Abstract
BackgroundBats are a highly successful, globally dispersed order of mammals that occupy a wide array of ecological niches. They are also intensely parasitized and implicated in multiple viral, bacterial and parasitic zoonoses. Trypanosomes are thought to be especially abundant and diverse in bats. In this study, we used 18S ribosomal RNA metabarcoding to probe bat trypanosome diversity in unprecedented detail.Methodology/Principal FindingsTotal DNA was extracted from the blood of 90 bat individuals (17 species) captured along Atlantic Forest fragments of Espírito Santo state, southeast Brazil. 18S ribosomal RNA was amplified by standard and/or nested PCR, then deep sequenced to recover and identify Operational Taxonomic Units (OTUs) for phylogenetic analysis. Blood samples from 34 bat individuals (13 species) tested positive for infection by 18S rRNA amplification. Amplicon sequences clustered to 14 OTUs, of which five were identified as Trypanosoma cruzi I, T. cruzi III/V, Trypanosoma cruzi marinkellei, Trypanosoma rangeli, and Trypanosoma dionisii, and seven were identified as novel genotypes monophyletic to basal T. cruzi clade types of the New World. Another OTU was identified as a trypanosome like those found in reptiles. Surprisingly, the remaining OTU was identified as Bodo saltans–closest non-parasitic relative of the trypanosomatid order. While three blood samples featured just one OTU (T. dionisii), all others resolved as mixed infections of up to eight OTUs.Conclusions/SignificanceThis study demonstrates the utility of next-generation barcoding methods to screen parasite diversity in mammalian reservoir hosts. We exposed high rates of local bat parasitism by multiple trypanosome species, some known to cause fatal human disease, others non-pathogenic, novel or yet little understood. Our results highlight bats as a long-standing nexus among host-parasite interactions of multiple niches, sustained in part by opportunistic and incidental infections of consequence to evolutionary theory as much as to public health.
Highlights
Trypanosoma cruzi is the etiological agent of Chagas disease, a complex zoonosis that continues to take dozens of human lives each day [1]
We focused on a degraded section of Atlantic Forest in Espırito Santo (ES) state where terrestrial mammals appear reduced in abundance as well as in T. cruzi infection
Of the 108 bats captured at Amarelos, Buenos Aires and Rio da Prata study sites, 105 individuals represent 16 species in the Phyllostomidae family, and three individuals represent one species (Myotis nigricans) in the Vespertilionidae family
Summary
Trypanosoma cruzi is the etiological agent of Chagas disease, a complex zoonosis that continues to take dozens of human lives each day [1]. Alongside its close relative Trypanosoma cruzi marinkellei in the Schizotrypanum subgenus, this important protozoan flagellate belongs to a broader, inter-continental group (the “T. cruzi clade”) of ancient endoparasites found to infect the mammalian fauna far and wide [2,3]. Infections have been reported in primates of Africa [4], marsupials of Australia [5] and a multitude of terrestrial mammals across the Americas [6], but most of this striking spread in host diversity tallies to few taxa within the clade (above all to T. cruzi sensu stricto, i.e., T. cruzi, and to T. rangeli). Bats are a highly successful, globally dispersed order of mammals that occupy a wide array of ecological niches. They are intensely parasitized and implicated in multiple viral, bacterial and parasitic zoonoses.
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