Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
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Date
2021
Journal Title
Journal ISSN
Volume Title
Publisher
PLoS pathogens
Abstract
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.
Description
Keywords
Infection, Endosymbiotic Spiroplasma, Tsetse (Glossina fuscipes fuscipes) metabolic, Reproductive homeostasis
Citation
Son 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.1009539