Genetic diversity of Trypanosoma cruzi parasites infecting dogs in southern Louisiana sheds light on parasite transmission cycles and serological diagnostic performance.

Eric Dumonteil,Ardem Elmayan,Brandy Duhon,Wendy Wolfson,Weihong Tu,Garry Balsamo,Alicia Majeau,Claudia Herrera,Preston Marx,Ananias A Escalante

doi:10.1371/journal.pntd.0008932

Abstract

Chagas disease is a neglected zoonosis of growing concern in the southern US, caused by the parasite Trypanosoma cruzi. We genotyped parasites in a large cohort of PCR positive dogs to shed light on parasite transmission cycles and assess potential relationships between parasite diversity and serological test performance. We used a metabarcoding approach based on deep sequencing of T. cruzi mini-exon marker to assess parasite diversity. Phylogenetic analysis of 178 sequences from 40 dogs confirmed the presence of T. cruzi discrete typing unit (DTU) TcI and TcIV, as well as TcII, TcV and TcVI for the first time in US dogs. Infections with multiple DTUs occurred in 38% of the dogs. These data indicate a greater genetic diversity of T. cruzi than previously detected in the US. Comparison of T. cruzi sequence diversity indicated that highly similar T. cruzi strains from these DTUs circulate in hosts and vectors in Louisiana, indicating that they are involved in a shared T. cruzi parasite transmission cycle. However, TcIV and TcV were sampled more frequently in vectors, while TcII and TcVI were sampled more frequently in dogs. These observations point to ecological host-fitting being a dominant mechanism involved in the diversification of T. cruzi-host associations. Dogs with negative, discordant or confirmed positive T. cruzi serology harbored TcI parasites with different mini-exon sequences, which strongly supports the hypothesis that parasite genetic diversity is a key factor affecting serological test performance. Thus, the identification of conserved parasite antigens should be a high priority for the improvement of current serological tests.

Highlights

Discordant or confirmed positive T. cruzi serology harbored genetically different TcI parasites, which shows that parasite genetic diversity is a key factor affecting serological test performance
Chagas disease is a neglected zoonosis caused by the protozoan parasite Trypanosoma cruzi, which is endemic in the Americas
73 samples from T. cruzi PCR positive dogs were included for genotyping using the mini-exon marker, and we were able to recover 178 quality mini-exon sequences from 40 samples (55%)

Summary

Introduction

Chagas disease is a neglected zoonosis caused by the protozoan parasite Trypanosoma cruzi, which is endemic in the Americas. Infection leads to chronic cardiomyopathy in 20–40% of humans. Dogs have been identified as a major domestic/peridomestic host for T. cruzi infection in many countries and epidemiological setting. They can play an important role as a domestic reservoir of the parasite, and can contribute to an increased risk for T. cruzi infection in humans [1,2,3,4]. Dogs can develop severe chronic cardiomyopathy with poor prognosis [5,6]. Chagas disease is a neglected zoonosis of growing concern in the southern US, caused by the parasite Trypanosoma cruzi. We genotyped parasites in a large cohort of PCR positive dogs to shed light on parasite transmission cycles and assess potential relationships between parasite diversity and serological test performance

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Discussion

Conclusion