TY  - JOUR
A1  - Eberhard, Fanny E.
A1  - Klimpel, Sven
A1  - Guarneri, Alessandra A.
A1  - Tobias, Nicholas J.
T1  - Exposure to Trypanosoma parasites induces changes in the microbiome of the Chagas disease vector Rhodnius prolixus
T2  - Microbiome
N2  - Background: The causative agent of Chagas disease, Trypanosoma cruzi, and its nonpathogenic relative, Trypanosoma rangeli, are transmitted by haematophagous triatomines and undergo a crucial ontogenetic phase in the insect’s intestine. In the process, the parasites interfere with the host immune system as well as the microbiome present in the digestive tract potentially establishing an environment advantageous for development. However, the coherent interactions between host, pathogen and microbiota have not yet been elucidated in detail. We applied a metagenome shotgun sequencing approach to study the alterations in the microbiota of Rhodnius prolixus, a major vector of Chagas disease, after exposure to T. cruzi and T. rangeli focusing also on the functional capacities present in the intestinal microbiome of the insect.
Results: The intestinal microbiota of R. prolixus was dominated by the bacterial orders Enterobacterales, Corynebacteriales, Lactobacillales, Clostridiales and Chlamydiales, whereas the latter conceivably originated from the blood used for pathogen exposure. The anterior and posterior midgut samples of the exposed insects showed a reduced overall number of organisms compared to the control group. However, we also found enriched bacterial groups after exposure to T. cruzi as well as T rangeli. While the relative abundance of Enterobacterales and Corynebacteriales decreased considerably, the Lactobacillales, mainly composed of the genus Enterococcus, developed as the most abundant taxonomic group. This applies in particular to vectors challenged with T. rangeli and at early timepoints after exposure to vectors challenged with T. cruzi. Furthermore, we were able to reconstruct four metagenome-assembled genomes from the intestinal samples and elucidate their unique metabolic functionalities within the triatomine microbiome, including the genome of a recently described insect symbiont, Candidatus Symbiopectobacterium, and the secondary metabolites producing bacteria Kocuria spp.
Conclusions: Our results facilitate a deeper understanding of the processes that take place in the intestinal tract of triatomine vectors during colonisation by trypanosomal parasites and highlight the influential aspects of pathogen-microbiota interactions. In particular, the mostly unexplored metabolic capacities of the insect vector’s microbiome are clearer, underlining its role in the transmission of Chagas disease.
KW  - Intestinal bacterial community
KW  - Triatominae
KW  - Host-parasite interaction
KW  - Trypanosoma cruzi
KW  - Trypanosoma rangeli
KW  - Secondary metabolites
KW  - Metagenomic shotgun sequencing
Y1  - 2022
UR  - http://publikationen.ub.uni-frankfurt.de/frontdoor/index/index/docId/69785
UR  - https://nbn-resolving.org/urn:nbn:de:hebis:30:3-697855
SN  - 2049-2618
N1  - Open Access funding enabled and organized by Projekt DEAL. This work was funded by the LOEWE-Centre TBG supported by the Hessen State Ministry of Higher Education, Research and the Arts (HMWK), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, CRA-APQ-00569-15 and CRA-PPM-00162-17) and Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCTEM/CNPq, 465678/2014-9).
N1  - The metagenomic sequencing data analysed during the current study are available in the NCBI Sequence Read Archive (SRA) under BioProject accession number PRJNA744378 (https://www.ncbi.nlm.nih.gov/bioproject/744378). Metagenome-assembled genomes have been deposited in NCBI BioSample and are available under the accessions SAMN20089395, SAMN20089396, SAMN20089397 and SAMN20089398.
N1  - The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
VL  - 10.2022
IS  - art. 45
SP  - 1
EP  - 19
PB  - Biomed Central
CY  - London
ER  -