Field-collected Triatoma sordida from central Brazil display high microbiota diversity that varies with regard to developmental stage and intestinal segmentation

Joana L Oliveira; Juliano C Cury; Rodrigo Gurgel-Gonçalves; Ana C Bahia; Fernando A Monteiro

doi:10.1371/journal.pntd.0006709

Field-collected Triatoma sordida from central Brazil display high microbiota diversity that varies with regard to developmental stage and intestinal segmentation

PLoS Negl Trop Dis. 2018 Aug 23;12(8):e0006709. doi: 10.1371/journal.pntd.0006709. eCollection 2018 Aug.

Authors

Joana L Oliveira^{1

2}, Juliano C Cury³, Rodrigo Gurgel-Gonçalves⁴, Ana C Bahia², Fernando A Monteiro^{1

5}

Affiliations

¹ Laboratório de Epidemiologia e Sistemática Molecular, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil.
² Laboratório de Bioquímica de Insetos e Parasitos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
³ Departamento de Ciências Exatas e Biológicas, Universidade Federal de São João del-Rei, Campus de Sete Lagoas, Sete Lagoas, Minas Gerais, Brazil.
⁴ Laboratório de Parasitologia Médica e Biologia de Vetores, Faculdade de Medicina, Universidade de Brasília, Brasília, Distrito Federal, Brazil.
⁵ Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro, Brazil.

Abstract

Background/methodology: Triatomine bugs are the vectors of Trypanosoma cruzi, the agent of Chagas disease. Vector control has for decades relied upon insecticide spraying, but insecticide resistance has recently emerged in several triatomine populations. One alternative strategy to reduce T. cruzi transmission is paratransgenesis, whereby symbiotic bacteria are genetically engineered to produce T. cruzi-killing proteins in the vector's gut. This approach requires in-depth knowledge of the vectors' natural gut microbiota. Here, we use metagenomics (16S rRNA 454 pyrosequencing) to describe the gut microbiota of field-caught Triatoma sordida-likely the most common peridomestic triatomine in Brazil. For large nymphs (4th and 5th stage) and adults, we also studied separately the three main digestive-tract segments-anterior midgut, posterior midgut, and hindgut.

Principal findings: Bacteria of four phyla (12 genera) were present in both nymphs (all five stages) and adults, thus defining T. sordida's 'bacterial core': Actinobacteria (Brevibacterium, Corynebacterium, Dietzia, Gordonia, Nitriliruptor, Nocardia, Nocardiopsis, Rhodococcus, and Williamsia), Proteobacteria (Pseudomonas and Sphingobium), and Firmicutes (Staphylococcus). We found some clear differences in bacterial composition and relative abundance among development stages; overall, Firmicutes and Proteobacteria increased, but Actinobacteria decreased, through development. Finally, the bacterial microbiotas of the bugs' anterior midgut, posterior midgut, and hindgut were sharply distinct.

Conclusions/significance: Our results identify the 'bacterial core set' of T. sordida and reveal important gut microbiota differences among development stages-particularly between 1st-3rd stage nymphs and adults. Further, we show that, within any given development stage, the vectors' gut cannot be regarded as a single homogeneous environment. Cultivable, non-pathogenic 'core' bacterial species may now be tested as candidates for paratransgenic control of T. cruzi transmission by T. sordida.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bacteria / classification*
Brazil
Female
Gastrointestinal Microbiome*
Gastrointestinal Tract / microbiology*
Male
Nymph
RNA, Bacterial / genetics
RNA, Ribosomal, 16S / genetics
Triatoma / growth & development
Triatoma / microbiology*

Substances

RNA, Bacterial
RNA, Ribosomal, 16S

Grants and funding

Funding was provided through Chamada MCTI/CNPq/MS-SCTIE - Pesquisa em Doenças Negligenciadas, grant number 404522/2012-2. The funders had no role in in study design, data collection and analysis, decision to publish, or preparation of the manuscript.