The Obligate Mutualist Wigglesworthia glossinidia Influences Reproduction, Digestion, and Immunity Processes of Its Host, the Tsetse Fly

Abstract

Tsetse flies (Diptera: Glossinidae) are vectors for trypanosome parasites, the agents of the deadly sleeping sickness disease in Africa. Tsetse also harbor two maternally transmitted enteric mutualist endosymbionts: the primary intracellular obligate Wigglesworthia glossinidia and the secondary commensal Sodalis glossinidius. Both endosymbionts are transmitted to the intrauterine progeny through the milk gland secretions of the viviparous female. We administered various antibiotics either continuously by per os supplementation of the host blood meal diet or discretely by hemocoelic injections into fertile females in an effort to selectively eliminate the symbionts to study their individual functions. A symbiont-specific PCR amplification assay and fluorescence in situ hybridization analysis were used to evaluate symbiont infection outcomes. Tetracycline and rifampin treatments eliminated all tsetse symbionts but reduced the fecundity of the treated females. Ampicillin treatments did not affect the intracellular Wigglesworthia localized in the bacteriome organ and retained female fecundity. The resulting progeny of ampicillin-treated females, however, lacked Wigglesworthia but still harbored the commensal Sodalis. Our results confirm the presence of two physiologically distinct Wigglesworthia populations: the bacteriome-localized Wigglesworthia involved with nutritional symbiosis and free-living Wigglesworthia in the milk gland organ responsible for maternal transmission to the progeny. We evaluated the reproductive fitness, longevity, digestion, and vectorial competence of flies that were devoid of Wigglesworthia. The absence of Wigglesworthia completely abolished the fertility of females but not that of males. Both the male and female Wigglesworthia-free adult progeny displayed longevity costs and were significantly compromised in their blood meal digestion ability. Finally, while the vectorial competence of the young newly hatched adults without Wigglesworthia was comparable to that of their wild-type counterparts, older flies displayed higher susceptibility to trypanosome infections, indicating a role for the mutualistic symbiosis in host immunobiology. The ability to rear adult tsetse that lack the obligate Wigglesworthia endosymbionts will now enable functional investigations into this ancient symbiosis.

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

“…Recent evidence is mounting that the transmission of vector‐borne pathogens can be inhibited by other vector‐associated microbes (Sinkins, 2013). In the past decade, studies have shown that certain microbes associated with insect vectors could be used to mediate the transmission of diseases including those transmitted by mosquitoes (Capone et al., 2013; Cirimotich et al., 2011; Dong, Manfredini, & Dimopoulos, 2009; Mourya, Pidiyar, Patole, Gokhale, & Shouche, 2002; Ramirez et al., 2014; Tchioffo et al., 2013; Xi, Ramirez, & Dimopoulos, 2008), tsetse flies (Pais, Lohs, Wu, Wang, & Aksoy, 2008; Wang, Wu, Yang, & Aksoy, 2009; Weiss, Wang, Maltz, Wu, & Aksoy, 2013), sand flies (Sant'Anna et al., 2014), and ticks (Gall et al., 2016; Narasimhan et al., 2014). The most striking example is the inhibition by bacterium Wolbachia pipientis of virus and parasite infection in mosquito vectors (Bian, Xu, Lu, Xie, & Xi, 2010; Blagrove, Arias‐Goeta, Di Genua, Failloux, & Sinkins, 2013; Frentiu et al., 2014; van den Hurk et al., 2012; Hussain et al., 2012; Moreira et al., 2009).…”

Bacterial symbionts in insects or the story of communities affecting communities

“…Removing Wigglesworthia symbionts in tse-tse flies makes them more susceptible to trypanosome infection [18]. Recent investigations suggest that the interaction is mediated by a host peptidoglycan recognition protein that is involved both in host immune tolerance to the obligate symbiont and in the trypanosome infection process [19].…”

Antimicrobial peptides and cell processes tracking endosymbiont dynamics

“…Particularly frequent in species thriving on nutritionally unbalanced environments, such endosymbioses are believed to impact several aspects of host biology, including physiology, immunity and reproduction [2][3][4][5][6][7][8]. They ensure a nutritional complementation of the host diet by providing vitamins and essential amino acids [3,7,9,10], thus greatly improving host fitness [2,3,7,11,12].…”