“Mi Casa, Tu Casa”: the coati nest as a hub of Trypanosoma cruzi transmission in the southern Pantanal biome revealed by molecular blood meal source identification in triatomines

Abstract

Background The study of the ecology of Trypanosoma cruzi is challenging due to its extreme adaptive plasticity, resulting in the parasitism of hundreds of mammal species and dozens of triatomine species. The genetic analysis of blood meal sources (BMS) from the triatomine vector is an accurate and practical approach for gathering information on which wild mammal species participate in a local transmission network. South American coatis, Nasua nasua, act as important reservoir host species of T. cruzi in the Pantanal biome because of their high rate of infection and elevated parasitemia, with the main discrete typing unit (DTU) lineages (TcI and TcII). Moreover, the carnivore coati is the only mammal species to build high arboreal nests for breeding and resting that can be shared by various vertebrate and invertebrate species. Herein, we applied the sensitive and specific methodology of DNA barcoding and molecular cloning to study triatomines found in a coati nest to access the diversity of mammal species that explore this structure, and therefore, may be involved in the parasite transmission network. Methods Twenty-three Triatoma sordida were collected in one coati’s nest in the subregion of Nhecolândia, Pantanal. The DNA isolated from the gut of insects was subjected to BMS detection by PCR using universal primers that flank variable regions of the cytochrome b (cytb) and 12S rDNA mitochondrial genes from vertebrates. The Trypanosoma spp. diagnosis and DTU genotyping were based on an 18S rDNA molecular marker and also using new cytb gene primers designed in this study. Phylogenetic analyses and chord diagrams were constructed to visualize BMS haplotypes, DTU lineages detected on vectors, and their interconnections. Results Twenty of 23 triatomines analyzed were PCR-positive (86.95%) showing lineages T. cruzi DTU TcI (n = 2), TcII (n = 6), and a predominance of TcI/TcII (n = 12) mixed infection. Intra-DTU diversity was observed mainly from different TcI haplotypes. Genetic analyses revealed that the southern anteater, Tamandua tetradactyla, was the unique species detected as the BMS of triatomines collected from the coati’s nest. At least three different individuals of T. tetradactyla served as BMS of 21/23 bugs studied, as indicated by the cytb and 12S rDNA haplotypes identified. Conclusions The identification of multiple BMS, and importantly, different individuals of the same species, was achieved by the methodology applied. The study demonstrated that the southern anteaters can occupy the South American coati’s nest, serving as the BMS of T. sordida specimens. Since anteaters have an individualist nonsocial behavior, the three individuals detected as BMS stayed at the coati’s nest at different times, which added a temporal character to BMS detection. The TcI and TcII infection, and significantly, a predominance of TcI/TcII mixed infection profile with different TcI and TcII haplotypes was observed, due to the discriminatory capacity of the methodology applied. Tamandua tetradactyla, a host which has been little studied, may have an important role in the T. cruzi transmission in that Pantanal subregion. The data from the present study indicate the sharing of coatis’ nests by other mammal species, expanding the possibilities for T. cruzi transmission in the canopy strata. We propose that coatis’ nests can act as the true hubs of the T. cruzi transmission web in Pantanal, instead of the coatis themselves, as previously suggested. Graphical Abstract

Vector mapping and bloodmeal metabarcoding demonstrate risk of urban Chagas disease transmission in Caracas, Venezuela

“…This update also describes triatomine biting reports by MDC inhabitants and uses cytochrome b (cytb) metabarcoding to provide a snapshot of triatomine blood feeding patterns in the parishes with highest triatomine collection yield. Bloodmeal metabarcoding (most often targeting cytb and 12S) is widely used in the study of Chagas disease vector ecology [22][23][24][25][26][27][28][29][30]. For example, this tool has helped infer triatomine dispersal rates between wild and human-inhabited ecotopes (e.g., cases of high connectivity and re-infestation potential shown for T. infestans in Bolivia [22] and T. dimidiata in Ecuador [23]), or gauge triatomine diet specialization and overlap (e.g., within [24] and across triatomine species in Colombia [25]).…”

Ecological factors alter how spatial overlap predicts viral infection dynamics in wild rodent populations

“…Spatial overlap in the previous month drove the probability of current hantavirus infection, indicating a link between shared use of the environment and pathogen exposure. Most knowledge of how spatial overlap shapes environmental pathogen transmission has focused on key spatial locations where wildlife congregate, such as dens, nests, or refuges (Corner et al, 2003; Godfrey et al, 2009; Pessanha et al, 2023) or point sources of food or water (Garnett et al, 2002; Titcomb et al, 2021). Studies exploring the role of spatial overlap more broadly have found mixed effects on transmission-related outcomes: spatial overlap predicted contact rates in racoons (Robert et al, 2012) and predicted tick loads and tick-borne blood parasite infection in a territorial lizard (Godfrey et al, 2010), but did not predict faecal-oral bacterial infection in studies of lizards and giraffes (Bull et al, 2012; VanderWaal et al, 2014).…”

“…We also found weak support for previous overlap with reproductive females decreasing the likelihood of current infection in non-reproductive voles (see Supplement: Fed-Control Treatment; Figure S3). key spatial locations where wildlife congregate, such as dens, nests, or refuges (35,44,77) or point sources of food or water (78,79). Studies exploring the role of spatial overlap more broadly have found mixed effects on transmission-related outcomes: spatial overlap predicted contact rates in racoons (80) and predicted tick loads and tick-borne blood parasite infection in a territorial lizard (45), but did not predict faecal-oral bacterial infection in other studies of lizards and giraffes (39,42).…”