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The holobiont transcriptome of teneral tsetse fly species of varying vector competence

BACKGROUND: Tsetse flies are the obligate vectors of African trypanosomes, which cause Human and Animal African Trypanosomiasis. Teneral flies (newly eclosed adults) are especially susceptible to parasite establishment and development, yet our understanding of why remains fragmentary. The tsetse gut...

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Autores principales: Medina Munoz, Miguel, Brenner, Caitlyn, Richmond, Dylan, Spencer, Noah, Rio, Rita V. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8166097/
https://www.ncbi.nlm.nih.gov/pubmed/34058984
http://dx.doi.org/10.1186/s12864-021-07729-5
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author Medina Munoz, Miguel
Brenner, Caitlyn
Richmond, Dylan
Spencer, Noah
Rio, Rita V. M.
author_facet Medina Munoz, Miguel
Brenner, Caitlyn
Richmond, Dylan
Spencer, Noah
Rio, Rita V. M.
author_sort Medina Munoz, Miguel
collection PubMed
description BACKGROUND: Tsetse flies are the obligate vectors of African trypanosomes, which cause Human and Animal African Trypanosomiasis. Teneral flies (newly eclosed adults) are especially susceptible to parasite establishment and development, yet our understanding of why remains fragmentary. The tsetse gut microbiome is dominated by two Gammaproteobacteria, an essential and ancient mutualist Wigglesworthia glossinidia and a commensal Sodalis glossinidius. Here, we characterize and compare the metatranscriptome of teneral Glossina morsitans to that of G. brevipalpis and describe unique immunological, physiological, and metabolic landscapes that may impact vector competence differences between these two species. RESULTS: An active expression profile was observed for Wigglesworthia immediately following host adult metamorphosis. Specifically, ‘translation, ribosomal structure and biogenesis’ followed by ‘coenzyme transport and metabolism’ were the most enriched clusters of orthologous genes (COGs), highlighting the importance of nutrient transport and metabolism even following host species diversification. Despite the significantly smaller Wigglesworthia genome more differentially expressed genes (DEGs) were identified between interspecific isolates (n = 326, ~ 55% of protein coding genes) than between the corresponding Sodalis isolates (n = 235, ~ 5% of protein coding genes) likely reflecting distinctions in host co-evolution and adaptation. DEGs between Sodalis isolates included genes involved in chitin degradation that may contribute towards trypanosome susceptibility by compromising the immunological protection provided by the peritrophic matrix. Lastly, G. brevipalpis tenerals demonstrate a more immunologically robust background with significant upregulation of IMD and melanization pathways. CONCLUSIONS: These transcriptomic differences may collectively contribute to vector competence differences between tsetse species and offers translational relevance towards the design of novel vector control strategies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07729-5.
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spelling pubmed-81660972021-06-02 The holobiont transcriptome of teneral tsetse fly species of varying vector competence Medina Munoz, Miguel Brenner, Caitlyn Richmond, Dylan Spencer, Noah Rio, Rita V. M. BMC Genomics Research Article BACKGROUND: Tsetse flies are the obligate vectors of African trypanosomes, which cause Human and Animal African Trypanosomiasis. Teneral flies (newly eclosed adults) are especially susceptible to parasite establishment and development, yet our understanding of why remains fragmentary. The tsetse gut microbiome is dominated by two Gammaproteobacteria, an essential and ancient mutualist Wigglesworthia glossinidia and a commensal Sodalis glossinidius. Here, we characterize and compare the metatranscriptome of teneral Glossina morsitans to that of G. brevipalpis and describe unique immunological, physiological, and metabolic landscapes that may impact vector competence differences between these two species. RESULTS: An active expression profile was observed for Wigglesworthia immediately following host adult metamorphosis. Specifically, ‘translation, ribosomal structure and biogenesis’ followed by ‘coenzyme transport and metabolism’ were the most enriched clusters of orthologous genes (COGs), highlighting the importance of nutrient transport and metabolism even following host species diversification. Despite the significantly smaller Wigglesworthia genome more differentially expressed genes (DEGs) were identified between interspecific isolates (n = 326, ~ 55% of protein coding genes) than between the corresponding Sodalis isolates (n = 235, ~ 5% of protein coding genes) likely reflecting distinctions in host co-evolution and adaptation. DEGs between Sodalis isolates included genes involved in chitin degradation that may contribute towards trypanosome susceptibility by compromising the immunological protection provided by the peritrophic matrix. Lastly, G. brevipalpis tenerals demonstrate a more immunologically robust background with significant upregulation of IMD and melanization pathways. CONCLUSIONS: These transcriptomic differences may collectively contribute to vector competence differences between tsetse species and offers translational relevance towards the design of novel vector control strategies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07729-5. BioMed Central 2021-05-31 /pmc/articles/PMC8166097/ /pubmed/34058984 http://dx.doi.org/10.1186/s12864-021-07729-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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.
spellingShingle Research Article
Medina Munoz, Miguel
Brenner, Caitlyn
Richmond, Dylan
Spencer, Noah
Rio, Rita V. M.
The holobiont transcriptome of teneral tsetse fly species of varying vector competence
title The holobiont transcriptome of teneral tsetse fly species of varying vector competence
title_full The holobiont transcriptome of teneral tsetse fly species of varying vector competence
title_fullStr The holobiont transcriptome of teneral tsetse fly species of varying vector competence
title_full_unstemmed The holobiont transcriptome of teneral tsetse fly species of varying vector competence
title_short The holobiont transcriptome of teneral tsetse fly species of varying vector competence
title_sort holobiont transcriptome of teneral tsetse fly species of varying vector competence
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8166097/
https://www.ncbi.nlm.nih.gov/pubmed/34058984
http://dx.doi.org/10.1186/s12864-021-07729-5
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