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

dc.contributor.authorSon, Jae Hak
dc.contributor.authorWeiss, Brian L.
dc.contributor.authorSchneider, Daniela I.
dc.contributor.authorDera, Kiswend-sida M.
dc.contributor.authorGstottenmayer, Fabian
dc.contributor.authorOpiro, Robert
dc.contributor.authorEchodu, Richard
dc.contributor.authorSaarman, Norah P.
dc.contributor.authorAttardo, Geoffrey M.
dc.contributor.authorOnyango, Maria
dc.contributor.authorAbd-Alla, Adly M. M.
dc.contributor.authorAksoy, Serap
dc.date.accessioned2022-11-20T09:26:13Z
dc.date.available2022-11-20T09:26:13Z
dc.date.issued2021
dc.description.abstractTsetse 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.en_US
dc.identifier.citationSon JH, Weiss BL, Schneider DI, Dera KsM, Gsto¨ttenmayer F, Opiro R, et al. (2021) Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis. PLoS Pathog 17(9): e1009539. https://doi.org/10.1371/journal. ppat.1009539en_US
dc.identifier.urihttps://doi.org/10.1371/journal. ppat.1009539
dc.identifier.urihttps://nru.uncst.go.ug/handle/123456789/5350
dc.language.isoenen_US
dc.publisherPLoS pathogensen_US
dc.subjectInfectionen_US
dc.subjectEndosymbiotic Spiroplasmaen_US
dc.subjectTsetse (Glossina fuscipes fuscipes) metabolicen_US
dc.subjectReproductive homeostasisen_US
dc.titleInfection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasisen_US
dc.typeArticleen_US
Files
Original bundle
Now showing 1 - 1 of 1
Loading...
Thumbnail Image
Name:
Infection with endosymbiotic Spiroplasma.pdf
Size:
1.92 MB
Format:
Adobe Portable Document Format
Description:
Article
License bundle
Now showing 1 - 1 of 1
No Thumbnail Available
Name:
license.txt
Size:
1.71 KB
Format:
Item-specific license agreed upon to submission
Description: