Hindgut microbiota in laboratory-reared and wild Triatoma infestans

Abstract

Triatomine vectors transmit Trypanosoma cruzi , the etiological agent of Chagas disease in humans. Transmission to humans typically occurs when contaminated triatomine feces come in contact with the bite site or mucosal membranes. In the Southern Cone of South America, where the highest burden of disease exists, Triatoma infestans is the principal vector for T . cruzi . Recent studies of other vector-borne illnesses have shown that arthropod microbiota influences the ability of infectious agents to colonize the insect vector and transmit to the human host. This has garnered attention as a potential control strategy against T . cruzi , as vector control is the main tool of Chagas disease prevention. Here we characterized the microbiota in T . infestans feces of both wild-caught and laboratory-reared insects and examined the relationship between microbial composition and T . cruzi infection using highly sensitive high-throughput sequencing technology to sequence the V3-V4 region of the 16S ribosomal RNA gene on the MiSeq Illumina platform. We collected 59 wild (9 with T . cruzi infection) and 10 lab-reared T . infestans (4 with T . cruzi infection) from the endemic area of Arequipa, Perú. Wild T . infestans had greater hindgut bacterial diversity than laboratory-reared bugs. Microbiota of lab insects comprised a subset of those identified in their wild counterparts, with 96 of the total 124 genera also observed in laboratory-reared insects. Among wild insects, variation in bacterial composition was observed, but time and location of collection and development stage did not explain this variation. T . cruzi infection in lab insects did not affect α- or β-diversity; however, we did find that the β-diversity of wild insects differed if they were infected with T . cruzi and identified 10 specific taxa that had significantly different relative abundances in infected vs . uninfected wild T . infestans ( Bosea , Mesorhizobium , Dietzia , and Cupriavidus were underrepresented in infected bugs; Sporosarcina , an unclassified genus of Porphyromonadaceae , Nestenrenkonia , Alkalibacterium , Peptoniphilus , Marinilactibacillus were overrepresented in infected bugs). Our findings suggest that T . c...

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

“…Similar findings are reported for two species of North American Triatoma, in which the authors further conclude that T. cruzi infection leads to apparent increases in bacterial diversity within the triatomine host gut (Rodríguez-Ruano et al, 2018). The finding of increased bacterial diversity in the hindgut of T. cruzi-infected triatomines is consistent with previously reported changes in the gut microbiome and host physiology upon T. cruzi infection in South American triatomines (Vieira et al, 2015;Díaz et al, 2016), though another study found no impact of T. cruzi infection on alpha diversity metrics in both lab-reared and wild triatomine individuals (Waltmann et al, 2019). These studies point to the potential shaping of the triatomine gut microbial population by T. cruzi during infection but also the dynamic nature of the hindgut community that may be governed by a variety of factors including interspecies variation, collection location, sex, life cycle stage, and wild versus lab-reared populations.…”

“…If there are microbial targets living in the hindgut of triatomines that may be effective for T. cruzi control, the relative impact of transient microbes on the interpretation of these communities must be verified. Despite the potential impact of transient microbes in the interpretation of overall diversity, we found a pattern of differential abundance of specific bacterial groups in T. cruzipositive and T. cruzi-negative individuals, one of which (i.e., members of the Porphyromonadacea family -in the current study represented by Petrimonas) has been previously reported as enriched in T. cruzi-positive members of Triatoma infestans collected from Peru (Waltmann et al, 2019). This result motivates further investigation of diverse species of triatomine insects to clarify the relationship between specific bacterial taxa and the T. cruzi parasite.…”

“…The large number of variables in this study may have masked most of the effects that T. cruzi exerts on its host bacterial microbiome, as reported elsewhere (Díaz et al, 2016;Rodríguez-Ruano et al, 2018). However, another study on the effect of T. cruzi infection status on the triatomine gut microbiome found a similar lack of impact on bacterial diversity (Waltmann et al, 2019), suggesting that increased species sampling and controls are necessary to fully appreciate the interaction between T. cruzi and the larger microbial community. The impact of T. cruzi infection on the gut microbiome of triatomines may also be related to the time since infection, which was an unknown variable in the current study due to the wild-caught nature of the triatomines.…”

“…Bacterial gut communities among different arthropods are known to vary widely in composition, function, and response to the environment (Engel and Moran, 2013;Menchaca et al, 2013). Gut microbiome studies in South American triatomines further indicate this high level of variability (da Mota et al, 2012;Gumiel et al, 2015;Díaz et al, 2016;Montoya-Porras et al, 2018;Waltmann et al, 2019). da Mota et al (2012) report relatively low overall species complexity in the gut microbiomes of South American triatomine bugs.…”

“…To date, few studies have examined the gut microbiome of triatomine vectors, and even fewer have looked at Triatoma spp. collected in the United States (da Mota et al, 2012;Gumiel et al, 2015;Díaz et al, 2016;Montoya-Porras et al, 2018;Rodríguez-Ruano et al, 2018;Waltmann et al, 2019). The composition and diversity of insect gut bacteria could play a significant role, not only in the life cycle of the insect itself (Rodríguez-Ruano et al, 2018), but also in relation to the life cycles of the parasites that they vector, including whether the insect is able to competently harbor and/or transmit various microbes to hosts (Engel and Moran, 2013;Goodrich Julia et al, 2014;Teotônio et al, 2019).…”