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Ontogeny, species identity and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae)

Joel J. Brown, Sonia M. Rodríguez-Ruano, Anbu Poosakkannu, Giampiero Batani, Justin O. Schmidt, Walter Roachell, Jan Zima Jr., Václav Hypša, View ORCID ProfileEva Nováková
doi: https://doi.org/10.1101/2020.06.05.135871
Joel J. Brown
1University of South Bohemia, Faculty of Science, Ceske Budejovice, Czech Republic
2Biology Centre of the Czech Academy of Sciences, Institute of Entomology, Ceske Budejovice, Czech Republic
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Sonia M. Rodríguez-Ruano
1University of South Bohemia, Faculty of Science, Ceske Budejovice, Czech Republic
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Anbu Poosakkannu
1University of South Bohemia, Faculty of Science, Ceske Budejovice, Czech Republic
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Giampiero Batani
1University of South Bohemia, Faculty of Science, Ceske Budejovice, Czech Republic
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Justin O. Schmidt
3Southwestern Biological Institute, Tucson, Arizona, USA
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Walter Roachell
4US Army Public Health Command-Central, JBSA Fort Sam Houston, Texas, USA
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Jan Zima Jr.
1University of South Bohemia, Faculty of Science, Ceske Budejovice, Czech Republic
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Václav Hypša
1University of South Bohemia, Faculty of Science, Ceske Budejovice, Czech Republic
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Eva Nováková
1University of South Bohemia, Faculty of Science, Ceske Budejovice, Czech Republic
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  • ORCID record for Eva Nováková
  • For correspondence: novake01@prf.jcu.cz
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Abstract

Background Kissing bugs (Triatominae) are blood-feeding insects best known as the vectors of Trypanosoma cruzi, the causative agent of Chagas’ disease. Considering the high epidemiological relevance of these vectors, their biology and bacterial symbiosis remains surprisingly understudied. While previous investigations revealed generally low individual complexity but high among-individual variability of the triatomine microbiomes, any consistent microbiome determinants have not yet been identified across multiple Triatominae species.

Methods To obtain a more comprehensive view of triatomine microbiomes, we investigated the host-microbiome relationship of five Triatoma species sampled from white-throated woodrat (Neotoma albigula) nests in multiple locations across the USA. We applied optimized 16S rRNA gene metabarcoding with a novel 18S rRNA gene blocking primer to a set of 170 T. cruzi negative individuals across all six instars.

Results Triatomine gut microbiome composition is strongly influenced by three principal factors: ontogeny, species identity, and the environment. The microbiomes are characterised by significant loss in bacterial diversity throughout ontogenetic development. First instars possess the highest bacterial diversity while adult microbiomes are routinely dominated by a single taxon. Primarily, the bacterial genus Dietzia dominates late-stage nymphs and adults of T. rubida, T. protracta, and T. lecticularia, but is not present in the phylogenetically more distant T. gerstaeckeri and T. sanguisuga. Species-specific microbiome composition, particularly pronounced in early instars, is further modulated by locality-specific effects. In addition, pathogenic bacteria of the genus Bartonella, acquired from the vertebrate hosts, are an abundant component of Triatoma microbiomes.

Conclusion Our study is the first to demonstrate deterministic patterns in microbiome composition among all life stages and multiple Triatoma species. We hypothesize that triatomine microbiome assemblages are produced by species- and life stage-dependent uptake of environmental bacteria and multiple indirect transmission strategies that promote bacterial transfer between individuals. Altogether, our study highlights the complexity of Triatominae symbiosis with bacteria and warrant further investigation to understand microbiome function in these important vectors.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 06, 2020.
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Ontogeny, species identity and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae)
Joel J. Brown, Sonia M. Rodríguez-Ruano, Anbu Poosakkannu, Giampiero Batani, Justin O. Schmidt, Walter Roachell, Jan Zima Jr., Václav Hypša, Eva Nováková
bioRxiv 2020.06.05.135871; doi: https://doi.org/10.1101/2020.06.05.135871
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Ontogeny, species identity and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae)
Joel J. Brown, Sonia M. Rodríguez-Ruano, Anbu Poosakkannu, Giampiero Batani, Justin O. Schmidt, Walter Roachell, Jan Zima Jr., Václav Hypša, Eva Nováková
bioRxiv 2020.06.05.135871; doi: https://doi.org/10.1101/2020.06.05.135871

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