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Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis

Tsetse flies (Glossina spp.) house a population-dependent assortment of microorganisms that can include pathogenic African trypanosomes and maternally transmitted endosymbiotic bacteria, the latter of which mediate numerous aspects of their host’s metabolic, reproductive, and immune physiologies. On...

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Autores principales: Son, Jae Hak, Weiss, Brian L., Schneider, Daniela I., Dera, Kiswend-sida M., Gstöttenmayer, Fabian, Opiro, Robert, Echodu, Richard, Saarman, Norah P., Attardo, Geoffrey M., Onyango, Maria, Abd-Alla, Adly M. M., Aksoy, Serap
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8478229/
https://www.ncbi.nlm.nih.gov/pubmed/34529715
http://dx.doi.org/10.1371/journal.ppat.1009539
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author Son, Jae Hak
Weiss, Brian L.
Schneider, Daniela I.
Dera, Kiswend-sida M.
Gstöttenmayer, Fabian
Opiro, Robert
Echodu, Richard
Saarman, Norah P.
Attardo, Geoffrey M.
Onyango, Maria
Abd-Alla, Adly M. M.
Aksoy, Serap
author_facet Son, Jae Hak
Weiss, Brian L.
Schneider, Daniela I.
Dera, Kiswend-sida M.
Gstöttenmayer, Fabian
Opiro, Robert
Echodu, Richard
Saarman, Norah P.
Attardo, Geoffrey M.
Onyango, Maria
Abd-Alla, Adly M. M.
Aksoy, Serap
author_sort Son, Jae Hak
collection PubMed
description Tsetse flies (Glossina spp.) house a population-dependent assortment of microorganisms that can include pathogenic African trypanosomes and maternally transmitted endosymbiotic bacteria, the latter of which mediate numerous aspects of their host’s metabolic, reproductive, and immune physiologies. One of these endosymbionts, Spiroplasma, was recently discovered to reside within multiple tissues of field captured and laboratory colonized tsetse flies grouped in the Palpalis subgenera. In various arthropods, Spiroplasma induces reproductive abnormalities and pathogen protective phenotypes. In tsetse, Spiroplasma infections also induce a protective phenotype by enhancing the fly’s resistance to infection with trypanosomes. However, the potential impact of Spiroplasma on tsetse’s viviparous reproductive physiology remains unknown. Herein we employed high-throughput RNA sequencing and laboratory-based functional assays to better characterize the association between Spiroplasma and the metabolic and reproductive physiologies of G. fuscipes fuscipes (Gff), a prominent vector of human disease. Using field-captured Gff, we discovered that Spiroplasma infection induces changes of sex-biased gene expression in reproductive tissues that may be critical for tsetse’s reproductive fitness. Using a Gff lab line composed of individuals heterogeneously infected with Spiroplasma, we observed that the bacterium and tsetse host compete for finite nutrients, which negatively impact female fecundity by increasing the length of intrauterine larval development. Additionally, we found that when males are infected with Spiroplasma, the motility of their sperm is compromised following transfer to the female spermatheca. As such, Spiroplasma infections appear to adversely impact male reproductive fitness by decreasing the competitiveness of their sperm. Finally, we determined that the bacterium is maternally transmitted to intrauterine larva at a high frequency, while paternal transmission was also noted in a small number of matings. Taken together, our findings indicate that Spiroplasma exerts a negative impact on tsetse fecundity, an outcome that could be exploited for reducing tsetse population size and thus disease transmission.
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spelling pubmed-84782292021-09-29 Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis Son, Jae Hak Weiss, Brian L. Schneider, Daniela I. Dera, Kiswend-sida M. Gstöttenmayer, Fabian Opiro, Robert Echodu, Richard Saarman, Norah P. Attardo, Geoffrey M. Onyango, Maria Abd-Alla, Adly M. M. Aksoy, Serap PLoS Pathog Research Article Tsetse flies (Glossina spp.) house a population-dependent assortment of microorganisms that can include pathogenic African trypanosomes and maternally transmitted endosymbiotic bacteria, the latter of which mediate numerous aspects of their host’s metabolic, reproductive, and immune physiologies. One of these endosymbionts, Spiroplasma, was recently discovered to reside within multiple tissues of field captured and laboratory colonized tsetse flies grouped in the Palpalis subgenera. In various arthropods, Spiroplasma induces reproductive abnormalities and pathogen protective phenotypes. In tsetse, Spiroplasma infections also induce a protective phenotype by enhancing the fly’s resistance to infection with trypanosomes. However, the potential impact of Spiroplasma on tsetse’s viviparous reproductive physiology remains unknown. Herein we employed high-throughput RNA sequencing and laboratory-based functional assays to better characterize the association between Spiroplasma and the metabolic and reproductive physiologies of G. fuscipes fuscipes (Gff), a prominent vector of human disease. Using field-captured Gff, we discovered that Spiroplasma infection induces changes of sex-biased gene expression in reproductive tissues that may be critical for tsetse’s reproductive fitness. Using a Gff lab line composed of individuals heterogeneously infected with Spiroplasma, we observed that the bacterium and tsetse host compete for finite nutrients, which negatively impact female fecundity by increasing the length of intrauterine larval development. Additionally, we found that when males are infected with Spiroplasma, the motility of their sperm is compromised following transfer to the female spermatheca. As such, Spiroplasma infections appear to adversely impact male reproductive fitness by decreasing the competitiveness of their sperm. Finally, we determined that the bacterium is maternally transmitted to intrauterine larva at a high frequency, while paternal transmission was also noted in a small number of matings. Taken together, our findings indicate that Spiroplasma exerts a negative impact on tsetse fecundity, an outcome that could be exploited for reducing tsetse population size and thus disease transmission. Public Library of Science 2021-09-16 /pmc/articles/PMC8478229/ /pubmed/34529715 http://dx.doi.org/10.1371/journal.ppat.1009539 Text en © 2021 Son et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Son, Jae Hak
Weiss, Brian L.
Schneider, Daniela I.
Dera, Kiswend-sida M.
Gstöttenmayer, Fabian
Opiro, Robert
Echodu, Richard
Saarman, Norah P.
Attardo, Geoffrey M.
Onyango, Maria
Abd-Alla, Adly M. M.
Aksoy, Serap
Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
title Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
title_full Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
title_fullStr Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
title_full_unstemmed Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
title_short Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
title_sort infection with endosymbiotic spiroplasma disrupts tsetse (glossina fuscipes fuscipes) metabolic and reproductive homeostasis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8478229/
https://www.ncbi.nlm.nih.gov/pubmed/34529715
http://dx.doi.org/10.1371/journal.ppat.1009539
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