more likely. Parasites from animals found to be genetically identical - at the few genes investigated - to morphologically indistinguishable parasites from human hosts, were described as having zoonotic potential. More discriminatory molecular tools have now sub-divided some protozoa again. Meanwhile, some infection events indicate that, circumstances permitting, some “host-specific” protozoa, can actually infect various hosts. These repeated changes in our understanding are linked intrinsically to the investigative tools available. Here we review how molecular tools have assisted, or sometimes confused, our understanding of the public health threat from nine enteric protozoa and example wildlife hosts ( Balantoides coli - wild boar; Blastocystis sp. - wild rodents; Cryptosporidium spp. - wild fish; Encephalitozoon spp. - wild birds; Entamoeba spp. - non-human primates; Enterocytozoon bieneusi - wild cervids; Giardia duodenalis - red foxes; Sarcocystis nesbitti - snakes; Toxoplasma gondii - bobcats). Molecular tools have provided evidence that some enteric protozoa in wildlife may infect humans, but due to limited discriminatory power, often only the zoonotic potential of the parasite is indicated. Molecular analyses, which should be as discriminatory as possible, are one, but not the only, component of the toolbox for investigating potential public health impacts from pathogenic enteric protozoa in wildlife.

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“…Far less well characterized is the pathophysiology of T. gondii infection following ingestion by sea otters, including potential strain-specific impacts on animal health and survival. The T. gondii genotypes previously isolated from infected southern sea otter carcasses, Type II and Type X (Haplogroup 12) [14,15], exist throughout North America, with Type II detected primarily in domestic animals and Type X in wildlife [16]. In California watersheds bordering the sea otter range, evidence supports separate, but overlapping domestic (Type II) and wild (Type X) transmission cycles [17,18].…”

Section: Introductionmentioning

confidence: 99%

Type X strains of Toxoplasma gondii are virulent for southern sea otters ( Enhydra lutris nereis) and present in felids from nearby watersheds

et al. 2019

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Why some Toxoplasma gondii -infected southern sea otters ( Enhydra lutris nereis ) develop fatal toxoplasmosis while others have incidental or mild chronic infections has long puzzled the scientific community. We assessed robust datasets on T. gondii molecular characterization in relation to detailed necropsy and histopathology results to evaluate whether parasite genotype influences pathological outcomes in sea otters that stranded along the central California coast. Genotypes isolated from sea otters were also compared with T. gondii strains circulating in felids from nearby coastal regions to assess land-to-sea parasite transmission. The predominant T. gondii genotypes isolated from 135 necropsied sea otters were atypical Type X and Type X variants (79%), with the remainder (21%) belonging to Type II or Type II/X recombinants. All sea otters that died due to T. gondii as a primary cause of death were infected with Type X or X-variant T. gondii strains. The same atypical T. gondii strains were detected in sea otters with fatal toxoplasmosis and terrestrial felids from watersheds bordering the sea otter range. Our results confirm a land–sea connection for virulent T. gondii genotypes and highlight how faecal contamination can deliver lethal pathogens to coastal waters, leading to detrimental impacts on marine wildlife.

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A partition of Toxoplasma gondii genotypes across spatial gradients and among host species, and decreased parasite diversity towards areas of human settlement in North America

Cited by 43 publications

References 53 publications

Isolation and genetic characterization of Toxoplasma gondii in Spanish sheep flocks

Isolation and genetic characterization of Toxoplasma gondii in Spanish sheep flocks

Are molecular tools clarifying or confusing our understanding of the public health threat from zoonotic enteric protozoa in wildlife?

Type X strains of Toxoplasma gondii are virulent for southern sea otters ( Enhydra lutris nereis) and present in felids from nearby watersheds

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