The holobiont transcriptome of teneral tsetse fly species of varying vector competence
Abstract 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 ts...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2021-05-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-021-07729-5 |
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| author | Miguel Medina Munoz Caitlyn Brenner Dylan Richmond Noah Spencer Rita V. M. Rio |
| author_facet | Miguel Medina Munoz Caitlyn Brenner Dylan Richmond Noah Spencer Rita V. M. Rio |
| author_sort | Miguel Medina Munoz |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-18T11:58:07Z |
| format | Article |
| id | doaj.art-f52b136b556548bea6222c91c76670d0 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-18T11:58:07Z |
| publishDate | 2021-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-f52b136b556548bea6222c91c76670d02022-12-21T21:09:01ZengBMCBMC Genomics1471-21642021-05-0122112010.1186/s12864-021-07729-5The holobiont transcriptome of teneral tsetse fly species of varying vector competenceMiguel Medina Munoz0Caitlyn Brenner1Dylan Richmond2Noah Spencer3Rita V. M. Rio4Department of Biology, Eberly College of Arts and Sciences, West Virginia UniversityDepartment of Biology, Washington and Jefferson CollegeDepartment of Biology, Eberly College of Arts and Sciences, West Virginia UniversityDepartment of Biology, Eberly College of Arts and Sciences, West Virginia UniversityDepartment of Biology, Eberly College of Arts and Sciences, West Virginia UniversityAbstract 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.https://doi.org/10.1186/s12864-021-07729-5SymbiosisRNA-SeqWigglesworthiaSodalisTsetseTeneral |
| spellingShingle | Miguel Medina Munoz Caitlyn Brenner Dylan Richmond Noah Spencer Rita V. M. Rio The holobiont transcriptome of teneral tsetse fly species of varying vector competence BMC Genomics Symbiosis RNA-Seq Wigglesworthia Sodalis Tsetse Teneral |
| 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 | Symbiosis RNA-Seq Wigglesworthia Sodalis Tsetse Teneral |
| url | https://doi.org/10.1186/s12864-021-07729-5 |
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