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

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.

On the genetic basis of the effect of Spiroplasma on the male reproductive fitness of Glossina fuscipes fuscipes

“…Notably, the amino acid residues encoded by the first exon of Sdic , which is conserved across all Sdic paralogs and unique to Sdic –therefore absent from sw –[ 5 ], are also lacking in the presumed Sdic proteins from the Glossina species. Collectively, these results strongly suggest that Son and colleagues [ 1 ] misidentified the ortholog to sw as the ortholog to Sdic , following the existing annotation in Vector Base.…”

“…Son and colleagues recently reported [ 1 ] the phenotypic effects of the infection of the endosymbiont Spiroplasma in the tsetse fly Glossina fuscipes fuscipes , a major disease vector in humans. The authors examined the impact of Spiroplasma on the reproductive biology of G .…”

“…f . fuscipes [ 1 ]. In relation to male reproductive fitness, the transcript of the putative ortholog to Sdic , as assumed by the authors [ 1 ]–here shown to be actually sw –, is particularly abundant in the spermathecae of females that mated with males free of Spiroplasma compared to equivalent matings involving infected males.…”

“…fuscipes [ 1 ]. In relation to male reproductive fitness, the transcript of the putative ortholog to Sdic , as assumed by the authors [ 1 ]–here shown to be actually sw –, is particularly abundant in the spermathecae of females that mated with males free of Spiroplasma compared to equivalent matings involving infected males. In stark contrast, no differences in expression levels for the putative ortholog to Sdic were found in the male reproductive tract of infected versus noninfected males.…”

Interactions between Glossina pallidipes Salivary Gland Hypertrophy Virus and tsetse endosymbionts in wild tsetse populations

“…Tsetse ies (Glossina spp.) accommodate various types of bacteria, including two gut-associated bacterial symbionts, the obligate Wigglesworthia glossinidia, and the commensal Sodalis glossinidius, the widespread symbiont Wolbachia pipientis, and a recently discovered Spiroplasma endosymbiont [7][8][9][10][11][12][13]. In addition, tsetse ies can house different types of viral infection, including the salivary gland hypertrophy virus (GpSGHV), i avirus, and negevirus, besides trypanosome parasites [14][15][16][17].…”