Using molecular epidemiology to track Toxoplasma gondii from terrestrial carnivores to marine hosts: implications for public health and conservation.

Elizabeth Vanwormer,Melissa A Miller,Michael E Grigg,Patricia A Conrad,Jonna A K Mazet,Tim E Carpenter,Daniel Rejmanek,Elodie Ghedin

doi:10.1371/journal.pntd.0002852

Abstract

BackgroundEnvironmental transmission of the zoonotic parasite Toxoplasma gondii, which is shed only by felids, poses risks to human and animal health in temperate and tropical ecosystems. Atypical T. gondii genotypes have been linked to severe disease in people and the threatened population of California sea otters. To investigate land-to-sea parasite transmission, we screened 373 carnivores (feral domestic cats, mountain lions, bobcats, foxes, and coyotes) for T. gondii infection and examined the distribution of genotypes in 85 infected animals sampled near the sea otter range.Methodology/Principal FindingsNested PCR-RFLP analyses and direct DNA sequencing at six independent polymorphic genetic loci (B1, SAG1, SAG3, GRA6, L358, and Apico) were used to characterize T. gondii strains in infected animals. Strains consistent with Type X, a novel genotype previously identified in over 70% of infected sea otters and four terrestrial wild carnivores along the California coast, were detected in all sampled species, including domestic cats. However, odds of Type X infection were 14 times higher (95% CI: 1.3–148.6) for wild felids than feral domestic cats. Type X infection was also linked to undeveloped lands (OR = 22, 95% CI: 2.3–250.7). A spatial cluster of terrestrial Type II infection (P = 0.04) was identified in developed lands bordering an area of increased risk for sea otter Type II infection. Two spatial clusters of animals infected with strains consistent with Type X (P≤0.01) were detected in less developed landscapes.ConclusionsDifferences in T. gondii genotype prevalence among domestic and wild felids, as well as the spatial distribution of genotypes, suggest co-existing domestic and wild T. gondii transmission cycles that likely overlap at the interface of developed and undeveloped lands. Anthropogenic development driving contact between these cycles may increase atypical T. gondii genotypes in domestic cats and facilitate transmission of potentially more pathogenic genotypes to humans, domestic animals, and wildlife.

Highlights

As human populations expand and alter global habitats, increased contact among people, domestic animals, and wildlife can lead to the emergence or re-emergence of diseases that threaten public and animal health [1,2,3]
Differences in T. gondii genotype prevalence among domestic and wild felids, as well as the spatial distribution of genotypes, suggest co-existing domestic and wild T. gondii transmission cycles that likely overlap at the interface of developed and undeveloped lands
By testing 373 and characterizing T. gondii infection in 85 terrestrial carnivores sharing the California coast, we found that Type X, the type previously identified in over 70% of infected sea otters tested, was more common in wild felids than domestic cats

Summary

Introduction

As human populations expand and alter global habitats, increased contact among people, domestic animals, and wildlife can lead to the emergence or re-emergence of diseases that threaten public and animal health [1,2,3]. Described in terrestrial environments, the zoonotic protozoan parasite, Toxoplasma gondii, is emerging as an important pathogen in aquatic systems. Toxoplasma gondii has been linked to widespread marine mammal infection and severe water-borne disease outbreaks in humans around the world [4]. In addition to playing a vital role in maintaining near-shore kelp forest ecosystems, sea otters serve as important sentinels for identifying disease threats, like T. gondii, to other marine species and humans sharing the coastal environment [6,7]. Environmental transmission of the zoonotic parasite Toxoplasma gondii, which is shed only by felids, poses risks to human and animal health in temperate and tropical ecosystems. Atypical T. gondii genotypes have been linked to severe disease in people and the threatened population of California sea otters. To investigate land-to-sea parasite transmission, we screened 373 carnivores (feral domestic cats, mountain lions, bobcats, foxes, and coyotes) for T. gondii infection and examined the distribution of genotypes in 85 infected animals sampled near the sea otter range

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