High Trypanosoma spp. diversity is maintained by bats and triatomines in Espírito Santo state, Brazil

Abstract

The aim of this study was to reevaluate the ecology of an area in the Atlantic Forest, southeast Brazil, where Chagas disease (CD) has been found to occur. In a previous study, immediately after the occurrence of a CD case, we did not observe any sylvatic small mammals or dogs with Trypanosoma cruzi cruzi infections, but Triatoma vitticeps presented high T. c. cruzi infection rates. In this study, we investigated bats together with non-volant mammals, dogs, and triatomines to explore other possible T. c. cruzi reservoirs/hosts in the area. Seventy-three non-volant mammals and 186 bats were captured at three sites within the Guarapari municipality, Espírito Santo state. Rio da Prata and Amarelos sites exhibited greater richness in terms of non-volant mammals and bats species, respectively. The marsupial Metachirus nudicaudatus, the rodent Trinomys paratus, and the bats Artibeus lituratus and Carollia perspicillata were the most frequently captured species. As determined by positive hemocultures, only two non-volant mammals were found to be infected by Trypanosoma species: Monodelphis americana, which was infected by T. cascavelli, T. dionisii and Trypanosoma sp., and Callithrix geoffroyi, which was infected by T. minasense. Bats presented T. c. cruzi TcI and TcIII/V, T. c. marinkellei, T. dionisii, T. rangeli B and D, and Trypanosoma sp. infections. Seven dogs were infected with T. cruzi based only on serological exams. The triatomines T. vitticeps and Panstrongylus geniculatus were found to be infected by trypanosomes via microscopy. According to molecular characterization, T. vitticeps specimens were infected with T. c. cruzi TcI, TcII, TcIII/V, and TcIV, T. c. marinkellei and T. dionisii. We observed high trypanosome diversity in a small and fragmented region of the Atlantic Forest. This diversity was primarily maintained by bats and T. vitticeps. Our findings show that the host specificity of the Trypanosoma genus should be thoroughly reviewed. In addition, our data show that CD cases can occur without an enzootic cycle near residential areas.

Biological and Genetic Heterogeneity in Trypanosoma dionisii Isolates from Hematophagous and Insectivorous Bats

“…To date, most of these studies have concentrated on the T. c. cruzi and T. rangeli species, as high morphological, biological, biochemical, and molecular variability has been observed in these species [ 30 , 31 ]. Studies regarding differences among T. dionisii isolates are scarce, and most recent publications have focused solely on the molecular identification of this parasite in both hosts and vectors from Brazil and some other countries [ 7 , 8 , 10 , 11 , 12 , 18 ]. The three isolates of T. dionisii investigated (M1011, M1014, and M1015) were obtained in a study in different municipalities of Rio de Janeiro, where 22 samples of trypanosomatids were isolated by hemoculture of 84 bats [ 32 ].…”

“…In Brazil, T. dionisii is found in almost all biomes, including the Amazon, Atlantic Forest, Cerrado, Pantanal, and transition areas of the Pantanal and Cerrado. The protozoan infects different bat families, including Phyllostomidae, Molossidae, Noctilionidae, and Vespertilionidae in various regions from northern to southern Brazil [ 4 , 10 , 11 , 12 , 13 ].…”

Trypanosoma cruzi transmission in the wild and its most important reservoir hosts in Brazil

“…A very interesting and puzzling finding was reported by Dario et al [ 44 ] who observed one Monodelphis americana (Didelphimorphia) specimen infected simultaneously with T . cascavelli , T .…”

“…The use of even more sensitive and high-performance tools like NGS would certainly demonstrate even greater diversity of genotypes and species in single and mixed infections in bats. In addition to bats, marsupials have also been found infected with numerous species of Trypanosoma including T. dionisii , a species considered to be an exclusive parasite of bats until recently [ 44 ]. An important question concerns the result of such mixed infections in hosts: what are the consequences in the outcome in such mixed infections?…”

Amazonian Reservoir Hosts of Trypanosoma cruzi

“…For instance, a mixed, triple infection with Trypanosoma cascavelli (reported in reptiles), Trypanosoma dionisii (reported in bats) and Trypanosoma sp. was reported in Monodelphis americana [27]. Other species such as Philander opossum show a high prevalence of T. cruzi positive hemoculture implying its ability to infect vectors.…”