Dataset Information

Comparison of the Bacterial Gut Microbiome of North American Triatoma spp. With and Without Trypanosoma cruzi.

ABSTRACT: Chagas disease, caused by the hemoflagellate protist Trypanosoma cruzi, affects nearly 6 million people worldwide, mainly in Latin America. Hematophagous triatomine insects ("kissing bugs") are the primary vectors of T. cruzi throughout the Americas and feed on a variety of animals, including humans. Control of triatomines is central to the control of T. cruzi infection. Recent advances in mitigation of other insect-borne diseases via the manipulation of insect-associated bacteria as a way to halt or slow disease transmission has opened questions to the applicability of these methods to Chagas disease vectors. Few studies have examined the hindgut microbiome of triatomines found in North America. In the current study, two species of triatomines were collected across Texas, United States, screened for the presence of T. cruzi, and analyzed for the bacterial composition of their hindguts using a 16S rRNA gene-fragment metabarcoding approach. We compared diversity of microbial community profiles across 74 triatomine insects to address the hypothesis that the richness and abundance of bacterial groups differ by T. cruzi infection and strain type, blood meal engorgement status, insect species, sex, and collection location. The gut microbial community of individual triatomines was characterized by low intraindividual taxonomic diversity and high interindividual variation that was weakly predicted by triatomine species, and was not predicted by triatomine sex, collection location, T. cruzi infection status, or blood meal score. However, we did find bacterial groups enriched in T. cruzi-positive individuals, including Enterobacterales, and Petrimonas. Additionally, we detected Salmonella enterica subspecies diarizonae in three triatomine individuals; this species is commonly associated with reptiles and domesticated animals and is a pathogen of humans. These data suggest that Triatoma spp. in Texas have variable patterns of colonized and transient bacteria, and may aid in development of novel means to interfere with transmission of the Chagas disease parasite T. cruzi. Deeper understanding of the effects of parasite infection on diverse insect vector microbiomes may highlight disease transmission risk and facilitate discovery of possible intervention strategies for biological control of this emerging vector-borne disease of global health significance.

SUBMITTER: Mann AE

PROVIDER: S-EPMC7082358 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Comparison of the Bacterial Gut Microbiome of North American Triatoma spp. With and Without Trypanosoma cruzi.

Mann Allison E AE Mitchell Elizabeth A EA Zhang Yan Y Curtis-Robles Rachel R Thapa Santosh S Hamer Sarah A SA Allen Michael S MS

Frontiers in microbiology 20200313

Chagas disease, caused by the hemoflagellate protist Trypanosoma cruzi, affects nearly 6 million people worldwide, mainly in Latin America. Hematophagous triatomine insects ("kissing bugs") are the primary vectors of T. cruzi throughout the Americas and feed on a variety of animals, including humans. Control of triatomines is central to the control of T. cruzi infection. Recent advances in mitigation of other insect-borne diseases via the manipulation of insect-associated ba ...[more]

PMID: 32231645

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Project description:Little is known about the strains of Trypanosoma cruzi circulating in Central America and specifically in the most important vector in this region, Triatoma dimidiata. Approximately six million people are infected with T. cruzi, the causative agent of Chagas disease, which has the greatest negative economic impact and is responsible for ~12,000 deaths annually in Latin America. By international consensus, strains of T. cruzi are divided into six monophyletic clades called discrete typing units (DTUs TcI-VI) and a seventh DTU first identified in bats called TcBat. TcI shows the greatest geographic range and diversity. Identifying strains present and diversity within these strains is important as different strains and their genotypes may cause different pathologies and may circulate in different localities and transmission cycles, thus impacting control efforts, treatment and vaccine development. To determine parasite strains present in T. dimidiata across its geographic range from Mexico to Colombia, we isolated abdominal DNA from T. dimidiata and determined which specimens were infected with T. cruzi by PCR. Strains from infected insects were determined by comparing the sequence of the 18S rDNA and the spliced-leader intergenic region to typed strains in GenBank. Two DTUs were found: 94% of infected T. dimidiata contained TcI and 6% contained TcIV. TcI exhibited high genetic diversity. Geographic structure of TcI haplotypes was evident by Principal Component and Median-Joining Network analyses as well as a significant result in the Mantel test, indicating isolation by distance. There was little evidence of association with TcI haplotypes and host/vector or ecotope. This study provides new information about the strains circulating in the most important Chagas vector in Central America and reveals considerable variability within TcI as well as geographic structuring at this large geographic scale. The lack of association with particular vectors/hosts or ecotopes suggests the parasites are moving among vectors/hosts and ecotopes therefore a comprehensive approach, such as the Ecohealth approach that makes houses refractory to the vectors will be needed to successfully halt transmission of Chagas disease.

Project description:BACKGROUND:Trypanosoma cruzi, causative agent of Chagas disease in humans and dogs, is a vector-borne zoonotic protozoan parasite that can cause fatal cardiac disease. While recognized as the most economically important parasitic infection in Latin America, the incidence of Chagas disease in the United States of America (US) may be underreported and even increasing. The extensive genetic diversity of T. cruzi in Latin America is well-documented and likely influences disease progression, severity and treatment efficacy; however, little is known regarding T. cruzi strains endemic to the US. It is therefore important to expand our knowledge on US T. cruzi strains, to improve upon the recognition of and response to locally acquired infections. METHODOLOGY/PRINCIPLE FINDINGS:We conducted a study of T. cruzi molecular diversity in California, augmenting sparse genetic data from southern California and for the first time investigating genetic sequences from northern California. The vector Triatoma protracta was collected from southern (Escondido and Los Angeles) and northern (Vallecito) California regions. Samples were initially screened via sensitive nuclear repetitive DNA and kinetoplast minicircle DNA PCR assays, yielding an overall prevalence of approximately 28% and 55% for southern and northern California regions, respectively. Positive samples were further processed to identify discrete typing units (DTUs), revealing both TcI and TcIV lineages in southern California, but only TcI in northern California. Phylogenetic analyses (targeting COII-ND1, TR and RB19 genes) were performed on a subset of positive samples to compare Californian T. cruzi samples to strains from other US regions and Latin America. Results indicated that within the TcI DTU, California sequences were similar to those from the southeastern US, as well as to several isolates from Latin America responsible for causing Chagas disease in humans. CONCLUSIONS/SIGNIFICANCE:Triatoma protracta populations in California are frequently infected with T. cruzi. Our data extend the northern limits of the range of TcI and identify a novel genetic exchange event between TcI and TcIV. High similarity between sequences from California and specific Latin American strains indicates US strains may be equally capable of causing human disease. Additional genetic characterization of Californian and other US T. cruzi strains is recommended.

Dataset Information

Comparison of the Bacterial Gut Microbiome of North American Triatoma spp. With and Without Trypanosoma cruzi.

Publications

Comparison of the Bacterial Gut Microbiome of North American <i>Triatoma</i> spp. With and Without <i>Trypanosoma cruzi</i>.

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