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. 2022 Feb 11:12:812708.
doi: 10.3389/fcimb.2022.812708. eCollection 2022.

Trypanosoma Species in Small Nonflying Mammals in an Area With a Single Previous Chagas Disease Case

Maria Augusta Dario  1 , Cristiane Varella Lisboa  1 , Samanta Cristina das Chagas Xavier  1 , Paulo Sérgio D'Andrea  2 , André Luiz Rodrigues Roque  1 , Ana Maria Jansen  1
Affiliations

Trypanosoma Species in Small Nonflying Mammals in an Area With a Single Previous Chagas Disease Case

Maria Augusta Dario et al. Front Cell Infect Microbiol. .

Abstract

Trypanosomatids are hemoflagellate parasites that even though they have been increasingly studied, many aspects of their biology and taxonomy remain unknown. The aim of this study was to investigate the Trypanosoma sp. transmission cycle in nonflying small mammals in an area where a case of acute Chagas disease occurred in Mangaratiba municipality, Rio de Janeiro state. Three expeditions were conducted in the area: the first in 2012, soon after the human case, and two others in 2015. Sylvatic mammals were captured and submitted to blood collection for trypanosomatid parasitological and serological exams. Dogs from the surrounding areas where the sylvatic mammals were captured were also tested for T. cruzi infection. DNA samples were extracted from blood clots and positive hemocultures, submitted to polymerase chain reaction targeting SSU rDNA and gGAPDH genes, sequenced and phylogenetic analysed. Twenty-one wild mammals were captured in 2012, mainly rodents, and 17 mammals, mainly marsupials, were captured in the two expeditions conducted in 2015. Only four rodents demonstrated borderline serological T. cruzi test (IFAT), two in 2012 and two in 2015. Trypanosoma janseni was the main Trypanosoma species identified, and isolates were obtained solely from Didelphis aurita. In addition to biological differences, molecular differences are suggestive of genetic diversity in this flagellate species. Trypanosoma sp. DID was identified in blood clots from D. aurita in single and mixed infections with T. janseni. Concerning dogs, 12 presented mostly borderline serological titers for T. cruzi and no positive hemoculture. In blood clots from 11 dogs, T. cruzi DNA was detected and characterized as TcI (n = 9) or TcII (n = 2). Infections by Trypanosoma rangeli lineage E (n = 2) and, for the first time, Trypanosoma caninum, Trypanosoma dionisii, and Crithidia mellificae (n = 1 each) were also detected in dogs. We concluded that despite the low mammalian species richness and degraded environment, a high Trypanosoma species richness species was being transmitted with the predominance of T. janseni and not T. cruzi, as would be expected in a locality of an acute case of Chagas disease.

Keywords: Atlantic Forest; Trypanosoma cruzi clade; Trypanosomatidae; infection; mammalian host.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Mangaratiba municipality study locations in 2012 and 2015. The red star represents the area where acute CD occurred in 2012. The blue dot is where the Cunhambebe Park is located. Data source: Instituto Brasileiro de Geografia e Estatística—IBGE (www.ibge.gov.br); Google Earth (https://www.google.com.br/intl/pt-BR/earth/).
Figure 2
Figure 2
Concatenated (SSU rDNA + gGAPDH) T. cruzi clade phylogenetic tree based on 1121 base pair fragment lengths of sylvatic mammal hemocultures. The tree was inferred using transitional3 equal frequencies plus gamma distribution (TIM3e+G) and generalized time reversible with invariant sites and amino acid frequencies plus gamma distribution (GTR+F+I+G) models for ML and BI, respectively. The numbers at nodes correspond to ML (ultrabootstrap, SH-aLRT) and BI (posterior probability). The scale bar shows the number of nucleotide substitutions per site. The red square represents group formed T. janseni sequences from different culture isolation.
Figure 3
Figure 3
Trypanosoma cruzi clade phylogenetic tree based on 692 base pair SSU rDNA fragment lengths from sylvatic mammal and dog blood clots. The tree was inferred using transitional3 with amino acid frequencies and freeRate heterogeneity (TIM3+F+R2) and generalized time reversible with amino acid frequencies plus gamma distribution (GTR+F+G) models for ML and BI, respectively. The numbers at nodes correspond to ML (ultrabootstrap and SH-aLRT) and BI (posterior probability). The scale bar shows the number of nucleotide substitutions per site. The blood clot samples grouped with T. cruzi, T. rangeli, Trypanosoma sp. DID and T. janseni. The blue curly brackets represent the sequences that grouped with T. cruzi TcI sequences. The green curly brackets represent the sequences that grouped with T. cruzi TcII/TcVI sequences. The purple curly brackets represent the sequences that grouped with T. rangeli lineage E sequences. The red curly brackets represent the sequences that grouped with Trypanosoma sp. DID sequences.
Figure 4
Figure 4
Crithidia mellificae phylogenetic tree based on 528 base pairs SSU rDNA fragment length from dog blood clot. The tree was inferred using transitional3 equal frequencies plus gamma distribution (TIM3e+G) and symmetrical plus gamma distribution (SYM+G) models for ML and BI, respectively. The numbers at nodes correspond to ML (ultrabootstrap and SH-aLRT) and BI (posterior probability). The scale bar shows the number of nucleotide substitutions per site. The green square represents the clade formed by LBT6704 with other C. mellifiace sequences from insects and mammals.
Figure 5
Figure 5
Trypanosoma caninum phylogenetic tree based on 605 base pair SSU rDNA fragment lengths from dog blood clots. The tree was inferred using transitional with amino acid frequencies and freeRate heterogeneity (TIM+F+R2) and symmetrical plus gamma distribution (SYM+G) models for ML and BI, respectively. The numbers at nodes correspond to ML (ultrabootstrap, SH-aLRT) and BI (posterior probability). The scale bar shows the number of nucleotide substitutions per site. The blue square represents the clade formed by LBT6702 with other T. caninum sequences from different Brazilian states.
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