Infection with endosymbioticSpiroplasmadisrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
Authors: Son Jae Hak , Weiss Brian L. , Schneider Daniela I. , Dera Kisweda-sida M. , Gstöttenmayer Fabian , Opiro Robert , Echodu Richard , Saarman Norah P. , Attardo Geoffrey M. , Onyango Maria , Abdalla Adly M.M. , Aksoy Serap 
Published: April 2021

Tsetse flies (Glossinaspp.) 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,Spiroplasmainduces reproductive abnormalities and pathogen protective phenotypes. In tsetse,Spiroplasmainfections also induce a protective phenotype by enhancing the fly’s resistance to infection with trypanosomes. However, the potential impact ofSpiroplasmaon tsetse’s viviparous reproductive physiology remains unknown. Herein we employed high-throughput RNA sequencing and laboratory-based functional assays to better characterize the association betweenSpiroplasmaand the metabolic and reproductive physiologies ofG. fuscipes fuscipes(Gff), a prominent vector of human disease. Using field-capturedGff, we discovered thatSpiroplasmainfection induces changes of sex-biased gene expression in reproductive tissues that may be critical for tsetse’s reproductive fitness. Using aGffline composed of individuals heterogeneously infected withSpiroplasma, 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 withSpiroplasma, the motility of their sperm is compromised following transfer to the female spermatheca. As such,Spiroplasmainfections 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 thatSpiroplasmaexerts a negative impact on tsetse fecundity, an outcome that could be exploited for reducing tsetse population size and thus disease transmission.

Author Summary

Endosymbiotic bacteria regulate numerous aspects of their host’s reproductive physiology. Natural populations of the tsetse fly,Glossina fuscipes fuscipes(Gff), house heterogeneous infections with the bacteriumSpiroplasma glossinidia. Infection with the bacterium results in the presentation of several phenotypes in both male and femaleGffthat would put them at a significant reproductive disadvantage when compared to their counterparts that do not house the bacterium. TheseSpiroplasmainduced phenotypes include changes in sex–biased gene expression in the reproductive organs, a depletion in the availability of metabolically critical lipids in pregnant females that results in delayed larval development, and compromised sperm fitness. These findings indicate thatSpiroplasmaexerts an overall negative impact on both male and female reproductive fitness and thus likely has a profound effect on fly population structure. This outcome, in conjunction with the fact thatSpiroplasmainfected tsetse are unusually refractory to infection with pathogenic African trypanosomes, indicates that the bacterium could be experimentally exploited to reduce disease transmission through the fly.